Comparison of Cervical Spine Anatomy in Calves,Pigs and Humans

Background Context

Animals are commonly used to model the human spine for in vitro and in vivo experiments. Many studies have investigated similarities and differences between animals and humans in the lumbar and thoracic vertebrae. However, a quantitative anatomic comparison of calf, pig, and human cervical spines has not been reported.

Purpose

To compare fundamental structural similarities and differences in vertebral bodies from the cervical spines of commonly used experimental animal models and humans.

Study Design

Anatomical morphometric analysis was performed on cervical vertebra specimens harvested from humans and two common large animals (i.e., calves and pigs).

Methods

Multiple morphometric parameters were directly measured from cervical spine specimens of twelve pigs, twelve calves and twelve human adult cadavers. The following anatomical parameters were measured: vertebral body width (VBW), vertebral body depth (VBD), vertebral body height (VBH), spinal canal width (SCW), spinal canal depth (SCD), pedicle width (PW), pedicle depth (PD), pedicle inclination (PI), dens width (DW), dens depth (DD), total vertebral width (TVW), and total vertebral depth (TVD).

Results

The atlantoaxial (C1–2) joint in pigs is similar to that in humans and could serve as a human substitute. The pig cervical spine is highly similar to the human cervical spine, except for two large transverse processes in the anterior regions ofC4–C6. The width and depth of the calf odontoid process were larger than those in humans. VBW and VBD of calf cervical vertebrae were larger than those in humans, but the spinal canal was smaller. Calf C7 was relatively similar to human C7, thus, it may be a good substitute.

Conclusion

Pig cervical vertebrae were more suitable human substitutions than calf cervical vertebrae, especially with respect to C1, C2, and C7. The biomechanical properties of nerve vascular anatomy and various segment functions in pig and calf cervical vertebrae must be considered when selecting an animal model for research on the spine.     

Validation of single-segment and three-segment spinal models used to represent lumbar flexion

Changes in spinal posture between the erect and flexed positions were calculated using angular measurements from lateral photographs and radiographs of ten adult male subjects. For photographic measurements, the thoracolumbar vertebral column was modelled as either a single segment or as three segments. In the three-segment model, there was a non-significant correlation between the decrease in lumbar concavity and intervertebral motion. In addition, there was a non-significant negative correlation between the increase in thoracic convexity and lumbar motion determined radiographically. In the single-segment model, the decrease in angulation between the thoracolumbar spine and pelvis was a good representation of lumbar spine flexion as determined by the mean lumbar intervertebral angular change. Therefore, modelling the thoracolumbar vertebral column as a single segment allowed better estimation of lumbar intervertebral angular change during flexion than a three-segment model. The results indicate that large range dynamic motion of the lumbar vertebral column can be represented using photographic analysis of the positions of three easily identified anatomical landmarks: the anterior superior iliac spine, posterior superior iliac spine and the spinous process of the first thoracic vertebra.     

Does the correlation between schmorl's nodes and vertebral morphology extend into the lumbar spine?

Schmorl's nodes are depressions on vertebrae due to herniation of the nucleus pulposus of the intervertebral disc into the vertebral body. This study provides an extension of our previous study which analyzed the shape of the lower thoracic spine and found that vertebral morphology was associated with the presence of Schmorl's nodes. Ninety adult individuals from the late Medieval site of Fishergate House, York, and the Post‐Medieval site of Coach Lane, North Shields, Tyne and Wear, England, were analysed using 2D geometric morphometrics to identify possible relationships between vertebral morphology and Schmorl's nodes at the thoraco‐lumbar junction and in the lumbar spine. A significant correlation was found between vertebral shape and the presence of Schmorl's nodes in the twelfth thoracic vertebrae and the first to third lumbar vertebrae. The findings corroborate previous studies and suggest that vertebral shape may be an important factor in spinal health. It is hypothesized that the pedicle shape of affected vertebrae may not provide adequate structural support for the vertebral bodies, resulting in vertical disc herniation. Am J Phys Anthropol 157:526–534, 2015. © 2015 Wiley Periodicals, Inc.     

