Pressure during compaction of morsellised bone gives an increase in stiffness: an in vitro study

Morsellised bone impaction is used in joint prosthesis revision surgery to repair structural damage to the periarticular bone stock. The initial stiffness of the impacted bone is crucial for the survival of the revised hip joint. Impaction of morsellised bone in a femoral canal can cause fractures that may induce implant loosening in both femur and acetabulum. Alternative techniques to increase stiffness can therefore be of major interest. In this study we analyse whether applying a constant pressure during impaction can increase the stiffness of the morsellised bone. We constructed bone pellets by impaction with and without applying a constant pressure. The constrained stiffness and coefficient of secondary strain were determined by unidirectional load testing after construction of the pellets. A significant increase in constrained stiffness (P < 0.001) from 3.9 to 5.5 MPa and a decrease in the coefficient of secondary strain (P < 0.001) from 1.1 to 0.5 were found.     

Viscoelastic modelling of impacted morsellised bone accurately describes unloading behaviour: an experimental study of stiffness moduli and recoil properties

Morsellised bone impaction grafting is commonly used for revision arthroplasty surgery. Several reports have described the mechanical behaviour of this bone material during impaction and loading. In this study we observed the unloading progress. The loose morsellised bone was modified by particle size, particle size distribution, water and fat content. Bone pellets were constructed using different impaction energies. After impaction, the pellets were loaded statically, after which their swelling was recorded at three unloading levels. We deduced two time-dependent recoil properties, the time resistant number (TRN) and the half total swelling time (HTST), and also one stiffness property, the unloading confined modulus of elasticity (UCME). In impacted morsellised bone, the progress of swelling is visco-elastic. Bone pellets with an even distribution of particle sizes have the most rapid recoil. Those with a high liquid content recoil more slowly, and to a significantly greater extent, than pellets with low liquid content. The recoil of pellets with low liquid content is instantaneous, i.e. unrecordable, and the displacement is significantly less than in other pellet samples.     

In vivo tibial stiffness is maintained by whole bone morphology and cross-sectional geometry in growing female mice

Whole bone morphology, cortical geometry, and tissue material properties modulate skeletal stresses and strains that in turn influence skeletal physiology and remodeling. Understanding how bone stiffness, the relationship between applied load and tissue strain, is regulated by developmental changes in bone structure and tissue material properties is important in implementing biophysical strategies for promoting healthy bone growth and preventing bone loss. The goal of this study was to relate developmental patterns of in vivo whole bone stiffness to whole bone morphology, cross-sectional geometry, and tissue properties using a mouse axial loading model. We measured in vivo tibial stiffness in three age groups (6, 10, 16 wk old) of female C57Bl/6 mice during cyclic tibial compression. Tibial stiffness was then related to cortical geometry, longitudinal bone curvature, and tissue mineral density using microcomputed tomography (microCT). Tibial stiffness and the stresses induced by axial compression were generally maintained from 6 to 16 wks of age. Growth-related increases in cortical cross-sectional geometry and longitudinal bone curvature had counteracting effects on induced bone stresses and, therefore, maintained tibial stiffness similarly with growth. Tissue mineral density increased slightly from 6 to 16 wks of age, and although the effects of this increase on tibial stiffness were not directly measured, its role in the modulation of whole bone stiffness was likely minor over the age range examined. Thus, whole bone morphology, as characterized by longitudinal curvature, along with cortical geometry, plays an important role in modulating bone stiffness during development and should be considered when evaluating and designing in vivo loading studies and biophysical skeletal therapies.     

Particle size influence in an impaction bone grafting model. Comparison of fresh-frozen and freeze-dried allografts

