The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates

It has been hypothesized for over a hundred years that trabecular bone plays an important structural role in the musculoskeletal system of animals and that it responds dynamically to applied loads through growth. The objectives of this study are to quantify the three-dimensional structure of femoral head trabecular bone in a sample of extant strepsirrhines and to relate patterns of interspecific variation to locomotor behavioral differences. The bone volume fraction (BV/TV) and fabric anisotropy of trabecular bone in the femoral heads of Cheirogaleus major, Avahi laniger, Galago senegalensis, Galago alleni, Loris tardigradus, Otolemur crassicaudatus, and Perodicticus potto were quantified in three dimensions using serial high-resolution X-ray computed tomography scan data. A volume based method was used to quantify the structural anisotropy in three cubic samples located inside the central portion of the femoral head. Significant structural differences were found between the predominantly leaping galagines and indriids and the nonleaping lorisines and cheirogaleids. The leapers in general have relatively anisotropic trabecular bone. The galagines display a unique pattern of decreasing bone volume and increasing anisotropy moving from the superior to the inferior half of the femoral head. By contrast, the nonleaping taxa possess relatively uniform and isotropic bone throughout the femoral head. The differences in femoral head trabecular structure among these taxa seem to be related to locomotor behavioral differences, reflecting variation in the use and loading of the hip joint during normal locomotion.     

Unique suites of trabecular bone features characterize locomotor behavior in human and non-human anthropoid primates

Understanding the mechanically-mediated response of trabecular bone to locomotion-specific loading patterns would be of great benefit to comparative mammalian evolutionary morphology. Unfortunately, assessments of the correspondence between individual trabecular bone features and inferred behavior patterns have failed to reveal a strong locomotion-specific signal. This study assesses the relationship between inferred locomotor activity and a suite of trabecular bone structural features that characterize bone architecture. High-resolution computed tomography images were collected from the humeral and femoral heads of 115 individuals from eight anthropoid primate genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, Symphalangus). Discriminant function analyses reveal that subarticular trabecular bone in the femoral and humeral heads is significantly different among most locomotor groups. The results indicate that when a suite of femoral head trabecular features is considered, trabecular number and connectivity density, together with fabric anisotropy and the relative proportion of rods and plates, differentiate locomotor groups reasonably well. A similar, yet weaker, relationship is also evident in the trabecular architecture of the humeral head. The application of this multivariate approach to analyses of trabecular bone morphology in recent and fossil primates may enhance our ability to reconstruct locomotor behavior in the fossil record.     

Femoral head trabecular bone structure in two omomyid primates

The study of the three-dimensional structure of trabecular bone and its relationship to locomotor behavioral differences across different primate taxa provides a potentially useful analytic tool for reconstructing the behavior of extinct taxa. The purpose of the current study is to quantify the three-dimensional architecture of trabecular bone in the femoral head of Omomys carteri and Shoshonius cooperi and to compare this structure to that of several extant strepsirrhine taxa. Bone volume fraction (BV/TV) and fabric anisotropy were quantified in three dimensions using serial high-resolution X-ray computed tomography scan data collected from one femoral head from each fossil taxon. Three cubic volumes of interest (VOI) were identified within the femoral head. The BV/TV was quantified by assessing the percentage of bone voxels within each VOI and the structural anisotropy was quantified using the star volume distribution method. The Omomys femur used here has a high BV/TV with the galagine-like pattern of decreasing BV/TV from the superior to the inferior half of the femoral head. The fabric structure, however, is more lorisine-like in being relatively isotropic throughout the femoral head. The trabecular structure in Omomys is unique in its mix of features and appears to be most similar overall to the lorisines, suggesting that Omomys engaged in a quadrupedal mode of locomotion. By contrast the Shoshonius specimen possesses a relatively uniform BV/TV across the head but displays the distinctly galagine-like pattern of increasing anisotropy moving inferiorly in the femoral head. Taken as a whole, the trabecular structure in Shoshonius appears to be most like that of the galagines and is consistent with that of either an occasional leaper-quadruped or a specialized leaper. Despite the overall similarities in the external postcranial anatomy of Omomys and Shoshonius, the results of this study indicate potentially important differences in the magnitude and orientation of the external loads at the hip joint, suggesting that these animals engaged in divergent locomotor behaviors.     

