Application of an image-based weighted measure of skeletal bending stiffness to great ape mandibles

Traditional measures of structural stiffness in the primate skeleton do not consider the heterogeneous material stiffness distribution of bone. This assumption of homogeneity introduces an unknown degree of error in estimating stiffness in skeletal elements. Measures of weighted stiffness can be developed by including heterogeneous grayscale variations evident in computed tomographic (CT) images. Since gray scale correlates with material stiffness, the distribution of bone quality and quantity can be simultaneously considered. We developed weighted measures of bending resistance and applied these to CT images at three locations along the mandibular corpus in the hominoids Gorilla, Pongo, and Pan. We calculated the traditional (unweighted) moment of inertia for comparison to our weighted measure, which weighs each pixel by its gray-scale value. This weighing results in assignment of reduced moment of inertia values to sections of reduced density. Our weighted and unweighted moments differ by up to 22%. These differences are not consistent among sections, however, such that they cannot be calculated by simple correction of unweighted moments. The effect of this result is that the rank ordering of individual sections within species changes if weighted moments are considered. These results suggest that the use of weighted moments may spur different interpretations of comparative data sets that rely on stiffness measures as estimates of biomechanical competence.     

Elastic modulus variation in mandibular bone: a microindentation study of Macaca fascicularis

We characterized the heterogeneous anisotropic elastic properties of mandibular bone in an adult female specimen of Macaca fascicularis using the technique of microindentation. This approach used an indenter of known mass and geometry to sample bone hardness at a spatial resolution in the order of 100 mum. Hardness values were converted to elastic modulus using empirically derived regression. We determined properties in alveolar, midcorpus, and basal regions of coronal and transverse sections taken from multiple locations along the corpus and ramus. Within sections, we determined properties from endosteal, midcortical, and periosteal regions. We found regional variations in bone structure, including bands of orthotropic circumferential lamellar bone at the endosteal and periosteal corpus base, angular region, and ramus. Transversely isotropic osteonal bone characterizes the midcortices of alveolar and basal regions, with many resorption spaces in alveolar regions restricting sampling opportunities. Regional variations in elasticity include relatively compliant bone in the anterior corpus and ramus. Basal cortical bone is stiffer longitudinally than transversely or superoinferiorly, while the evidence for directional dependence in alveolar bone is equivocal. Alveolar bone appears to be relatively compliant with respect to bone found in midcorpus or basal regions. Considerable variation exists in structure and material properties on a highly localized scale, more so than is discernible through conventional approaches for determining material property variation.     

Functional significance of cortical bone distribution in anthropoid mandibles: an in vitro assessment of bone strain under combined loads

Local variation in cortical bone thickness in the postcanine mandibular corpus appears to be stereotypical among anthropoids. Specifically, at sections under the molars, lingually situated cortical bone is typically thinner than that along the lateral aspect. This pattern applies despite phylogenetic, dietary, and allometric differences among the anthropoids sampled to date. Demes et al. (Food Acquisition and Processing in Primates [1984] New York: Plenum Press, p. 369-390) employed a theoretical analysis of mastication in Gorilla and Homo to argue that this pattern could be explained with reference to biomechanical stresses. Specifically, they proposed that the combined effects of torsion and direct shear on the working-side corpus create a condition in which net stresses and strains are reduced along the lingual cortical plate. Demonstration of this effect would suggest a functional linkage between localized differences in bone mass and strain gradients in the facial skeleton. We conducted an empirical evaluation of the effects of the combined loads of torsion and direct shear in vitro on a sample of formalin-fixed human mandibles. Rosette strain gages were affixed to the lateral and medial aspects of the corpus in each specimen, and surface strains were recorded separately under controlled torsional and occlusal loads, and under simultaneous application of these loads. The hypothesis that lingual strains are reduced under combined twisting and occlusal loads was generally supported; however, we observed reduction in surface strains at some sites along the lateral aspect of the corpus under these combined loads as well. These unexpected findings are attributable to unanticipated loading conditions imposed by occlusal forces, which result from sources of stress in addition to direct shear. These experiments provide provisional support for the hypothesis that superposed sources of bone strain produce large strain gradients between buccal and lingual aspects of the mandibular corpus, and that local variation in bone mass may be associated with these gradients.     