BackgroundImpaction bone grafting with large particles is considered as mechanically superior to smaller morsels. Interest of freeze-dried irradiated bone for impaction bone grafting has been observed with small particles. Influence of bone process on other particle sizes still needed to be assessed.Material and methodsTwenty-four osteoarthrotic femoral heads were used to prepare fresh-frozen and freeze-dried irradiated cancellous bone. Each group was divided into four batches of different particle sizes, each batch containing 18 samples. The different particle sizes were obtained with a Retsch Cross Beater Mill SK 100, Noviomagus rotating bone mills with two sizes of rasps and a Luer bone rongeur. Bone grafts were impacted in a contained cylinder. Stiffness was monitored during impaction.ResultsFreeze-dried irradiated grafts showed higher stiffness than fresh-frozen bone whatever the size of the particles. Large particles obtained with the rongeur and the large rasp from the Noviomagus bone mill were mechanically superior than small particles up to 30 impactions.InterpretationLarge particles offer better mechanical performance as a greater magnitude of force would be required to deform and break the particles. Freeze-dried irradiated bone brittleness reduces this advantage after 30 impactions. Large particles embrittlement leads to similar mechanical results as small particles at higher impaction rate. This may account for partial collapse of the graft layer in clinical situation when impaction rate is lower. This model supports the use of small particles obtained with thin rasp bone mill when freeze-dried irradiated bone for impaction bone grafting and large particles obtained with the Rongeur when fresh-frozen bone is available.     

A laboratory simulation for morselized bone graft fusion: apparent modulus under operatively based femoral impaction kinetics

The purpose of this study was to determine the apparent modulus changes accompanying a novel procedure for simulating in situ fusion of morselized cancellous bone femoral impaction grafts. An experienced surgeon's habitual intra-operative impaction grafting protocol was first quantified in human cadaver femurs, using a customized impulse force hammer. A corresponding standardized impaction procedure was then defined, and was used to prepare impaction grafts in axisymmetric metallic fixturing designed to replicate the nominal geometry of femoral canal confinement. Impaction graft fusion was simulated by mixing morselized cancellous bone with an amine-based epoxy adhesive before the impaction, then allowing the mixture to fuse after the impaction (J. Biomech. 34 (2001) 811). Force/deflection behavior of the unfused and fused impaction grafts was measured for both the (tapered) proximal and (untapered) distal portions of the grafts. Apparent modulus was then calculated from force/deflection stiffness. The impaction graft fusion simulation increased apparent modulus by an order of magnitude over the unfused state, for mixture parameters appropriate to have the fused graft apparent modulus be comparable to the compressive modulus of intact femoral cancellous bone.     

Altered tissue properties induce changes in cancellous bone architecture in aging and diseases

The mechanical properties of cancellous bone depend on its architecture and the tissue properties of the mineralized matrix. The architecture is continuously adapted to external loads. In this paper, it was assumed that changes in tissue properties leading to changes in tissue deformation can induce adaptation of the architecture. We asked whether changes in cancellous bone architecture with aging and in e.g. early osteoarthrosis can be explained from changes in tissue properties.This was investigated using computer models in which the cancellous architecture was adapted to external loads. Bone tissue with deformations below a certain threshold was resorbed, deformations above another threshold induced formation. Deformations between these two boundaries, in the 'lazy zone', did not induce bone adaptation. The effects of changes in bone tissue stiffness on bone mass, global stiffness and architecture were investigated. The bone gain (40-60%) resulting from a 50% decrease in tissue stiffness (simulating diseased tissue) was much larger than the bone loss (2-30%) resulting from a 50% increase in tissue stiffness (simulating highly mineralized, old tissue). The adaptation induced by a decrease in tissue stiffness resulted in an almost constant stiffness in the main load bearing direction, but the transversal stiffness decreased. An increased tissue stiffness resulted in a higher stiffness in the main direction and overcompensation in the transversal directions: the global stiffness could become even smaller than the stiffness of the original model. Concluding, we showed that changes in trabecular bone in aging and diseases can be partly explained from changes in tissue properties.     

Stiffening of the femoral head due to inter-trabecular fluid and intraosseous pressure

The mechanical properties of cancellous bone, as measured from bone plug samples have been widely documented. However, few tests have been attempted to explore the effects the intertrabecular contents may have on the load bearing capabilities. In this study, canine femoral heads were subjected to dynamic compressive strain cycles. The femoral heads were tested intact, as well as with disrupted boundary conditions of the continuous, intraosseous fluid space. A significant reduction in mechanical stiffness was observed when the fluid compartment boundary was disrupted by drilling a hole part way into the femoral neck. A finite element model of a typical femoral head showed that the stiffness change was not due to removal of material from the neck, hydraulic effects notwithstanding. Refilling the hole in the neck with saline solution and sealing the boundary restored the stiffness to the intact baseline level. However, an increase in the fluid pressure did not cause a statistically significant increase in the stiffness of the femoral head.     