Mechanical significance of femoral head trabecular bone structure in Loris and Galago evaluated using micromechanical finite element models

Work on the interspecific and intraspecific variation of trabecular bone in the proximal femur of primates demonstrates important architectural variation between animals with different locomotor behaviors. This variation is thought to be related to the processes of bone adaptation whereby bone structure is optimized to the mechanical environment. Micromechanical finite element models were created for the proximal femur of the leaping Galago senegalensis and the climbing and quadrupedal Loris tardigradus by converting bone voxels from high-resolution X-ray computed tomography scans of the femoral head to eight-noded brick elements. The resulting models had approximately 1.8 million elements each. Loading conditions representing takeoff phase of a leap and more generalized load orientations were applied to the models, and the models were solved using the iterative "row-by-row" matrix-vector multiplication algorithm. The principal strain and Von Mises stress results for the leaping model were similar for both species at each load orientation. Similar hip joint reaction forces in the range of 4.9 x to 12 x body weight were calculated for both species under each loading condition, but the hip reaction values estimated for Loris were higher than predicted based on locomotor behavior. These results suggest that functional adaptation to hip joint loading may not fully explain the differences in femoral head trabecular bone structure in Galago and Loris. The finite element method represents a unique and useful tool for analyzing the functional adaptation of trabecular bone in a diversity of animals and for reconstructing locomotor behavior in extinct taxa.     

A comparison of the femoral head and neck trabecular architecture of Galago and Perodicticus using micro-computed tomography (microCT)

Innovations in micro-computed tomography (microCT) in the medical field have resulted in the development of techniques that allow the precise quantification of bone density and fabric related parameters of trabecular bone. For the purpose of this study, the technique was applied to a small sample of Perodicticus potto and Galago senegalensis femora to see if differences in loading environment elicit the predicted effects on trabecular structure. While the overall bone volume was approximately three times larger in the potto, there was no significant difference in the apparent volume density in the two taxa. When regional differences in the proximal femur were examined, the cancellous bone of the femoral head of Perodicticus potto and Galago senegalensis, while not differing in volume density, showed differences in trabecular orientation, with the potto having more randomly oriented trabeculae than the bushbaby. This was as hypothesized, given that the bushbaby submits its femora to more stereotypical loading environments than the potto. In the femoral neck, the cancellous bone was not only more randomly oriented, it was also denser in the potto compared with the bushbaby. This suggests that trabecular morphology may be extremely sensitive to certain differences in the loading environment and that this information, combined with information on cortical bone structure and external geometry, will result in a more complete understanding of how bone shape and composition correspond to loading and locomotor patterns. Ultimately, a synthesis of these different lines of evidence may have considerable applications in paleontological studies that attempt to reconstruct bone use from morphology.     

The mechanical characteristics of cancellous bone at the upper femoral region

Mechanical behaviour of trabecular bone at the upper femoral region of human bones has been studied by compression tests on trabecular bone specimens removed from normal femora obtained at autopsy. Compression tests were performed along three different axes of loading on wet specimens and high loading rates. Femoral head specimens proved to be the strongest for any axis of loading.

Large variation in compressive strength and modulus of elasticity is seen within and between femoral bone samples. Anisotropy and differences in anisotropy for the different regions have been observed. A significant correlation between mechanical properties (σ max − E) and bone mineral content of the specimen was found.

Tests on whole bone structures demonstrate that removal of the central part of the trabecular bone at the proximal femur reduces the strength for impact loading considerably (± 50%).     