The assessment of trabecular bone parameters and cortical bone strength: A comparison of micro-CT and dental cone-beam CT

This study compared the capabilities of micro-computed tomography (micro-CT) and dental cone-beam computed tomography (CBCT) in assessing trabecular bone parameters and cortical bone strength. Micro-CT and CBCT scans were applied to 28 femurs from 14 rats to obtain independent measurements of the volumetric cancellous bone mineral density (vCanBMD) in the femoral head, volumetric cortical bone mineral density (vCtBMD) in the femoral diaphysis, cross-sectional moment of inertia (CSMI), and bone strength index (BSI) (=CSMI×vCtBMD). Five structural parameters of the trabecular bone of the femoral head were calculated from micro-CT images. A three-point bending test was then conducted to measure the fracture load of each femur. Bivariate linear Pearson analysis was conducted to calculate the correlation coefficients (r values) of the micro-CT, dental CBCT, and three-point bending measurements. The statistical analyses showed a strong correlation between vCanBMD values obtained using micro-CT and dental CBCT (r=0.830). There were strong or moderate correlation between vCanBMD measured using dental CBCT and five parameters of trabecular structure measured using micro-CT. Additionally, the results were satisfactory regardless of whether micro-CT or dental CBCT was used to measure the femoral diaphysis vCtBMD (r=0.733 and 0.680, respectively), CSMI (r=0.756 and 0.726, respectively), or BSI (r=0.846 and 0.847, respectively) to predict fracture loads. This study has yielded a new method for using dental CBCT to evaluate bone parameters and bone strength; however, further studies are necessary to validate the use of dental CBCT on humans.     

Brief communication: dental development and enamel thickness in the Lakonis Neanderthal molar

Developmental and structural affinities between modern human and Neanderthal dental remains continue to be a subject of debate as well as their utility for informing assessments of life history and taxonomy. Excavation of the Middle Paleolithic cave site Lakonis in southern Greece has yielded a lower third molar (LKH 1). Here, we detail the crown development and enamel thickness of the distal cusps of the LKH 1 specimen, which has been classified as a Neanderthal based on the presence of an anterior fovea and mid-trigonid crest. Crown formation was determined using standard histological techniques, and enamel thickness was measured from a virtual plane of section. Developmental differences include thinner cuspal enamel and a lower periodicity than modern humans. Crown formation in the LKH 1 hypoconid is estimated to be 2.6-2.7 years, which is shorter than modern human times. The LKH 1 hypoconid also shows a more rapid overall crown extension rate than modern humans. Relative enamel thickness was approximately half that of a modern human sample mean; enamel on the distal cusps of modern human third molars is extremely thick in absolute and relative terms. These findings are consistent with recent studies that demonstrate differences in crown development, tissue proportions, and enamel thickness between Neanderthals and modern humans. Although overlap in some developmental variables may be found, the results of this and other studies suggest that Neanderthal molars formed in shorter periods of time than modern humans, due in part to thinner enamel and faster crown extension rates.     

