Modifications of the locomotor system in habitually quadrupedal humans.

The acquisition of habitual bipedal locomotion, which resulted in numerous modifications of the skeleton was a crucial step in hominid evolution. However, our understanding of the inherited skeletal modifications versus those acquired while learning to walk remains limited. We here present data derived from X-rays and CT scans of quadrupedal adult humans and compare the morphology of the vertebral column, pelvis and femur to that of a bipedal brother. We show how a skeleton forged by natural selection for bipedal locomotion is modified when used to walk quadrupedally. The quadrupedal brother is characterised by the absence of femoral obliquity, a very high anteversion angle of the femoral neck, a very high collo-diaphyseal angle and a very reduced lordosis. The differences in the pelvis are more subtle and complex, yet of functional importance. The modification of the ischial spines to an ischial ridge and the perfectly rounded shape of the sacral curvature are two unique features that can be directly attributed to a quadrupedal posture and locomotion. We propose a functional interpretation of these two exceptional modifications. Unexpectedly, the quadrupedal brother and sister show a greater angle of pelvic incidence compared to their bipedal brother, a trait previously shown to increase with learning to walk in bipedal subjects. Moreover, the evolution from an occasional towards a permanent bipedality has given rise to a functional association between the angle of pelvic incidence and the lumbar curvature, with high angles of incidence and greater lumbar curvature promoting stability during bipedal locomotion. The quadrupedal brother and sister with a high angle of incidence and a very reduced lordosis thus show a complete decoupling of this complex functional integration.

Functional integrative analysis of the human hip joint: the three-dimensional orientation of the acetabulum and its relation with the orientation of the femoral neck.

In humans, the hip joint occupies a central place in the locomotor system, as it plays an important role in body support and the transmission of the forces between the trunk and lower limbs. The study of the three-dimensional biomechanics of this joint has important implications for documenting the morphological changes associated with the acquisition of a habitual bipedal gait in humans. Functional integration at any joint has important implications in joint stability and performance. The aim of the study was to evaluate the functional integration at the human hip joint. Both the level of concordance between the three-dimensional axes of the acetabulum and the femoral neck in a bipedal posture, and patterns of covariation between these two axes were analysed. First, inter-individual variations were quantified and significant differences in the three-dimensional orientations of both the acetabulum and the femoral neck were detected. On a sample of 57 individuals, significant patterns of covariation were identified, however, the level of concordance between the axes of both the acetabulum and the femoral neck in a bipedal posture was lower than could be expected for a key joint such as the hip. Patterns of covariation were explored regarding the complex three-dimensional biomechanics of the full pelvic-femoral complex. Finally, we suggest that the lower degree of concordance observed at the human hip joint in a bipedal posture might be partly due to the phylogenetic history of the human species.

How is sagittal balance acquired during bipedal gait acquisition? Comparison of neonatal and adult pelves in three dimensions. Evolutionary implications.

We compare adult and intact neonatal pelves, using a pelvic sagittal variable, the angle of sacral incidence, which presents significant correlations with vertebral curvature in adults and plays an important role in sagittal balance of the trunk on the lower limbs. Since the lumbar curvature develops in the child in association with gait acquisition, we expect a change in this angle during growth which could contribute to the acquisition of sagittal balance. To understand the mechanisms underlying the sagittal balance in the evolution of human bipedalism, we also measure the angle of incidence of hominid fossils. Fourty-seven landmarks were digitized on 50 adult and 19 intact neonatal pelves. We used a three-dimensional model of the pelvis (DE-VISU program) which calculates the angle of sacral incidence and related functional variables. Cross-sectional data from newborns and adults show that the angle of sacral incidence increases and becomes negatively correlated with the sacro-acetabular distance. During ontogeny the sacrum becomes curved, tends to sink down between the iliac blades as a wedge and moves backward in the sagittal plane relative to the acetabula, thus contributing to the backwards displacement of the center of gravity of the trunk. A chain of correlations links the degree of the sacral slope and of the angle of incidence, which is tightly linked with the lumbar lordosis. We sketch a model showing the coordinated changes occurring in the pelvis and vertebral column during the acquisition of bipedalism in infancy. In the australopithecine pelves, Sts 14 and AL 288-1, and in the Homo erectus Gona pelvis the angle of sacral incidence reaches the mean values of humans. Discussing the incomplete pelves of Ardipithecus ramidus, Australopithecus sediba and the Nariokotome Boy, we suggest how the functional linkage between pelvis and spine, observed in humans, could have emerged during hominid evolution.

Study of the three-dimensional orientation of the labrum: its relations with the osseous acetabular rim.