Quantification of trabecular spatial orientation from low-resolution images

No accepted methodology exists to assess trabecular bone orientation from clinical CT scans. The aim of this study was to test the hypothesis that the distribution of grey values in clinical CT images is related to the underlying trabecular architecture and that this distribution can be used to identify the principal directions and local anisotropy of trabecular bone. Fourteen trabecular bone samples were extracted from high-resolution (30 μm) micro-CT scans of seven human femoral heads. Trabecular orientations and local anisotropy were calculated using grey-level deviation (GLD), a novel method providing a measure of the three-dimensional distribution of image grey values. This was repeated for different image resolutions down to 300 μm and for volumes of interest (VOIs) ranging from 1 to 7 mm. Outcomes were compared with the principal mechanical directions and with mean intercept length (MIL) as calculated for the segmented 30-μm images. For the 30-μm images, GLD predicted the mechanical principal directions equally well as MIL. For the 300-μm images, which are resolutions that can be obtained in vivo using clinical CT, only a small increase (3°–6°) in the deviation from the mechanical orientations was found. VOIs of 5 mm resulted in a robust quantification of the orientation. We conclude that GLD can quantify structural bone parameters from low-resolution CT images.     

Trabecular bone adaptation with an orthotropic material model.

Most bone adaptation algorithms, that attempt to explain the connection between bone morphology and loads, assume that bone is effectively isotropic. An isotropic material model can explain the bone density distribution, but not the structure and pattern of trabecular bone, which clearly has a mechanical significance. In this paper, an orthotropic material model is utilized to predict the proximal femur trabecular structure. Two hypotheses are combined to determine the local orientation and material properties of each element in the model. First, it is suggested that trabecular directions, which correspond to the orthotropic material axes, are determined locally by the maximal principal stress directions due to the multiple load cases (MLC) the femur is subject to. The second hypothesis is that material properties in each material direction can be determined using directional stimuli, thus extending existing adaptation algorithms to include directionality. An algorithm is utilized, where each iteration comprises of two stages. First, material axes are rotated to the direction of the largest principal stress that occurs from a multiple load scheme applied to the proximal femur. Next, material properties are modified in each material direction, according to a directional stimulus. Results show that local material directions correspond with known trabecular patterns, reproducing all main groups of trabeculae very well. The local directional stiffnesses, degree of anisotropy and density distribution are shown to conform to real femur morphology.     

Prediction of trabecular bone principal structural orientation using quantitative ultrasound scanning

Bone has the ability to adapt its structure in response to the mechanical environment as defined as Wolff's Law. The alignment of trabecular structure is intended to adapt to the particular mechanical milieu applied to it. Due to the absence of normal mechanical loading, it will be extremely important to assess the anisotropic deterioration of bone during the extreme conditions, i.e., long term space mission and disease orientated disuse, to predict risk of fractures. The propagation of ultrasound wave in trabecular bone is substantially influenced by the anisotropy of the trabecular structure. Previous studies have shown that both ultrasound velocity and amplitude is dependent on the incident angle of the ultrasound signal into the bone sample. In this work, seven bovine trabecular bone balls were used for rotational ultrasound measurement around three anatomical axes to elucidate the ability of ultrasound to identify trabecular orientation. Both ultrasound attenuation (ATT) and fast wave velocity (UV) were used to calculate the principal orientation of the trabecular bone. By comparing to the mean intercept length (MIL) tensor obtained from μCT, the angle difference of the prediction by UV was 4.45°, while it resulted in 11.67° angle difference between direction predicted by μCT and the prediction by ATT. This result demonstrates the ability of ultrasound as a non-invasive measurement tool for the principal structural orientation of the trabecular bone.     