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.     

The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra).

In order to assess the mechanical properties of xenarthrous vertebrae, and to evaluate the role of xenarthrae as fossorial adaptations, in vitro bending tests were performed on posterior thoracic and lumbar vertebral segments excised from specimens of the armadillo Dasypus novemcinctus and the opossum Didelphis virginiana, the latter being used to represent the primitive mammalian condition. The columns of the two species were subjected to dorsal, ventral, and lateral bending, as well as torsion, in order to determine their stiffness in each of these directions. During these tests, bone strains in the centra of selected vertebrae were determined using rosette strain gages. Overall stiffness of the armadillo backbone at physiologically relevant displacement levels was significantly higher than that of the opossum for both dorsal and lateral bending. The two species also exhibited significant differences in angular displacement of individual vertebrae and in vertebral strain magnitudes and orientations in these two directions. No significant differences were observed when the columns of the two species were subjected to torsion or to ventral bending. Our results suggest that some, but not all, of the mechanical differences between the two species are due to the presence of xenarthrae. For example, removal of the xenarthrae from selected vertebrae (L2-L4) changes strain orientation and shear, but not strain magnitudes. Comparisons with functional data from other digging mammals indicate that the modified mechanical properties of the Dasypus column are consistent with an interpretation of xenarthrae as digging adaptations and lend support to the idea that the order Xenarthra represents an early offshoot of placental mammals specialized for fossoriality.     

Human evolution and osteoporosis-related spinal fractures

The field of evolutionary medicine examines the possibility that some diseases are the result of trade-offs made in human evolution. Spinal fractures are the most common osteoporosis-related fracture in humans, but are not observed in apes, even in cases of severe osteopenia. In humans, the development of osteoporosis is influenced by peak bone mass and strength in early adulthood as well as age-related bone loss. Here, we examine the structural differences in the vertebral bodies (the portion of the vertebra most commonly involved in osteoporosis-related fractures) between humans and apes before age-related bone loss occurs. Vertebrae from young adult humans and chimpanzees, gorillas, orangutans, and gibbons (T8 vertebrae, n = 8–14 per species, male and female, humans: 20–40 years of age) were examined to determine bone strength (using finite element models), bone morphology (external shape), and trabecular microarchitecture (micro-computed tomography). The vertebrae of young adult humans are not as strong as those from apes after accounting for body mass (p<0.01). Human vertebrae are larger in size (volume, cross-sectional area, height) than in apes with a similar body mass. Young adult human vertebrae have significantly lower trabecular bone volume fraction (0.26±0.04 in humans and 0.37±0.07 in apes, mean ± SD, p<0.01) and thinner vertebral shells than apes (after accounting for body mass, p<0.01). Since human vertebrae are more porous and weaker than those in apes in young adulthood (after accounting for bone mass), even modest amounts of age-related bone loss may lead to vertebral fracture in humans, while in apes, larger amounts of bone loss would be required before a vertebral fracture becomes likely. We present arguments that differences in vertebral bone size and shape associated with reduced bone strength in humans is linked to evolutionary adaptations associated with bipedalism.     

Trunk Muscle Activity Is Modified in Osteoporotic Vertebral Fracture and Thoracic Kyphosis with Potential Consequences for Vertebral Health

This study explored inter-relationships between vertebral fracture, thoracic kyphosis and trunk muscle control in elderly people with osteoporosis. Osteoporotic vertebral fractures are associated with increased risk of further vertebral fractures; but underlying mechanisms remain unclear. Several factors may explain this association, including changes in postural alignment (thoracic kyphosis) and altered trunk muscle contraction patterns. Both factors may increase risk of further fracture because of increased vertebral loading and impaired balance, which may increase falls risk. This study compared postural adjustments in 24 individuals with osteoporosis with and without vertebral fracture and with varying degrees of thoracic kyphosis. Trunk muscle electromyographic activity (EMG) associated with voluntary arm movements was recorded and compared between individuals with and without vertebral fracture, and between those with low and high thoracic kyphosis. Overall, elderly participants in the study demonstrated co-contraction of the trunk flexor and extensor muscles during forwards arm movements, but those with vertebral fractures demonstrated a more pronounced co-contraction than those without fracture. Individuals with high thoracic kyphosis demonstrated more pronounced alternating flexor and extensor EMG bursts than those with less kyphosis. Co-contraction of trunk flexor and extensor muscles in older individuals contrasts the alternating bursts of antagonist muscle activity in previous studies of young individuals. This may have several consequences, including altered balance efficacy and the potential for increased compressive loads through the spine. Both of these outcomes may have consequences in a population with fragile vertebrae who are susceptible to fracture.     