Understanding the three-dimensional orientation of the coxo-femoral joint remains a challenge as an accurate three-dimensional orientation ensure an efficient bipedal gait and posture. The quantification of the orientation of the acetabulum can be performed using the three-dimensional axis perpendicular to the plane that passes along the edge of the acetabular rim. However, the acetabular rim is not regular as an important indentation in the anterior rim was observed. An innovative cadaver study of the labrum was developed to shed light on the proper quantification of the three-dimensional orientation of the acetabulum. Dissections on 17 non-embalmed corpses were performed. Our results suggest that the acetabular rim is better represented by an anterior plane and a posterior plane rather than a single plane along the entire rim as it is currently assumed. The development of the socket from the Y-shaped cartilage was suggested to explain the different orientations in these anterior and posterior planes. The labrum forms a plane that takes an orientation in between the anterior and posterior parts of the acetabular rim, filling up inequalities of the bony rim. The vectors V(L) , V(A2) and V(P) , representing the three-dimensional orientation of the labrum, the anterior rim and the posterior rim, are situated in a unique plane that appears biomechanically dependent. The three-dimensional orientation of the acetabulum is a fundamental parameter to understand the hip joint mechanism. Important applications for hip surgery and rehabilitation, as well as for physical anthropology, were discussed.

A three-dimensional axis for the study of femoral neck orientation.

A common problem in the quantification of the orientation of the femoral neck is the difficulty to determine its true axis; however, this axis is typically estimated visually only. Moreover, the orientation of the femoral neck is commonly analysed using angles that are dependent on anatomical planes of reference and only quantify the orientation in two dimensions. The purpose of this study is to establish a method to determine the three-dimensional orientation of the femoral neck using a three-dimensional model. An accurate determination of the femoral neck axis requires a reconsideration of the complex architecture of the proximal femur. The morphology of the femoral neck results from both the medial and arcuate trabecular systems, and the asymmetry of the cortical bone. Given these considerations, two alternative models, in addition to the cylindrical one frequently assumed, were tested. The surface geometry of the femoral neck was subsequently used to fit one cylinder, two cylinders and successive cross-sectional ellipses. The model based on successive ellipses provided a significantly smaller average deviation than the two other models (P < 0.001) and reduced the observer-induced measurement error. Comparisons with traditional measurements and analyses on a sample of 91 femora were also performed to assess the validity of the model based on successive ellipses. This study provides a semi-automatic and accurate method for the determination of the functional three-dimensional femoral neck orientation avoiding the use of a reference plane. This innovative method has important implications for future studies that aim to document and understand the change in the orientation of the femoral neck associated with the acquisition of a bipedal gait in humans. Moreover, the precise determination of the three-dimensional orientation has implications in current research involved in developing clinical applications in diagnosis, hip surgery and rehabilitation.

Technical note: Shape variability induced by reassembly of human pelvic bones.

In traditional as well as in geometric morphometric studies, the shape of the pelvis is often quantified after the reassembly of the two hip bones and the sacrum. However, on dry bones, the morphology of the cartilaginous tissues that form the two sacroiliac joints and the pubic symphysis before death remains unknown, leading to potential inaccuracies and errors during the reassembly process. A protocol was established to investigate the effects of reassembly on the quantification of pelvis shape. The shape of fresh pelves obtained after dissection, in which the three bones are in an anatomically relevant position, was compared with the shape of different reassemblies based on the individual dry bones of the same individuals. Our results demonstrated a significant effect of the reassembly. Variation in the reassembly process is likely related, first, to the complete absence of cartilaginous tissues on dry bones and, second, to the morphology of the sacroiliac joint which, in vivo, allows physiological movements, resulting in different potential positions of the two sacroiliac surfaces relative to one another. However, the artificial variation introduced by the reassembly process appears small compared with the biological variation between the different individuals.

Study of femoral torsion during prenatal growth: interpretations associated with the effects of intrauterine pressure.

The developing fetus is protected from external environmental influences by maternal tissues. However, these structures have a limited elasticity, such that the fetus must grow in a confined space, constraining its size at the end of pregnancy. Can these constraints modify the morphology of the fetal skeleton? The intensity of these constraints increases between 5 months and birth, making it the most appropriate period to address this question. A sample of 89 fetal femora was analyzed, and results provide evidence that during this period, the torsion of the femoral shaft (quantified by means of a new three-dimensional method) increases gradually. Two explanations were considered: this increase could signal effects of constraints induced by the intrauterine cavity, developmental patterning, or some combination of these two. Different arguments tend to support the biomechanical explanation, rather than a programming pattern formation. Indeed, the identification of the femur as a first degree lever, created by the hyperflexion of the fetal lower limbs on the pelvis, could explain the increase in femoral shaft torsion during prenatal life. A comparison with femora of infants is in accordance with this mechanical interpretation, which is possible through bone modeling/remodeling. Although genetic and epigenetic mechanisms may regulate timing of fetal development, our data suggest that at birth, the fetal skeleton also has an intrauterine mechanical history through adaptive bone plasticity.