Brief communication: Forelimb compliance in arboreal and terrestrial opossums

Primates display high forelimb compliance (increased elbow joint yield) compared to most other mammals. Forelimb compliance, which is especially marked among arboreal primates, moderates vertical oscillations of the body and peak vertical forces and may represent a basal adaptation of primates for locomotion on thin, flexible branches. However, Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) reported that marsupials have forelimb compliance comparable to or greater than that of most primates, but did not distinguish between arboreal and terrestrial marsupials. If forelimb compliance is functionally linked to locomotion on thin branches, then elbow yield should be highest in marsupials relying on arboreal substrates more often. To test this hypothesis, we compared forelimb compliance between two didelphid marsupials, Caluromys philander (an arboreal opossum relying heavily on thin branches) and Monodelphis domestica (an opossum that spends most of its time on the ground). Animals were videorecorded while walking on a runway or a horizontal 7‐mm pole. Caluromys showed higher elbow yield (greater changes in degrees of elbow flexion) on both substrates, similar to that reported for arboreal primates. Monodelphis was characterized by lower elbow yield that was intermediate between the values reported by Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) for more terrestrial primates and rodents. This finding adds evidence to a model suggesting a functional link between arboreality—particularly locomotion on thin, flexible branches—and forelimb compliance. These data add another convergent trait between arboreal primates, Caluromys, and other arboreal marsupials and support the argument that all primates evolved from a common ancestor that was a fine‐branch arborealist. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Regional,ontogenetic, and sex‐related variations in elastic properties of cortical bone in baboon mandibles

Understanding the mechanical features of cortical bone and their changes with growth and adaptation to function plays an important role in our ability to interpret the morphology and evolution of craniofacial skeletons. We assessed the elastic properties of cortical bone of juvenile and adult baboon mandibles using ultrasonic techniques. Results showed that, overall, cortical bone from baboon mandibles could be modeled as an orthotropic elastic solid. There were significant differences in the directions of maximum stiffness, thickness, density, and elastic stiffness among different functional areas, indicating regional adaptations. After maturity, the cortical bone becomes thicker, denser, and stiffer, but less anisotropic. There were differences in elastic properties of the corpus and ramus between male and female mandibles which are not observed in human mandibles. There were correlations between cortical thicknesses and densities, between bone elastic properties and microstructural configuration, and between the directions of maximum stiffness and bone anatomical axes in some areas. The relationships between bone extrinsic and intrinsic properties bring us insights into the integration of form and function in craniofacial skeletons and suggest that we need to consider both macroscopic form, microstructural variation, and the material properties of bone matrix when studying the functional properties and adaptive nature of the craniofacial skeleton in primates. The differences between baboon and human mandibles is at variance to the pattern of differences in crania, suggesting differences in bone adaption to varying skeletal geometries and loading regimes at both phylogenetic and ontogenetic levels. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Measurement of body segment mass,center of gravity,and determination of moments of inertia by double pendulum in Lemur fulvus

The collection of data on physical parameters of body segments is a preliminary critical step in studying the biomechanics of locomotion. Little data on nonhuman body segment parameters has been published. The lack of standardization of techniques for data collection and presentation has made the comparative use of these data difficult and at times impossible. This study offers an approach for collecting data on center of gravity and moments of inertia for standardized body segments. The double swing pendulum approach is proposed as a solution for difficulties previously encountered in calculating moments of inertia for body segments. A format for prompting a computer to perform these calculations is offered, and the resulting segment mass data for Lemur fulvus is presented.     

The relation between external dimensions of the human mandible and cortical bone morphology as determined with the aid of CT scans

Computerized tomographs were taken of 22 mandibles, selected from an early Arab population and aged between 17 and 60 years. A specially designed holder was used to define specific locations along the mandible, namely symphysis, mid sagittal section through the corpus, midpoint of the first molar (M1), gonion and ramus. Cortical cross sectional area and principal moments of inertia were then calculated for the locations specified, to obtain estimates of the resistance of the bone to deformation. They were analyzed in relation to age, sex, side and external dimensions of the mandible. The error of measurement calculated from (i) repeated CT scans (ii) repeated measurements (iii) from comparison of CT scans with a sectioned mandible, were of the same order of magnitude. All values were greater in males than in females; they were only slightly affected by age and were unaffected by side. Mandibular length and ramus height accounted for most of the variation observed in moments of inertia. We consider that these results can best be interpreted in accordance with the hypotheses put forward by Hylander (1975, 1985) according to which the mandible acts as a third degree lever, with “wishboning” forces acting at the symphysis and parasagittal bending at the first molar. We now plan to apply this method to study the “strength” of the mandibles of past populations with different dietary adaptations.     