Measurement of structural anisotropy in femoral trabecular bone using clinical-resolution CT images

Discrepancies in finite-element model predictions of bone strength may be attributed to the simplified modeling of bone as an isotropic structure due to the resolution limitations of clinical-level Computed Tomography (CT) data. The aim of this study is to calculate the preferential orientations of bone (the principal directions) and the extent to which bone is deposited more in one direction compared to another (degree of anisotropy). Using 100 femoral trabecular samples, the principal directions and degree of anisotropy were calculated with a Gradient Structure Tensor (GST) and a Sobel Structure Tensor (SST) using clinical-level CT. The results were compared against those calculated with the gold standard Mean-Intercept-Length (MIL) fabric tensor using micro-CT. There was no significant difference between the GST and SST in the calculation of the main principal direction (median error=28°), and the error was inversely correlated to the degree of transverse isotropy (r=−0.34, p<0.01). The degree of anisotropy measured using the structure tensors was weakly correlated with the MIL-based measurements (r=0.2, p<0.001). Combining the principal directions with the degree of anisotropy resulted in a significant increase in the correlation of the tensor distributions (r=0.79, p<0.001). Both structure tensors were robust against simulated noise, kernel sizes, and bone volume fraction. We recommend the use of the GST because of its computational efficiency and ease of implementation. This methodology has the promise to predict the structural anisotropy of bone in areas with a high degree of anisotropy, and may improve the in vivo characterization of bone.     

Heterogeneity of yield strain in low-density versus high-density human trabecular bone

Understanding the off-axis behavior of trabecular yield strains may lend unique insight into the etiology of fractures since yield strains provide measures of failure independent of elastic behavior. We sought to address anisotropy of trabecular yield strains while accounting for variations in both density and anatomic site and to determine the mechanisms governing this behavior. Cylindrical specimens were cored from vertebral bodies (n=22, BV/TV=0.11±0.02) and femoral necks (n=28, BV/TV=0.22±0.06) with the principal trabecular orientation either aligned along the cylinder axis (on-axis, n=22) or at an oblique angle of 15° or 45° (off-axis, n=28). Each specimen was scanned with micro-CT, mechanically compressed to failure, and analysed with nonlinear micro-CT-based finite element analysis. Yield strains depended on anatomic site (p=0.03, ANOVA), and the effect of off-axis loading was different for the two sites (p=0.04)—yield strains increased for off-axis loading of the vertebral bone (p=0.04), but were isotropic for the femoral bone (p=0.66). With sites pooled together, yield strains were positively correlated with BV/TV for on-axis loading (R²=58%, p<0.0001), but no such correlation existed for off-axis loading (p=0.79). Analysis of the modulus-BV/TV and strength-BV/TV relationships indicated that, for the femoral bone, the reduction in strength associated with off-axis loading was greater than that for modulus, while the opposite trend occurred for the vertebral bone. The micro-FE analyses indicated that these trends were due to different failure mechanisms for the two types of bone and the different loading modes. Taken together, these results provide unique insight into the failure behavior of human trabecular bone and highlight the need for a multiaxial failure criterion that accounts for anatomic site and bone volume fraction.     

Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb?

Vertebrate morphologists often implicate functional adaptationsof bone to mechanical milieus when comparing animals with distinctbehavioral repertoires. Functional morphologists frequentlyuse comparative osteology and locomotor behavior to constructcorrelative form–function relationships. While some experimentalwork has investigated functional adaptations of bone elicitedby specific locomotor behaviors, these studies usually manipulaterepertoires by introducing artificial situations (e.g., treadmills)or creating differences in the level of activity (i.e., exercise),either of which can compromise extrapolations to free-ranginganimals. Here, we present trabecular bone morphology and microarchitecturefrom an inbred mouse model in which components of naturalisticlocomotor repertoires were accentuated. Using inbred mice, wecontrol for genetic variability, further isolating the osteogenicresponses to these behaviors. Single female (BALB/cByJ) mice(n = 10 per group) were housed for 8 weeks beginning at 30 dayspostbirth in custom-designed cages that accentuated either linearquadrupedalism or turning. Concurrently, mice in a control groupwere housed singly in open cages. The distal femoral metaphysiswas scanned by micro-computed tomography at the end of the 8-weekexperiment protocol. The experimental groups, particularly the"linear" group, differed significantly from the control group(simulated "free-ranging" condition) in several variables: bonevolume fraction ("linear" 42% less than controls; "turning"24% less than controls), trabecular number ("linear" 12% lessthan controls; "turning" 9% less than controls), connectivitydensity ("linear" 43% less than controls; "turning" 35% lessthan controls), and a characterization of trabecular surfaces("linear" 15% greater than controls; "turning" 11% greater thancontrols). No differences in the degree of anisotropy were observedamong groups, and generally, "linear" and "turning" groups didnot differ significantly from one another in any measures oftrabecular microarchitecture. Considering the distinct differencesin locomotor behaviors between the "linear" quadrupedalism and"turning" groups, these data suggest that comparisons at thedistal femoral metaphysis of trabecular microarchitecture ororientation between different groups of animals may be somewhatlimited in accurately reconstructing the loading conditionsassociated with different locomotor modes.     