On the applicability of bovine morsellized cortico-cancellous bone as a substitute for human morsellized cortico-cancellous bone for in vitro mechanical testing

Morsellized cortico-cancellous bone (MCB) is frequently used in orthopaedic revision surgery to restore lost bone stock. In this study, we examine the validity of using bovine MCB as a substitute for human MCB in in vitro mechanical testing of bone grafts. The paper describes the fat and water content of impacted and unimpacted human and bovine MCB. During this work we applied constrained compression testing to describe the elastic, plastic and time dependent response. Nearly all parameters were found to be significantly different and were influenced differently by impaction for the two types of MCB. The denser trabecular structure, higher fat content of bovine MCB and higher stiffness and compressive strength of cortical bovine bone may explain the differences observed. Consequently we are not confident about the applicability of bovine MCB as a substitute for human MCB for in vitro mechanical testing.     

A study on bone induction in hydroxyapatite combined with bone morphogenetic protein.

Our present study consisted of an implantation of artificially made hydroxyapatite (HAP) ceramic pellets under the periosteum of the rabbit skull with subsequent inspection of further progress of bone formation and also of an evaluation of the effects of bone morphogenetic protein (BMP). The results revealed that the alkali phosphatase (AL-P) activity of the pellets was elevated only in those of the bone morphogenetic protein group. The results of determination of bone mineral density at the site of the pellets revealed that the increase in bone mineral density was the most remarkable in the bone morphogenetic protein group rather than the control group. The results of the histopathologic examinations revealed that marginal bone formation was found in the pores on the surface between the pellets and the skull in the control group and in the collagen group, whereas in the bone morphogenetic protein group very active bone formation was found not only on the interface in contact with the skull but also surrounding the whole pellet. It also was noted in the animals in the bone morphogenetic protein group that the pellets were corrupted from the peripheries and then absorbed into the newly formed bone. From these results, the efficacy of the hydroxyapatite-collagen-bone morphogenetic protein complex was made clear, and applications in clinical practice are expected in the near future.     

The elastic properties of morsellised cortico-cancellous bone graft are dependent on its prior loading

Confined compression experiments were carried out on cortico-cancellous bone taken from bovine femoral condyles to assess the effect of prior loading on the elastic confined modulus, E(c) of morsellised cortico-cancellous bone (MCB). Measurements were taken to find the values of E(c) for MCB subjected to cyclic loading resulting in axial stresses in the range of 0.5-3.0 N mm(2). Two values of E(c) were considered: E(ic), the instantaneous modulus, and E(dc), the delayed modulus allowing for stress relaxation effects. It was found that the values of E(c) increased with increasing maximum axial stress. It was also found that for each stress level the values of E(c) increased as the number of load cycles increased. The dependence of E(c) on the maximum axial stress and the number of load cycles is seen to explain the wide range of values for the apparent modulus of MCB found in previous studies. Tests examining the stress relaxation behaviour of MCB are also discussed. The results indicate that a minimum of 10 compaction episodes are required for MCB to achieve around 90% of its predicted maximum stiffness for a given compaction force.     

Predicting the structural integrity of bone defects repaired using bone graft materials

Bone defects create stress concentrations which can cause fracture under impact or cyclic loading. Defects are often repaired by filling them with a bone graft material; this will reduce the stress concentration, but not completely, because these materials have lower stiffness than bone. The fracture risk decreases over time as the graft material is replaced by living bone. Many new bone graft materials are being developed, using tissue engineering and other techniques, but currently there is no rational way to compare these materials and predict their effectiveness in repairing a given defect. This paper describes, for the first time, a theoretical model which can be used to predict failure by brittle fracture or fatigue, initiating at the defect. Preliminary results are presented, concentrating on the prediction of stress fracture during the crucial post-operative period. It is shown that the likelihood of fracture is strongly influenced by the shape of the defect as well as its size, and also by the level of post-operative exercise. The most important finding is that bone graft materials can be successful in preventing fracture even when their mechanical properties are greatly inferior to those of bone. Future uses of this technique include pre-clinical assessment of bone replacement materials and pre-operative planning in orthopaedic surgery.     