The partial skeleton StW 431 from Sterkfontein - Is it time to rethink the Plio-Pleistocene hominin diversity in South Africa?

The discovery of the nearly complete Plio-Pleistocene skeleton StW 573 Australopithecus prometheus from Sterkfontein Member 2, South Africa, has intensified debates as to whether Sterkfontein Member 4 contains a hominin species other than Australopithecus africanus. For example, it has recently been suggested that the partial skeleton StW 431 should be removed from the A. africanus hypodigm and be placed into A. prometheus. Here we re-evaluate this latter proposition, using published information and new comparative data. Although both StW 573 and StW 431 are apparently comparable in their arboreal (i.e., climbing) and bipedal adaptations, they also show significant morphological differences. Surprisingly, StW 431 cannot be unequivocally aligned with either StW 573 or other hominins from Sterkfontein commonly attributed to A. africanus (nor with Paranthropus robustus and Australopithecus sediba). This finding, together with considerations about the recent dating of Plio-Pleistocene hominin-bearing sites in South Africa and palaeoecological/palaeoclimatic conditions, raises questions whether it is justified to subsume hominins from Taung, Makapansgat and Sterkfontein (and Gladysvale) within a single taxon. Given the wealth of fossil material and analytical techniques now available, we call for a re-evaluation of the taxonomy of South African Plio-Pleistocene hominins. Such an endeavour should however go beyond the current (narrow) focus on establishing an A. africanus-A. prometheus dichotomy.

How Did the Pelvis and Vertebral Column Become a Functional Unit during the Transition from Occasional to Permanent Bipedalism?

The functional linkage between pelvis and spine remained long hidden to science. Here, we recount the history of research that led in 1992 to the discovery of the "angle of sacral incidence" by the team of G. Duval-Beaupère. This angle, formed between a ray from the hip joint center to the superior sacral surface and the perpendicular to the sacral surface, was later called pelvic incidence. Specific to each individual, pelvic incidence is tightly correlated with the degree of lumbar lordosis. It is each individual's "signature" for an efficient sagittal balance since it represents the sum of two positional parameters, sacral slope and pelvic tilt. The simultaneous experimental determination of the trunk line of gravity permitted Duval-Beaupère's team to elucidate the conditions of an efficient sagittal balance of the trunk on the lower limbs. We present an in vivo EOS study of eight spino-pelvic parameters describing the sagittal balance in 131 adults. We observe a chain of correlations between the six angular parameters and discuss the functional significance of these results. We show that pelvic incidence increases and lumbar lordosis develops when the infant learns to walk, leading to a correlation between these parameters. This process of association between pelvis and spine might have acquired a solid genetic basis during hominid evolution by natural selection acting on both pelvis and spine. We suggest that this process of functional integration was only possible in the context of bipedal locomotion becoming permanent and stereotyped, expressed by a relatively invariant, periodic walking cycle. Anat Rec, 300:912-931, 2017. © 2017 Wiley Periodicals, Inc.

Anatomical study of the proximal femur in the fetus.

Two angles effectively describe the upper femur geometry: The neck shaft angle (NSA) and anteversion (AV). AV and NSA decrease from birth until they reach their adult values, but little work has focused on in-utero life. Our aim was to determine if and how AV and NSA change through the fetal life. Eighty-seven femurs from 44 formalin preserved fetuses were sampled to achieve a biometry. Correlation tests and linear regression showed that AV was highly correlated with age: AV increases during the second half of gestation. No conclusion can be given concerning NSA. It is speculated that these changes may be caused by mechanical stresses.

Pelvic incidence: a predictive factor for three-dimensional acetabular orientation-a preliminary study.

