The relationship of weathering cracks to split-line orientation in bone

The essential identity of weathering cracks and split-lines is demonstrated experimentally. Innominate bones, left in the open to weather, developed cracks similar to the split-line orientation typically observed in the same region. These bones were decalcified and intermittent split-lines prepared along their course. The orientation of the split-lines always corresponds to the weathering splits. The same results were obtained with bird and mammal bones collected in the field and showing weathering cracks. The same also applies to cracks in bones of a gorilla which had been partly defleshed and salted down for preservation. Apparently any process which shrinks bone will produce cracks with the same orientation as split-lines. Possibilities for split-line analysis of fossil and archeological bone are opened up by these experiments.     

The split-line phenomenon and the microscopic structure of bone

This investigation was undertaken to study the relation of split-lines to the microscopic structure of cortical bone by means of microradiography and conventional histologic staining techniques. The results indicate that the feature of bone structure that determines the production and orientation of split-lines is the disposition of collagenous fibers, whether the bone organization is Haversian (osteone-containing) or not. Differences of opinion in the literature concerning the “causation” of split-lines appear to stem from a failure to distinguish between the morphologic and functional aspects of the problem.     

Two orinetational features of compact bone as predictors of split-line patterns

Ways of determining orientation patterns in compact bone are needed for specimens which are not available for split-line analysis. Weathering cracks have been shown to be essentially identical in orientation to split-lines, but they are more often than not absent or very few in number. Two other features of compact bone which promise to extend the range of orientational analysis are illustrated and described. These are (1) red or brown lines near the surface, and (2) numerous light-colored filaments, at or near the surface, laid parallel to each other. The latter manifestation has been observed more frequently and usually gives a more complete picture of orientational patterns. Specimens showing the two indicators were decalcified and processed for split-line patterns, which were essentially identical to the indicators in orientation. The first type of indicator is shown microscopically to be a manifestation of resorption spaces and immature osteons containing coagulated blood. The second represents oriented mature osteons in monkey pelves, but the microscopic basis in a cat pelvic bone is not clear.     

The relationship between split-line orientation and in vivo bone strain in galago (G. crassicaudatus) and macaque (Macaca mulatta and M. fascicularis) Mandibles

There is still disagreement concerning the functional significance of split-line patterns in bone. This study was undertaken to reexamine the mechanical forces hypothesis for split-line formation by comparing split-line patterns with in vivo mandibular bone strain patterns. The relationship between split-line orientation and in vivo stress and strain patterns on macaque and galago mandibles was examined during jaw opening and the power stroke of mastication and incision. An attempt was made to relate split-line orientation to the direction of tensile stress and strain along the primate mandible. In addition, we also investigated the alternative possibility that split-line orientation is related to the direction of low stresses (and strains) on the primate mandible. The results of this study showed that there was no consistent relationship between split-line orientation and the principal strains or stresses. Thus, split-lines did not run consistently in the direction of high or low stress and strain. Therefore, we have concluded that split-line orientation provides little useful information for inferring patterns of stress and strain in bone.     

Propagation of surface fatigue cracks in human cortical bone

An understanding of how fatigue cracks grow in bone is of importance as fatigue is thought to be the main cause of clinical stress fractures. This study presents new results on the fatigue-crack growth behavior of small surface cracks (approximately 75-1000 microm in size) in human cortical bone, and compares their growth rates with data from other published studies on the behavior of both surface cracks and many millimeter, through-thickness large cracks. Results are obtained with a cyclically loaded cantilever-beam geometry using optical microscopy to examine for crack growth after every 100-500 cycles. Based on the current and previous results, small fatigue cracks appear to become more resistant to fatigue-crack growth with crack extension, analogous to the way the fracture resistance of cortical bone increases with crack growth. Mechanistically, a theory attributing such behavior to the development of bridges in the wake of the crack with crack growth is presented. The existence of such bridges is directly confirmed using optical microscopy.     

Effect of superficial collagen patterns and fibrillation of femoral articular cartilage on knee joint mechanics-a 3D finite element analysis