Nanostructure and elastic modulus of single trabecula in bovine cancellous bone

We aimed to investigate the elastic modulus of trabeculae using tensile tests and assess the effects of nanostructure at the hydroxyapatite (HAp) crystal scale on the elastic modulus. In the experiments, 18 trabeculae that were at least 3 mm in length in the proximal epiphysis of three adult bovine femurs were used. Tensile tests were conducted using a small tensile testing device coupled with microscopy under air-dried condition. The c-axis orientation of HAp crystals and the degree of orientation were measured by X-ray diffraction. To observe the deformation behavior of HAp crystals under tensile loading, the same tensile tests were conducted in X-ray diffraction measurements. The mineral content of specimens was evaluated using energy dispersive X-ray spectrometry. The elastic modulus of a single trabecula varied from 4.5 to 23.6 GPa, and the average was 11.5±5.0 GPa. The c-axis of HAp crystals was aligned with the trabecular axis and the crystals were lineally deformed under tensile loading. The ratio of the HAp crystal strain to the tissue strain (strain ratio) had a significant correlation with the elastic modulus (r=0.79; P<0.001). However, the mineral content and the degree of orientation did not vary widely and did not correlate with the elastic modulus in this study. It suggests that the strain ratio may represent the nanostructure of a single trabecula and would determine the elastic modulus as well as mineral content and orientation.     

The relationship between muscle activation and shear elastic modulus of the sternocleidomastoid muscle during 3-D torque production

The sternocleidomastoid (SCM) is a primary neck torque generator, but the relationship between its muscle activation and shear elastic modulus during 3-D torque production is unknown. This study examined variations in neural control and shear elastic modulus of the SCM across various 3-D isometric torques. Our primary hypothesis was that the SCM would display similar preferred directions where muscle activity and shear elastic modulus were maximal during voluntary 3-D isometric torque production. Surface electromyography (EMG) and ultrasound shear wave elastography (SWE) data were collected from the SCM in 20 participants performing 3-D isometric target-matching at two different torque amplitudes. We used spherical statistics to compare the preferred directions calculated from the SWE and EMG data at 40% and 80% torque level during 3-D isometric torque production. We demonstrated a small but significant difference between EMG and SWE preferred directions, with the SWE preferred direction oriented more towards ipsilateral bending and less towards contralateral axial rotation than the preferred direction for the EMG data. We conclude that, although small differences exist, SCM shear elastic modulus is largely driven by activation during 3-D neck torques for healthy individuals.     

Brief communication: intertooth and intrafacet dental microwear variation in an archaeological sample of modern humans from the Jordan Valley

Dental microwear was recorded in a Bronze-Iron Age (3570-3000 BP) sample of modern humans recovered from Tell es-Sa'idiyeh in the Jordan Valley. Microwear patterns were compared between mandibular molars, and between the upper and lower part of facet 9. The comparison revealed a greater frequency of pits and shorter scratches on the second and third molars, compared to the first. Pit frequency also increased on the lower part of the facet on the first molar, compared to the upper part. These results support previous calls for standardization when selecting a molar type for a diet-microwear study. Otherwise the microwear variations along the tooth row could mask any diet-microwear correlations. The results also suggest that there may be a need to choose a consistent location on a facet in order to enhance comparability among studies.     

Biomechanical response of impacted bony pelvis: influence of the morphometry and bone density

Mechanical properties of human pelvic bone tissue according morphological parameters were few studied in anterior–posterior compression tests and few data are available to correctly validate finite element pelvis models. In order to reduce this gap, 12 pelvic bones were removed from male and female embalmed cadavers and compressed. Anatomic angles were measured and bone's density was calculated after each test.

Fractures observed during those tests were coherent with those observed in real life. Bone's density and percentage of mineralisation were not significantly different between the male and female groups. The retropubic angle was significantly larger in the female group (p < 0.05). Mean load necessary to obtain the collapse was significantly higher in the male group (p < 0.05).     