Acetabular cup orientation (inclination and anteversion) is a fundamental topic in orthopaedics and depends on pelvis tilt (positional parameter) emphasising the notion of a safe range of pelvis tilt. The hypothesis was that pelvic incidence (morphologic parameter) could yield a more accurate and reliable assessment than pelvis tilt. The aim was to find out a predictive equation of acetabular 3D orientation parameters which were determined by pelvic incidence to include in the model. The second aim was to consider the asymmetry between the right and left acetabulae. Twelve pelvic anatomic specimens were measured with an electromagnetic Fastrak system (Polhemus Society) providing 3D position of anatomical landmarks to allow measurement of acetabular and pelvic parameters. Acetabulum and pelvis data were correlated by a Spearman matrix. A robust linear regression analysis provided prediction of acetabulum axes. The orientation of each acetabulum could be predicted by the incidence. The incidence is correlated with the morphology of acetabula. The asymmetry of the acetabular roof was correlated with pelvic incidence. This study allowed analysis of relationships of acetabular orientation and pelvic incidence. Pelvic incidence (morphologic parameter) could determine the safe range of pelvis tilt (positional parameter) for an individual and not a group.

Relationship between sacral pelvic incidence and acetabular orientation.

The importance of the sacral pelvic incidence (SPI) in relation to individual variations of sagittal spinal curvature has become well-recognised. We attempted to determine the relationship between SPI and acetabular orientation. The three-dimensional coordinates of 47 homologous points were observed on 51 adult anatomical pelvises (26 female and 25 male). The reference vertical plane was Lewinnek's anterior pelvic plane. 10 angular parameters and 11 linear parameters were defined and calculated. These were expressed both in absolute value (in millimetres) and in "acetabular unit" (relative to the mean value of the right and left acetabular rays). Mean values of the parameters were calculated for all pelvises and according to gender. There were two dominant parameters: the "sacral slope" and the "V pubic angle". "Acetabular tilting" was primarily dependent on the "sacral slope" and its intermediary on the "SPI", while "acetabular anteversion" dependent on the "V pubic angle" via the "angle of prow". It is recommended that positioning of the acetabular cup in total hip arthroplasty relates to anatomical parameters, and to the global sagittal balance of the pelvi-spinal unit.

Three-dimensional study of pelvic asymmetry on anatomical specimens and its clinical perspectives.

The aim of this study was to assess pelvic asymmetry (i.e. to determine whether the right iliac bone and the right part of the sacrum are mirror images of the left), both quantitatively and qualitatively, using three-dimensional measurements. Pelvic symmetry was described osteologically using a common reference coordinate system for a large sample of pelvises. Landmarks were established on 12 anatomical specimens with an electromagnetic Fastrak system. Seventy-one paired variables were tested with a paired t-test and a non-parametric test (Wilcoxon). A Pearson correlation matrix between the right and left values of the same variable was applied exclusively to values that were significantly asymmetric in order to calculate a dimensionless asymmetry index, ABGi, for each variable. Fifteen variables were significantly asymmetric and correlated with the right vs. left sides for the following anatomical regions: sacrum, iliac blades, iliac width, acetabulum and the superior lunate surface of the acetabulum. ABGi values above a threshold of +/- 4.8% were considered significantly asymmetric in seven variables of the pelvic area. Total asymmetry involving the right and the left pelvis seems to follow a spiral path in the pelvis; in the upper part, the iliac blades rotate clockwise, and in the lower part, the pubic symphysis rotates anticlockwise. Thus, pelvic asymmetry may be evaluated in clinical examinations by measuring iliac crest orientation.

Anatomic study of femoral patellar groove in fetus.

The authors performed a biometric analysis of the femoral patellar groove in fetus and compared their findings with those observed in adults. Forty-four formalin-preserved fetuses were studied (13-38 weeks). Digitalized images were used to obtain measurements (alpha angle of the groove, trochlear slopes thetaL and thetaM). A comparison of means of independent samples between our series and adults was performed. For each angle of the distal epiphysis (alpha, thetaL, thetaM) there was no significant difference between this fetal series and adults. This is the first biometry of the fetal patellar groove. The morphology of the lower femur appears to be the same in fetus and adults. The results of this study suggest that the anatomic characteristics of the patellar groove could have been integrated into the genome during the course of evolution. This would be in favor of a genetic origin of patellar groove dysplasia.

An anatomical and biometrical study of the femoral trochlear groove in the human fetus.

We performed a biometric analysis of the femoral trochlear groove in the fetus and compared our findings with those observed in adults. We studied 44 formalin-preserved fetuses (13-38 weeks) and used digitized images to obtain measurements (alpha angle of the groove, trochlear slopes thetaL and thetaM). A comparison of means between our series and adults was achieved. For each angle of the distal epiphysis (alpha, thetaL, thetaM) there was no significant difference between our fetal series and adults. This is the first biometric study of fetal trochlea. The morphology of the lower femur appears to be the same in the fetus and the adult.