Collagen fibrils of articular cartilage have specific depth-dependent orientations and the fibrils bend in the cartilage surface to exhibit split-lines. Fibrillation of superficial collagen takes place in osteoarthritis. We aimed to investigate the effect of superficial collagen fibril patterns and collagen fibrillation of cartilage on stresses and strains within a knee joint. A 3D finite element model of a knee joint with cartilage and menisci was constructed based on magnetic resonance imaging. The fibril-reinforced poroviscoelastic material properties with depth-dependent collagen orientations and split-line patterns were included in the model. The effects of joint loading on stresses and strains in cartilage with various split-line patterns and medial collagen fibrillation were simulated under axial impact loading of 1000 N. In the model, the collagen fibrils resisted strains along the split-line directions. This increased also stresses along the split-lines. On the contrary, contact and pore pressures were not affected by split-line patterns. Simulated medial osteoarthritis increased tissue strains in both medial and lateral femoral condyles, and contact and pore pressures in the lateral femoral condyle. This study highlights the importance of the collagen fibril organization, especially that indicated by split-line patterns, for the weight-bearing properties of articular cartilage. Osteoarthritic changes of cartilage in the medial femoral condyle created a possible failure point in the lateral femoral condyle. This study provides further evidence on the importance of the collagen fibril organization for the optimal function of articular cartilage.     

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.     

Microcrack accumulation at different intervals during fatigue testing of compact bone

Fatigue damage in bone occurs in the form of microcracks. This microdamage contributes to the formation of stress fractures and acts as a stimulus for bone remodelling. A technique has been developed, which allows microcrack growth to be monitored during the course of a fatigue test by the application of a series of fluorescent chelating agents. Specimens were taken from bovine tibiae and fatigue tested in cyclic compression at a stress range of 80MPa. The specimens were stained before testing with alizarin and up to three other chelating agents were applied during testing to label microcracks formed at different times. Microcracks initiated in interstitial bone in the early part of a specimen's life. Further accumulation of microcracks is then suppressed until the period late in the specimen's life. Microcracks were found to be longer in the longitudinal than in the transverse direction. Only a small proportion of cracks are actively propagating; these are longer than non-propagating cracks. These results support the concept of a microstructural barrier effect existing in bone, whereby cracks initiate easily but slow down or stop at barriers such as cement lines.     

The pulsed water jet for selective removal of bone cement during revision arthroplasty]

Conventional tools used in prosthetic revision surgery have a limited range of action within the narrow cement mantle. Water jet cutting technology permits tiny and precisely controlled cuts, and may therefore be an alternative method of bone cement removal. Our study compares the cutting performance on bone cement (PMMA) and bone of a pulsed water jet and a continuous water jet. The aim of the study was to establish whether selective removal of PMMA is possible. 55 bone specimens (bovine femora) and 32 specimens of PMMA were cut with a continuous and a pulsed water jet at different pressures (40 MPa, 60 MPa) and pulse frequencies (0Hz, 50Hz, 250Hz). To ensure comparability of the results, the depths of cut were related to the hydraulic power of that part of the jet actually impinging on the material. While for PMMA the power-related depth of cut increased significantly with the pulse frequency, this did not apply to bone. The cuts produced in bone were sharp-edged. Since PMMA is more brittle than bone, the water jet caused cracks that enlarged further until particles of bone broke away. Although selective removal of PMMA without doing damage to the bone was not possible at the investigated settings of the jet parameters, the results do show that a pulsed water jet can cut bone cement much more effectively than bone. This is an important advantage over conventional non-selective tools for the removal of bone cement.     

Stress intensity variations in bone microcracks during the repair process

Microscopic cracks form and grow in compact bone in vivo due to cyclic loading. Their growth can cause stress fractures and has been implicated in the processes of remodelling and adaptation. These cracks are repaired by the actions of BMUs which are mobile resorption cavities. In this work, we studied the interaction between cracks and BMUs by making finite element models representing different stages in the repair process. The tendency of the crack to grow was measured by its stress intensity factor, K. We found that K changes in a complex manner during the repair process, both decreasing and increasing depending on the size of the crack and the type of loading applied. For loading conditions similar to those that exist in vivo, the presence of the BMU can cause K to rise significantly, in some cases by more than 20%, implying a substantial increase in crack growth rate. This information is important for our general understanding of the complexities of the repair process, and especially for the development of theoretical models to simulate damage and repair in bone.     

Normal contact of elastic spheres with two elastic layers as a model of joint articulation.

An analytical model of two elastic spheres with two elastic layers in normal, frictionless contact is developed which simulates contact of articulating joints, and allows for the calculation of stresses and displacements in the layered region of contact. Using various layer/layer/substrate combinations, the effects of variations in layer and substrate properties are determined in relation to the occurrence of tensile and shear stresses as the source of crack initiation in joint cartilage and bone. Vertical cracking at the cartilage surface and horizontal splitting at the tidemark have been observed in joints with primary osteoarthritis. Deep vertical cracks in the calcified cartilage and underlying bone have been observed in blunt trauma experiments. The current model shows that cartilage stresses for a particular system are a function of the ratio of contact radius to total layer thickness (a/h). Surface tension, which is observed for a/h small, is alleviated as a/h is increased due to increased load, softening and/or thinning of the cartilage layer. Decreases in a/h due to cartilage stiffening lead to increased global compressive stresses and increased incidence of surface tension, consistent with impact-induced surface cracks. Cartilage stresses are not significantly affected by variations in stiffness of the underlying material. Tensile radial strains in the cartilage layer approach one-third of the normal compressive strains, and increase significantly with cartilage softening. For cases where the middle layer stiffness exceeds that of the underlying substrate, tensile stresses occur at the base of the middle layer, consistent with impact induced cracks in the zone of calcified cartilage and subchondral bone. The presence of the superficial tangential zone appears to have little effect on underlying cartilage stresses.     