Articular structure and function in Hylobates,Colobus, and Papio

It has been demonstrated in clinical and experimental studies that subarticular trabecular bone responds to mechanical loads transmitted across joints through changes in mass and structural organization. We investigated differences in mass, volume, and density of subarticular trabecular bone of the humeral and femoral head in Hylobates syndactylus, Colobus guereza, and Papio cynocephalus. Our hypothesis was that variations in trabecular properties between taxa may reflect differences in mechanical loading associated with different locomotor repertoires. A nondestructive method for measuring trabecular properties using optical luminance data measured from radiographs was developed. We also examined the relationship between internal trabecular properties and the external size and surface area of the humeral and femoral heads in these taxa. Our results suggest that internal and external articular structure are relatively independent of each other and may be adapted to different aspects of the mechanical environment. Differences in trabecular mass between taxa appear to correspond to differences in the magnitudes of mechanical loads borne by the joint, whereas aritcular volume and surface area are related primarily to differences in joint mobility. Because of the apparent physiological “de-coupling” of articular mass and volume, variations in articular density (mass/volume) are difficult to interpret in isolation. Comparisons of internal and external articular structure may provide new ways to reconstruct the locomotor/positional behavior of extinct taxa. © 1994 Wiley-Liss, Inc.     

Trabecular bone ontogeny in the human proximal femur

Ontogenetic changes in the human femur associated with the acquisition of bipedal locomotion, especially the development of the bicondylar angle, have been well documented. The purpose of this study is to quantify changes in the three-dimensional structure of trabecular bone in the human proximal femur in relation to changing functional and external loading patterns with age. High-resolution X-ray computed tomography scan data were collected for 15 juvenile femoral specimens ranging in age from prenatal to approximately nine years of age. Serial slices were collected for the entire proximal femur of each individual with voxel resolutions ranging from 0.017 to 0.046 mm depending on the size of the specimen. Spherical volumes of interest were defined within the proximal femur, and the bone volume fraction, trabecular thickness, trabecular number, and fabric anisotropy were calculated in three dimensions. Bone volume fraction, trabecular number, and degree of anisotropy decrease between the age of 6 months and 12 months, with the lowest values for these parameters occurring in individuals near 12 months of age. By age 2-3 years, the bone volume, thickness, and degree of anisotropy increase slightly, and regions in the femoral neck become more anisotropic corresponding to the thickening of the inferior cortical bone of the neck. These results suggest that trabecular structure in the proximal femur reflects the shift in external loading patterns associated with the initiation of unassisted walking in infants.     