Trabecular bone structure in the mandibular condyles of gouging and nongouging platyrrhine primates

The relationship between mandibular form and biomechanical function is a topic of significant interest to morphologists and paleontologists alike. Several previous studies have examined the morphology of the mandible in gouging and nongouging primates as a means of understanding the anatomical correlates of this feeding behavior. The goal of the current study was to quantify the trabecular bone structure of the mandibular condyle of gouging and nongouging primates to assess the functional morphology of the jaw in these animals. High‐resolution computed tomography scan data were collected from the mandibles of five adult common marmosets (Callithrix jacchus), saddle‐back tamarins (Saguinus fuscicollis), and squirrel monkeys (Saimiri sciureus), respectively, and various three‐dimensional morphometric parameters were measured from the condylar trabecular bone. No significant differences were found among the taxa for most trabecular bone structural features. Importantly, no mechanically significant parameters, such as bone volume fraction and degree of anisotropy, were found to vary significantly between gouging and nongouging primates. The lack of significant differences in mechanically relevant structural parameters among these three platyrrhine taxa may suggest that gouging as a habitual dietary behavior does not involve significantly higher loads on the mandibular condyle than other masticatory behaviors. Alternatively, the similarities in trabecular architecture across these three taxa may indicate that trabecular bone is relatively unimportant mechanically in the condyle of these primates and therefore is functionally uninformative. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Brief communication: comparing loading scenarios in lower first molar supporting bone structure using 3D finite element analysis

Finite element analysis (FEA) is a widespread technique to evaluate the stress/strain distributions in teeth or dental supporting tissues. However, in most studies occlusal forces are usually simplified using a single vector (i.e., point load) either parallel to the long tooth axis or oblique to this axis. In this pilot study we show how lower first molar occlusal information can be used to investigate the stress distribution with 3D FEA in the supporting bone structure. The LM₁ and the LP²‐LM¹ of a dried modern human skull were scanned by μCT in maximum intercuspation contact. A kinematic analysis of the surface contacts between LM₁ and LP²‐LM¹ during the power stroke was carried out in the occlusal fingerprint analyzer (OFA) software to visualize contact areas during maximum intercuspation contact. This information was used for setting the occlusal molar loading to evaluate the stress distribution in the supporting bone structure using FEA. The output was compared to that obtained when a point force parallel to the long axis of the tooth was loaded in the occlusal basin. For the point load case, our results indicate that the buccal and lingual cortical plates do not experience notable stresses. However, when the occlusal contact areas are considered, the disto‐lingual superior third of the mandible experiences high tensile stresses, while the medio‐lingual cortical bone is subjected to high compressive stresses. Developing a more realistic loading scenario leads to better models to understand the relationship between masticatory function and mandibular shape and structures. Am J Phys Anthropol, 2012. © 2011 Wiley Periodicals, Inc.     

Brief communication: Contributions of enamel‐dentine junction shape and enamel deposition to primate molar crown complexity

Molar crown morphology varies among primates from relatively simple in some taxa to more complex in others, with such variability having both functional and taxonomic significance. In addition to the primary cusps, crown surface complexity derives from the presence of crests, cuspules, and crenulations. Developmentally, this complexity results from the deposition of an enamel cap over a basement membrane (the morphology of which is preserved as the enamel‐dentine junction, or EDJ, in fully formed teeth). However, the relative contribution of the enamel cap and the EDJ to molar crown complexity is poorly characterized. In this study we examine the complexity of the EDJ and enamel surface of a broad sample of primate (including fossil hominin) lower molars through the application of micro‐computed tomography and dental topographic analysis. Surface complexity of the EDJ and outer enamel surface (OES) is quantified by first mapping, and then summing, the total number of discrete surface orientation patches. We investigate the relative contribution of the EDJ and enamel cap to crown complexity by assessing the correlation in patch counts between the EDJ and OES within taxa and within individual teeth. We identify three patterns of EDJ/OES complexity which demonstrate that both crown patterning early in development and the subsequent deposition of the enamel cap contribute to overall crown complexity in primates. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.