Micro CT-based multiscale elasticity of double-porous (pre-cracked) hydroxyapatite granules for regenerative medicine

Hundred micrometers-sized porous hydroxyapatite globules have proved as a successful tissue engineering strategy for bone defects in vivo, as was shown in studies on human mandibles. These granules need to provide enough porous space for bone ingrowth, while maintaining sufficient mechanical competence (stiffness and strength) in this highly load-bearing organ. This double challenge motivates us to scrutinize more deeply the micro- and nanomechanical characteristics of such globules, as to identify possible optimization routes. Therefore, we imaged such a (pre-cracked) granule in a microCT scanner, transformed the attenuation coefficients into voxel-specific nanoporosities, from which we determined, via polycrystal micromechanics, voxel-specific (heterogeneous) elastic properties. The importance of the latter and of the presence of one to several hundred micrometers-sized cracks for realistically estimating the load-carrying behavior of the globule under a typical two-point compressive loading (as in a "splitting" test) is shown through results of large-scale Finite Element analyses, in comparison to analytical results for a sphere loaded at its poles: Use of homogeneous instead of heterogeneous elastic properties would overestimate the structure's stiffness by 5% (when employing a micromechanics-based process as to attain homogeneous properties)-the cracks, in comparison, weaken the structure by one to two orders of magnitudes.     

Measuring the shape and size of microcracks in bone

Microcracks in bone are normally measured from two-dimensional, transverse sections but this provides incomplete information about their three-dimensional shape and size. The methods of stereology can usefully be applied in such a case. This problem has been addressed using a theoretical model and a numerical simulation. Results show that the data are consistent with a crack shape which is elliptical, with axis ratio approximately 4.5 : 1 and with size variation (expressed as the ratio of standard deviation to mean length) of at least 0.1. Measured lengths will, on average, be smaller and have more scatter than true lengths. Errors caused by omitting small cracks are relatively unimportant. Knowledge of the true crack dimensions, and their variability, is important for the analysis of damage, stress fracture, remodelling and adaptation.     

Microdamage accumulation in the cement layer of hip replacements under flexural loading.

Mechanical fatigue of bone cement leading to damage accumulation is implicated in the loosening of cemented hip components. Even though cracks have been identified in autopsy-retrieved mantles, damage accumulation by continuous growth and increase in number of microcracks has not yet been demonstrated experimentally. To determine just how damage accumulation occurs in the cement layer of a hip replacement, a physical model of the joint was used in an experimental study. The model regenerates the stress pattern found in the cement layers whilst at the same time allowing visualisation of microcrack initiation and growth. In this way the gradual process of damage accumulation can be determined. Six specimens were tested to 5 million cycles and a total of 1373 cracks were observed. It was found that, under the flexural loading allowed by the model, the majority of cracks come from pores in the bulk cement and not from the interfaces. Furthermore, the lateral and medial sides have statistically different damage accumulation behaviours, and pre-load cracks significantly accelerate the damage accumulation process. The experimental results confirm that damage accumulation commences early on in the loading history and that it is continuously increasing with load in the form of crack initiation and crack propagation. The results highlight the importance of replicating the loading and restraint conditions of clinical cement mantles when endeavouring to accurately model the damage accumulation process.     

Subchondral bone failure in overload arthrosis: a scanning electron microscopic study in horses

Mechanical overload leads to a common arthrosis in the metacarpal condyle of the fetlock joint of racehorses. This is usually asymptomatic but severe forms can cause lameness. Subchondral bone failure is often present and the predictability of the site provided an opportunity to study of the progression of bone failure from microcracks to actual collapse of subchondral bone. Twenty-five fetlock condyles from racehorses with various stages of disease were selected. Stages ranged from mild through severe subchondral bone sclerosis, to the collapse of bone and indentation or loss of cartilage known as 'traumatic osteochondrosis'. Parasagittal slices were radiographed and examined with scanning electron microscopy. Fine matrix cracks were seen in the subchondral bone layer above the calcified cartilage and suggested loss of water or other non-collagenous components. The earliest microcracks appeared to develop in the sclerotic bone within 1-3 mm of the calcified cartilage layer and extend parallel to it in irregular branching lines. Longer cracks or microfractures appeared to develop gaps as fragmentation occurred along the margins. Occasional osteoclastic resorption sites along the fracture lines indicated activated remodeling may have caused previous weakening. In one sample, smoothly ground fragments were found in a fracture gap. Bone collapse occurred when there was compaction of the fragmented matrix along the microfracture. Bone collapse and fracture lines through the calcified cartilage were associated with indentation of articular cartilage at the site.     