How morphology predicts mechanical properties of trabecular structures depends on intra-specimen trabecular thickness variations

Two observations underlie this work. First, that the architecture of trabecular bone can accurately predict the mechanical stiffness characteristics of bone specimens when considering the combination of volume fraction and fabric, which is a measure of architectural anisotropy. Second, that the same morphological measures could not accurately predict the mechanical properties of porous structures in general. We hypothesize that this discrepancy can be explained by the special nature of trabecular bone as a structure in remodeling equilibrium relative to the external loads. We tested this hypothesis using a generic model of trabecular bone. Five series of 153 different architectures were created with this model. Each architecture was subjected to morphological analysis, and four different fabric measures were calculated to evaluate their effectiveness in characterizing the architecture. Relationships were determined relating morphology to the elastic constants. The quality of these relationships was tested by correlating the predicted elastic constants with those determined from finite element analysis. We found that the four fabric measures used could estimate the mechanical properties almost equally well. So the suggestion that fabric measures based on trabecular bone volume better represent the architecture than mean intercept length could not be affirmed. We conclude that for structures with equally sized elliptical voids the mechanical properties can be predicted well only if trabecular thickness variations within each structure are limited. These structures closely resemble previously developed models of trabecular bone. Furthermore, they are stiff in the principal fabric direction, hence, according to Cowin (J. Biomech. Eng. (108) (1986) 83), they are in remodeling equilibrium. These structures are also stiff over a large range of loading orientations, hence, are relatively insensitive to deviations in direction of loading.     

A theoretical model to predict distribution of the fabric tensor and apparent density in cancellous bone

 The adaptation of cancellous bone to mechanical forces is well recognized. Theoretical models for predicting cancellous bone architecture have been developed and have mainly focused on the distribution of trabecular mass or the apparent density. The purpose of this study was to develop a theoretical model which can simultaneously predict the distribution of trabecular orthotropy/orientation, as represented by the fabric tensor, along with apparent density. Two sets of equations were derived under the assumption that cancellous bone is a biological self-optimizing material which tends to minimize strain energy. The first set of equations provide the relationship between the fabric tensor and stress tensor, and have been verified to be consistent with Wolff’s law of trabecular architecture, that is, the principal directions of the fabric tensor coincide with the principal stress trajectories. The second set of equations yield the apparent density from the stress tensor, which was shown to be identical to those obtained based on local optimization with strain energy density of true bone tissue as the objective function. These two sets of equations, together with elasticity field equations, provide a complete mathematical formulation for the adaptation of cancellous bone. Received: 25 February 1997/Revised version: 23 September 1997     

Does skeletal anatomy reflect adaptation to locomotor patterns? cortical and trabecular architecture in human and nonhuman anthropoids

Although the correspondence between habitual activity and diaphyseal cortical bone morphology has been demonstrated for the fore- and hind-limb long bones of primates, the relationship between trabecular bone architecture and locomotor behavior is less certain. If sub-articular trabecular and diaphyseal cortical bone morphology reflects locomotor patterns, this correspondence would be a valuable tool with which to interpret morphological variation in the skeletal and fossil record. To assess this relationship, high-resolution computed tomography images from both the humeral and femoral head and midshaft of 112 individuals from eight anthropoid genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, and Symphalangus) were analyzed. Within-bone (sub-articular trabeculae vs. mid-diaphysis), between-bone (forelimb vs. hind limb), and among-taxa relative distributions (femoral:humeral) were compared. Three conclusions are evident: (1) Correlations exists between humeral head sub-articular trabecular bone architecture and mid-humerus diaphyseal bone properties; this was not the case in the femur. (2) In contrast to comparisons of inter-limb diaphyseal bone robusticity, among all species femoral head trabecular bone architecture is significantly more substantial (i.e., higher values for mechanically relevant trabecular bone architectural features) than humeral head trabecular bone architecture. (3) Interspecific comparisons of femoral morphology relative to humeral morphology reveal an osteological "locomotor signal" indicative of differential use of the forelimb and hind limb within mid-diaphysis cortical bone geometry, but not within sub-articular trabecular bone architecture.     