Age-dependent fatigue behaviour of human cortical bone

Despite a general understanding that bone quality contributes to skeletal fragility, very little information exits on the age-dependent fatigue behavior of human bone. In this study four-point bending fatigue tests were conducted on aging bone in conjunction with the analysis of stiffness loss and preliminary investigation of nanoindentation based measurements of local tissue stiffness and histological evaluation of resultant tensile and compressive damage to identify the damage mechanism responsible for the increase in age-related bone fragility. The results obtained show that there is an exponential decrease in fatigue life with age, and old bone exhibits different modulus degradation profiles than young bone. In addition, this study provides preliminary evidence indicating that during fatigue loading, younger bone formed diffuse damage, lost local tissue stiffness on the tensile side. Older bone, in contrast, formed linear microcracks lost local tissue stiffness on the compressive side. Thus, the propensity of aging human bone to form more linear microcracks than diffuse damage may be a significant contributor to bone quality, and age related fragility in bone.     

Predicting the structural integrity of bone defects repaired using bone graft materials

Bone defects create stress concentrations which can cause fracture under impact or cyclic loading. Defects are often repaired by filling them with a bone graft material; this will reduce the stress concentration, but not completely, because these materials have lower stiffness than bone. The fracture risk decreases over time as the graft material is replaced by living bone. Many new bone graft materials are being developed, using tissue engineering and other techniques, but currently there is no rational way to compare these materials and predict their effectiveness in repairing a given defect. This paper describes, for the first time, a theoretical model which can be used to predict failure by brittle fracture or fatigue, initiating at the defect. Preliminary results are presented, concentrating on the prediction of stress fracture during the crucial post-operative period. It is shown that the likelihood of fracture is strongly influenced by the shape of the defect as well as its size, and also by the level of post-operative exercise. The most important finding is that bone graft materials can be successful in preventing fracture even when their mechanical properties are greatly inferior to those of bone. Future uses of this technique include pre-clinical assessment of bone replacement materials and pre-operative planning in orthopaedic surgery.     

The dependence of the elastic properties of osteoporotic cancellous bone on volume fraction and fabric

Osteoporosis is a progressive systemic skeletal condition characterized by low bone mass and microarchitectural deterioration, with a consequent increase in susceptibility to fracture. Hence, osteoporosis would be best diagnosed by in vivo measurements of bone strength. As this is not clinically feasible, our goal is to estimate bone strength through the assessment of elastic properties, which are highly correlated to strength. Previously established relations between morphological parameters (volume fraction and fabric) and elastic constants could be applied to estimate cancellous bone stiffness in vivo. However, these relations were determined for normal cancellous bone. Cancellous bone from osteoporotic patients may require different relations. In this study we set out to answer two questions. First, can the elastic properties of osteoporotic cancellous bone be estimated from morphological parameters? Second, do the relations between morphological parameters and elastic constants, determined for normal bone, apply to osteoporotic bone as well? To answer these questions we used cancellous bone cubes from femoral heads of patients with (n=26) and without (n=32) hip fractures. The elastic properties of the cubes were determined using micro-finite element analysis, assuming equal tissue moduli for all specimens. The morphological parameters were determined using microcomputed tomography. Our results showed that, for equal tissue properties, the elastic properties of cancellous bone from fracture patients could indeed be estimated from morphological parameters. The morphology-based relations used to estimate the elastic properties of cancellous bone are not different for women with or without fractures.     

Fatigue of immature baboon cortical bone

Strain-controlled uniaxial fatigue and monotonic tensile tests were conducted on turned femoral cortical bone specimens obtained from baboons at various ages of maturity. Fatigue loading produced a progressive loss in stiffness and an increase in hysteresis prior to failure, indicating that immature primate cortical bone responds to repeated loading in a fashion similar to that previously observed for adult human cortical bone. Bone fatigue resistance under this strain controlled testing decreased during maturation. Maturation was also associated with an increase in bone dry density, ash fraction and elastic modulus. The higher elastic modulus of more mature bone meant that these specimens were subjected to higher stress levels during testing than more immature bone specimens. Anatomical regions along the femoral shaft exhibited differences in strength and fatigue resistance.     