Functional implications of variation in lumbar vertebral count among hominins

As early as the 1970s, Robinson defined lumbar vertebrae according to their zygapophyseal orientation. He identified six lumbar elements in fossil Sts 14 Australopithecus africanus, one more than is commonly present in modern humans. It is now generally inferred that the modal number of lumbar vertebrae for australopiths and early Homo was six, from which the mode of five in later Homo is derived. The two central questions this study investigates are (1) to what extent do differences in human lumbar vertebral count affect lordotic shape and lumbar function, and (2) what does lumbar number variation imply about lumbar spine function in early hominins? To address these questions, I first outline a biomechanical model of lumbar number effect on lordotic function. I then identify relevant morphological differences in the human modal and extra-modal variants, which I use to test the model. These tests permit evaluation of the human L6 variant as a model for reconstructing early hominin modal number and spine function. Application of the biomechanical model in reconstructing australopith/early Homo lumbar spines highlights shared principles of Euler column strength and sagittal spine flexibility among early and modern hominins. Within modern humans, the extra-modal L6 variant has an extended series of three cranially positioned kyphotic vertebrae and strongly oblique zygapophyseal facets at the last lumbar level. Although they share the same radius and length of lumbar curvature, the L6 variant differs functionally from the L5 mode in its expanded range of sagittal flexion/extension and enhanced resistance to shear. Given the modal number of six lumbar vertebrae in australopiths and early Homo, lumbar spine mobility and strength would have been key properties of vertebral function in early bipeds whose upper and lower body segments were coupled by close approximation of the thorax and iliac crests.     

Sex differences in the vertebral column of gombe chimpanzees

Male and female chimpanzees from Gombe National Park, Tanzania (Pan troglodytes schweinfurthii) differ in live body weights but not in cranial capacity or fore-and hindlimb long bone lengths. Skeletal dimensions of the limbs and vertebral column indicate a mosaic of sex differences. Vertebral column measurements generally are greater in males. While linear measurements identify differences in the breadth and depth of the lower cervical and upper thoracic vertebrae, areal assessments show significant differences in weight-bearing surfaces throughout the thoracic and lumbar segments. These can be interpreted in terms of distribution of weight and body composition (i.e. amount of musculature).     

Spatial distribution of trabeculae in iliac bone from 145 osteoporotic females

145 women showing clinical and radiological signs of involutional osteoporosis of the spine were biopsed at the ilium for histomorphometric analysis of bone mass including trabecular bone volume and parameters reflecting the spatial distribution of bony elements (mean trabecular plate thickness, density and separation). Results were compared with an age-matched population of 22 healthy females. Postmenopausal osteoporotics (i.e. younger than 75 years) were characterized by a significant reduction in trabecular bone volume, plate density and thickness, while senile osteoporotics (i.e. older than 75 years) did not exhibit any difference with controls. 51% of the osteoporotic patients had a trabecular bone volume higher than the spontaneous vertebral crush threshold defined by Meunier. Osteoporotic patients with trabecular bone volume under the vertebral crush threshold had a significant decrease in all trabecular parameters. On the opposite, patients with trabecular bone volume above the vertebral crush threshold had only a significant decrease in the number of trabeculae. A negative correlation was found between age and plate density in both osteoporotic patients and controls. A linear correlation was found between trabecular bone volume and plate density, but thickness and density of trabecular plates were not correlated. This study confirms that involutional osteoporosis is not only a decreased bone mass disorder. A modified spatial distribution of trabeculae or a mechanically less resistant bone matrix could be additional factors.     