In vitro interface and cement mantle analysis of different femur stem designs

The aim of this study is to define stem design related factors causing both gaps in the metal-bone cement interface and cracks within the cement mantle. Six different stem designs (Exeter; Lubinus SP II; Ceraver Osteal; Mueller-straight stem; Centega; Spectron EF) (n=15 of each design) were cemented into artificial femur bones. Ten stems of each design were loaded, while five stems served as an unloaded control. Physiologically adapted cyclical loading (DIN ISO 7206-4) was performed with a hip simulator. After loading both interfaces and the bone cement itself were analysed regarding gaps and cracks in the cement mantle. Significant differences between the stem designs concerning gaps in the metal-bone cement interface and cracks in the cement mantle became apparent. Additionally, a high correlation between gaps in the metal-bone cement interface and cracks within the cement mantle could be proven. Gaps in the metal-bone cement interface but no cracks within the cement mantle were seen in the unloaded specimens. Differences between the unloaded control groups and the cyclical loaded stems regarding the longitudinal extension and width of gaps in the metal-bone cement interface were obvious. The designs of cemented femoral stems have an influence on both the quality of the metal-bone cement contact and the failure rate of the cement mantle. Less interface gaps and less cement defects were found with anatomically formed, collared, well-rounded stem designs without undercuttings.     

Measurement of the microstructural fracture toughness of cortical bone using indentation fracture

The purpose of this work is to investigate the use of indentation fracture as a method of measuring toughness at the microscale in cortical bone. Indentation fracture employs sharp indenters to initiate cracks, whose length can be used to calculate the toughness of the material. Only a cube corner indenter tip is found to initiate cracks at a suitable size scale for microstructural measurement. Cracks from 7 to 56 microm in length are produced using loads from 0.05 to 3N. Preliminary data predicts rising toughness with increasing crack length (rising R-curve behaviour) at the microscale. This technique provides a new insight into fracture in cortical bone since it allows the investigator to observe mechanisms and measure toughness at a size scale at which in vivo damage is known to exist.     

Advances in the fracture mechanics of cortical bone

As cortical bone is a semi-brittle solid, its fracture is dependent not only on the magnitude of the applied stress, but also on the nature of any intrinsic or introduced cracks. Consequently a variety of fracture mechanics techniques have been utilised to evaluate the fracture toughness of cortical bone, including the single edge notched, centre notched cylindrical and compact tension methods, and values have been established for the critical stress intensity factor (Kc) and the critical strain energy release rate (Gc). The Kc and Gc values obtained depend on the orientation of the cortical bone, as well as on bone density, the velocity of crack propagation and specimen geometry. The significance of these fracture mechanics parameters for cortical bone is critically reviewed.     

The mechanical effects of different levels of cement penetration at the cement–bone interface

The mechanical effects of varying the depth of cement penetration in the cement–bone interface were investigated using finite element analysis (FEA) and validated using companion experimental data. Two FEA models of the cement–bone interface were created from micro-computed tomography data and the penetration of cement into the bone was varied over six levels each. The FEA models, consisting of the interdigitated cement–bone constructs with friction between cement and bone, were loaded to failure in tension and in shear. The cement and bone elements had provision for crack formation due to excessive stress. The interfacial strength showed a strong relationship with the average interdigitation (r²=0.97 and r²=0.93 in tension and shear, respectively). Also, the interface strength was strongly related with the contact area (r²=0.98 and r²=0.95 in tension and shear, respectively). The FEA results compared favorably to the stiffness–strength relationships determined experimentally. Overall, the cement–bone interface was 2.5 times stronger in shear than in tension and 1.15 times stiffer in tension than in shear, independent of the average interdigitation. More cracks occurred in the cement than in the bone, independent of the average interdigitation, consistent with the experimental results. In addition, more cracks were generated in shear than in tension. In conclusion, achieving and maintaining maximal infiltration of cement into the bone to obtain large interdigitation and contact area is key to optimizing the interfacial strength.