Compressive fatigue behavior of human vertebral trabecular bone

Damage accumulation under compressive fatigue loading is believed to contribute significantly to non-traumatic, age-related vertebral fractures in the human spine. Only few studies have explored trabecular bone fatigue behavior under compressive loading and none examined the influence of trabecular architecture on fatigue life. In this study, trabecular bone samples of human lumbar and thoracic vertebrae (4 donors from age 29 to 86, n=29) were scanned with a microCT system prior to compressive fatigue testing to determine morphology-mechanical relationships for this relevant loading mode. Inspired from previous fabric-based relationships for elastic properties and quasi-static strength of trabecular bone, a simple power relationship between volume fraction, fabric eigenvalue, applied stress and the number of cycles to failure is proposed. The experimental results demonstrate a high correlation for this relationship (R2=0.95) and detect a significant contribution of the degree of anisotropy towards prediction of fatigue life. Step-wise regression for total and residual strains at failure suggested a weak, but significant correlation with volume fraction. From the obtained results, we conclude that the applied stress normalized by volume fraction and axial fabric eigenvalue can estimate fatigue life of human vertebral trabecular bone in axial compressive loading.     

Relationships between loading history and femoral cancellous bone architecture

A theory relating bone maintenance to mechanical loading history has been applied to successfully predict the distribution of bone density and trabecular orientation in the adult proximal femur. The loading history was simulated by determining the stress fields in a two-dimensional finite element model exposed to various discrete loading cases and making assumptions about the relative number of loading cycles associated with each load case. The total stimulus to bone maintenance was then calculated by a linear superposition of the stimulus of each loading case. Based on the calculated total stimulus, the apparent density and material properties of each element were changed and the stress solutions were again determined. Using this iterative technique, the bone apparent density and orientation characteristics were predicted. The results indicate that the trabecular morphology of the femur can only be explained by considering the joint loadings from multiple directions. Contrary to the 'trajectorial theory' promoted by Wolff (The Law of Bone Remodelling, 1892), trabecular orientations predicted from our multiple-load analyses are not necessarily perpendicular and do not correspond to the principal stress directions of any one loading condition. Our predicted orientations correspond better to the drawing of bone trabecular morphology by von Meyer (Archs Anat. Physiol. wiss. Med. 34, 615-628, 1867) than to the classic drawing by Wolff and suggest that further study of the trajectorial theory is warranted.     

A comparative study of the trabecular bony architecture of the talus in humans, non-human primates, and Australopithecus

This study tested the hypothesis that talar trabecular microarchitecture reflects the loading patterns in the primate ankle joint, to determine whether talar trabecular morphology might be useful for inferring locomotor behavior in fossil hominins. Trabecular microarchitecture was quantified in the anteromedial, anterolateral, posteromedial, and posterolateral quadrants of the talar body in humans and non-human primates using micro-computed tomography. Trabecular bone parameters, including bone volume fraction, trabecular number and thickness, and degree of anisotropy differed between primates, but not in a manner entirely consistent with hypotheses derived from locomotor kinematics. Humans have highly organized trabecular struts across the entirety of the talus, consistent with the compressive loads incurred during bipedal walking. Chimpanzees possess a high bone volume fraction, consisting of plate-like trabecular struts. Orangutan tali are filled with a high number of thin, connected trabeculae, particularly in the anterior portion of the talus. Gorillas and baboons have strikingly similar internal architecture of the talus. Intraspecific analyses revealed no regional differences in trabecular architecture unique to bipedal humans. Of the 22 statistically significant regional differences in the human talus, all can also be found in other primates. Trabecular thickness, number, spacing, and connectivity density had the same regional relationship in the talus of humans, chimpanzees, gorillas, and baboons, suggesting a deeply conserved architecture in the primate talus. Australopithecus tali are human-like in most respects, differing most notably in having more oriented struts in the posteromedial quadrant of the body compared with the posterolateral quadrant. Though this result could mean that australopiths loaded their ankles in a unique manner during bipedal gait, the regional variation in degree of anisotropy was similar in humans, chimpanzees, and gorillas. These results collectively suggest that the microarchitecture of the talus does not simply reflect the loading environment, limiting its utility in reconstructing locomotion in fossil primates.