Micromechanical analyses of vertebral trabecular bone based on individual trabeculae segmentation of plates and rods

Trabecular plates play an important role in determining elastic moduli of trabecular bone. However, the relative contribution of trabecular plates and rods to strength behavior is still not clear. In this study, individual trabeculae segmentation (ITS) and nonlinear finite element (FE) analyses were used to evaluate the roles of trabecular types and orientations in the failure initiation and progression in human vertebral trabecular bone. Fifteen human vertebral trabecular bone samples were imaged using micro computed tomography (μCT), and segmented using ITS into individual plates and rods by orientation (longitudinal, oblique, and transverse). Nonlinear FE analysis was conducted to perform a compression simulation for each sample up to 1% apparent strain. The apparent and relative trabecular number and tissue fraction of failed trabecular plates and rods were recorded during loading and data were stratified by trabecular orientation. More trabecular rods (both in number and tissue fraction) failed at the initiation of compression (0.1–0.2% apparent strain) while more plates failed around the apparent yield point (>0.7% apparent strain). A significant correlation between plate bone volume fraction (pBV/TV) and apparent yield strength was found (r²=0.85). From 0.3% to 1% apparent strain, significantly more longitudinal trabecular plate and transverse rod failed than other types of trabeculae. While failure initiates at rods and rods fail disproportionally to their number, plates contribute significantly to the apparent yield strength because of their larger number and tissue volume. The relative failed number and tissue fraction at apparent yield point indicate homogeneous local failure in plates and rods of different orientations.     

Hip bone trabecular architecture shows uniquely distinctive locomotor behaviour in South African australopithecines

Cancellous bone retains structural and behavioural properties which are time and strain-rate dependent. As the orientation of the trabeculae (trajectories) follows the direction of the principal strains imposed by daily loadings, habitual postural and locomotor behaviours are responsible for a variety of trabecular architectures and site-specific textural arrangements of the pelvic cancellous network. With respect to the great ape condition, the human trabecular pattern is characterized by a distinctive ilioischial bundle, an undivided sacropubic bundle, and a full diagonal crossing (approximately 100 degrees) over the acetabulum between the ilioischial and the sacropubic bundles. Advanced digital image processing (DIP) of hip bone radiographs has revealed that adolescent and adult South African australopithecines retained an incompletely developed human-like trabecular pattern associated with gait-related features that are unique among the extant primates.     

Simulation of vertebral trabecular bone loss using voxel finite element analysis

Trabecular bone loss in human vertebral bone is characterised by thinning and eventual perforation of the horizontal trabeculae. Concurrently, vertical trabeculae are completely lost with no histological evidence of significant thinning. Such bone loss results in deterioration in apparent modulus and strength of the trabecular core. In this study, a voxel-based finite element program was used to model bone loss in three specimens of human vertebral trabecular bone. Three sets of analyses were completed. In Set 1, strain adaptive resorption was modelled, whereby elements which were subject to the lowest mechanical stimulus (principal strain) were removed. In Set 2, both strain adaptive and microdamage mechanisms of bone resorption were included. Perforation of vertical trabeculae occurred due to microdamage resorption of elements with strains that exceeded a damage threshold. This resulted in collapse of the trabecular network under compression loading for two of the specimens tested. In Set 3, the damage threshold strain was gradually increased as bone loss progressed, resulting in reduced levels of microdamage resorption. This mechanism resulted in trabecular architectures in which vertical trabeculae had been perforated and which exhibited similar apparent modulus properties compared to experimental values reported in the literature. Our results indicate that strain adaptive remodelling alone does not explain the deterioration in mechanical properties that have been observed experimentally. Our results also support the hypothesis that horizontal trabeculae are lost principally by strain adaptive resorption, while vertical trabeculae may be lost due to perforation from microdamage resorption followed by rapid strain adaptive resorption of the remaining unloaded trabeculae.     