The effect of constraint on the mechanical behaviour of trabecular bone specimens

The effect of the boundary conditions between trabecular bone specimens and the test columns of the testing machine was studied together with the effect of side-constraint on the mechanical behaviour of trabecular bone during axial compression. Cylindrical specimens taken from the upper tibial epiphysis of autopsy knees were tested non-destructively by cyclic compression to 0.8% strain under different conditions. Fixation of the specimens to the test columns by a thin layer of bone cement increased the stiffness by 40% and reduced the energy dissipation to 67% of those measured under unconstrained conditions (p less than 0.001). The thin cement layer alone increased the stiffness 19% and reduced energy dissipation to 86% (n.s.). When the machine was equipped with polished steel columns coated by a film of low-viscous oil, both the stiffness and the energy dissipation were reduced to 93% of those measured under standard conditions (p less than 0.005). Trabecular bone specimens tested side-constrained by the surrounding trabecular bone (in situ) showed a 19% larger stiffness than that measured during later testing of the corresponding machined specimens (p less than 0.005) whereas the energy dissipation was not altered significantly. The same specimens showed a 22% increase of stiffness and a 68% increase of energy dissipation when they were side-constrained by a closely fitting steel cylinder (p less than 0.005).     

Comparison of the linear finite element prediction of deformation and strain of human cancellous bone to 3D digital volume correlation measurements

The mechanical properties of cancellous bone and the biological response of the tissue to mechanical loading are related to deformation and strain in the trabeculae during function. Due to the small size of trabeculae, their motion is difficult to measure. To avoid the need to measure trabecular motions during loading the finite element method has been used to estimate trabecular level mechanical deformation. This analytical approach has been empirically successful in that the analytical models are solvable and their results correlate with the macroscopically measured stiffness and strength of bones. The present work is a direct comparison of finite element predictions to measurements of the deformation and strain at near trabecular level. Using the method of digital volume correlation, we measured the deformation and calculated the strain at a resolution approaching the trabecular level for cancellous bone specimens loaded in uniaxial compression. Smoothed results from linearly elastic finite element models of the same mechanical tests were correlated to the empirical three-dimensional (3D) deformation in the direction of loading with a coefficient of determination as high as 97% and a slope of the prediction near one. However, real deformations in the directions perpendicular to the loading direction were not as well predicted by the analytical models. Our results show, that the finite element modeling of the internal deformation and strain in cancellous bone can be accurate in one direction but that this does not ensure accuracy for all deformations and strains.     

Derivation of the mesoscopic elasticity tensor of cortical bone from quantitative impedance images at the micron scale

This paper addresses the relationships between the microscopic properties of bone and its elasticity at the millimetre scale, or mesoscale. A method is proposed to estimate the mesoscale properties of cortical bone based on a spatial distribution of acoustic properties at the microscopic scale obtained with scanning acoustic microscopy. The procedure to compute the mesoscopic stiffness tensor involves (i) the segmentation of the pores to obtain a realistic model of the porosity; (ii) the construction of a field of anisotropic elastic coefficients at the microscopic scale which reflects the heterogeneity of the bone matrix; (iii) finite element computations of mesoscopic homogenized properties. The computed mesoscopic properties compare well with available experimental data. It appears that the tissue anisotropy at the microscopic level has a major effect on the mesoscopic anisotropy and that assuming the pores filled with an incompressible fluid or, alternatively, empty, leads to significantly different mesoscopic properties.     

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.     

The effect of resorption cavities on bone stiffness is site dependent

Resorption cavities formed during the bone remodelling cycle change the structure and thus the mechanical properties of trabecular bone. We tested the hypotheses that bone stiffness loss due to resorption cavities depends on anatomical location, and that for identical eroded bone volumes, cavities would cause more stiffness loss than homogeneous erosion. For this purpose, we used beam–shell finite element models. This new approach was validated against voxel-based FE models. We found an excellent agreement for the elastic stiffness behaviour of individual trabeculae in axial compression (R² = 1.00) and in bending (R²>0.98), as well as for entire trabecular bone samples to which resorption cavities were digitally added (R² = 0.96, RMSE = 5.2%). After validation, this new method was used to model discrete cavities, with dimensions taken from a statistical distribution, on a dataset of 120 trabecular bone samples from three anatomical sites (4th lumbar vertebra, femoral head, iliac crest). Resorption cavities led to significant reductions in bone stiffness. The largest stiffness loss was found for samples from the 4th lumbar vertebra, the lowest for femoral head samples. For all anatomical sites, resorption cavities caused significantly more stiffness loss than homogeneous erosion did. This novel technique can be used further to evaluate the impact of resorption cavities, which are known to change in several metabolic bone diseases and due to treatment, on bone competence.