Trabecular shear stress in human vertebral cancellous bone: intra- and inter-individual variations

Correlation of the mean and standard deviation of trabecular stresses has been proposed as a mechanism by which a strong relationship between the apparent strength and stiffness of cancellous bone can be achieved. The current study examined whether the relationship between the mean and standard deviation of trabecular von Mises stresses can be generalized for any group of cancellous bone. Cylindrical human vertebral cancellous bone specimens were cut in the infero-superior direction from T12 of 23 individuals (inter-individual group). Thirty nine additional specimens were prepared similarly from the T4-T12 and L2-L5 vertebrae of a 63 year old male (intra-individual group). The specimens were scanned by micro-computed tomography (microCT) and trabecular von Mises stresses were calculated using finite element modeling. The expected value, standard deviation and coefficient of variation of the von Mises stress were calculated form a three-parameter Weibull function fitted to von Mises stress data from each specimen. It was found that the average and standard deviation of trabecular von Mises shear stress were: (i) correlated with each other, supporting the idea that high correlation between the apparent strength and stiffness of cancellous bone can be achieved through controlling the trabecular level shear stress variations, (ii) dependent on anatomical site and sample group, suggesting that the variation of stresses are correlated to the mean stress to different degrees between vertebrae and individuals, and (iii) dependent on bone volume fraction, consistent with the idea that shear stress is less well controlled in bones with low BV/TV. The conversion of infero-superior loading into trabecular von Mises stresses was maximum for the tissue at the junction of the thoracic and lumbar spine (T12-L1) consistent with this junction being a common site of vertebral fracture.     

Biomechanics of vertebral level, geometry, and transcortical tumors in the metastatic spine

Metastatic involvement can disrupt the mechanical integrity of the spine, rendering vertebrae susceptible to burst fracture and neurologic damage. Fracture risk assessment for patients with spinal metastases is important in considering prophylactic treatment options. Stability of thoracic vertebrae affected by metastatic disease has been shown to be dependent on tumor size and bone density, but additional structural and geometric factors may also play a role in fracture risk assessment. The objective of this study was to use parametric finite element modeling to determine the effects of vertebral level, geometry, and metastatic compromise to the cortical shell on the risk of burst fracture in the thoracic spine. Analysis of vertebral level and geometry was assessed by investigation of seven scenarios ranging in geometry from T2-T4 to T10-T12. The effects of cortical shell compromised were assessed by comparison of four transcortical scenarios to a fully contained central vertebral body tumor scenario. Results demonstrated that upper thoracic vertebrae are at greater risk of burst fracture and that kyphotic motion segments are at decreased risk of burst fracture. Vertebrae with transcortical lesions are up to 30% less likely to lead to burst fracture initiation. The findings of this study are important for improving the understanding of burst fracture mechanics in metastatically involved vertebrae and guiding future modeling efforts.     

Functional morphology of the primate head and neck

The vertebral column plays a key role in maintaining posture, locomotion, and transmitting loads between body components. Cervical vertebrae act as a bridge between the torso and head and play a crucial role in the maintenance of head position and the visual field. Despite its importance in positional behaviors, the functional morphology of the cervical region remains poorly understood, particularly in comparison to the thoracic and lumbar sections of the spinal column. This study tests whether morphological variation in the primate cervical vertebrae correlates with differences in postural behavior. Phylogenetic generalized least-squares analyses were performed on a taxonomically broad sample of 26 extant primate taxa to test the link between vertebral morphology and posture. Kinematic data on primate head and neck postures were used instead of behavioral categories in an effort to provide a more direct analysis of our functional hypothesis. Results provide evidence for a function-form link between cervical vertebral shape and postural behaviors. Specifically, taxa with more pronograde heads and necks and less kyphotic orbits exhibit cervical vertebrae with longer spinous processes, indicating increased mechanical advantage for deep nuchal musculature, and craniocaudally longer vertebral bodies and more coronally oriented zygapophyseal articular facets, suggesting an emphasis on curve formation and maintenance within the cervical lordosis, coupled with a greater resistance to translation and ventral displacement. These results not only document support for functional relationships in cervical vertebrae features across a wide range of primate taxa, but highlight the utility of quantitative behavioral data in functional investigations. Am J Phys Anthropol 156:531–542, 2015. © 2015 Wiley Periodicals, Inc.     

Placement of the diaphragmatic vertebra in catarrhines: implications for the evolution of dorsostability in hominoids and bipedalism in hominins

A fundamental adaptation to orthograde posture and locomotion amongst living hominoid primates is a numerically reduced lumbar column, which acts to stiffen the lower back and reduce injuries to the intervertebral discs. A related and functionally complementary strategy of spinal stability is a caudal position of the diaphragmatic vertebra relative to the primitive condition found in nonhominoid primates and most other mammals. The diaphragmatic vertebra marks the transition in vertebral articular facet (zygapophysis) orientation, which either resists (prediaphragmatic) or allows (postdiaphragmatic) trunk movement in the sagittal plane (i.e., flexion and extension). Unlike most mammals, which have dorsomobile spines (long lumbar columns and cranially placed diaphragmatic vertebrae) for running and leaping, hominoids possess dorsostable spines (short lumbar columns and caudally placed diaphragmatic vertebrae) adapted to orthogrady and antipronogrady. In contrast to humans and other extant hominoids, all known early hominin partial vertebral columns demonstrate cranial displacement of the diaphragmatic vertebra. To address this difference, variation in diaphragmatic placement is assessed in a large sample of catarrhine primates. I show that while hominoids are characterized by modal common placement of diaphragmatic and last rib-bearing vertebrae in general, interspecific differences in intraspecific patterns of variation exist. In particular, humans and chimpanzees show nearly identical patterns of diaphragmatic placement. A scenario of hominin evolution is proposed in which early hominins evolved cranial displacement from the ancestral hominid condition of common placement to achieve effective lumbar lordosis during the evolution of bipedal locomotion.     

Characterization of the age-dependent shape of the pediatric thoracic spine and vertebrae using generalized procrustes analysis

Generalized Procrustes Analysis (GPA) is a superimposition method used to generate size-invariant distributions of homologous landmark points. Several studies have used GPA to assess the three-dimensional (3D) shapes of or to evaluate sex-related differences in the human brain, skull, rib cage, pelvis and lower limbs. Previous studies of the pediatric thoracic vertebrae suggest that they may undergo changes in shape as a result of normative growth. This study uses GPA and second order polynomial equations to model growth and age- and sex-related changes in shape of the pediatric thoracic spine. We present a thorough analysis of the normative 3D shape, size, and orientation of the pediatric thoracic spine and vertebrae as well as equations which can be used to generate models of the thoracic spine and vertebrae for any age between 1 and 19 years. Such models could be used to create more accurate 3D reconstructions of the thoracic spine, generate improved age-specific geometries for finite element models (FEMs) and used to assist clinicians with patient-specific planning and surgical interventions for spine deformity.     

Natural variability and effects of cleaning and storage procedures on vertebral chemistry of the blacktip shark Carcharhinus limbatus

Key methodological assumptions regarding the degree of natural variability and influence of sample handling and storage of elasmobranch vertebral chemistry were assessed using laser‐ablation inductively coupled plasma mass spectrometry. Vertebral chemistry of juvenile blacktip sharks Carcharhinus limbatus was examined to identify whether differences existed among different regions of the vertebral column, between thoracic vertebrae of individual fish or within individual vertebrae. Additionally, the effects of bleach exposure and storage in ethanol on vertebral chemistry were compared. No significant variation in vertebral chemistry was found among different regions of the vertebral column or between thoracic vertebrae, but significant differences among transect locations within individual vertebrae were observed. The variation at all three levels appears comparable with published data on sagittal otoliths of bilaterally symmetrical teleost fishes. The experimental assessment of potential treatment effects indicated vertebral chemistry was not significantly affected by bleach or exposure to ethanol. Taken together, these results support the idea that vertebrae taken from the same region of the vertebral column can be treated as equivalent and at least certain elements remain robust to exposure to bleach and ethanol.