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

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Abstract

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 lumbar curvature develops in children 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 sagittal balance in the evolution of human bipedalism, we also measure the angle of incidence in hominid fossils.

Forty-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 lumbar lordosis. We describe 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 the pelvis and spine observed in humans could have emerged during hominid evolution.

Introduction

Our aim is to compare adult and intact neonatal pelves to identify pelvic modifications, which could have occurred during the acquisition of bipedalism in infancy, more precisely with trunk erectness and the formation of lumbar and dorsal curvature. The pelvic changes we expect concern the sagittal morphology of the pelvis in relation to the acquisition of a sagittal balance of the trunk on the lower limbs. Our hypothesis is that these pelvic changes might be the result of both gravity and development. In studies on the growth of the human pelvis (Le Damany, 1905, Waterman, 1929, Kummer, 1975, Abitbol, 1987a, Abitbol, 1987b, Abitbol, 1996, Berge, 1993, Marchal, 2000) the shape of the sacrum, a key pelvic modification, was linked to gravity, being straight in newborns and curved in adults. This sacral curvature was associated with the formation of the lumbar curvature, thus presenting a posterior concavity, in contrast to the anterior concavity of the sacrum (Le Damany, 1905, Abitbol, 1987a, Abitbol, 1987b). During hominid evolution, the acquisition of sagittal balance of the trunk on the lower limbs was a decisive stage in the transition from occasional to permanent bipedalism. The double S shape of the vertebral column was one of the most important evolutionary adaptations to bipedal locomotion, providing an ideal compromise between mobility and stability. Our hypothesis is that the sagittal morphology of the hominid pelvis would have been also modified in association with this major evolutionary adaptation.

The most important mechanical function of the pelvic girdle is to transmit the weight of the head, trunk and upper limbs to the lower extremities. This transmission occurs through the different pelvic joints. The pelvis includes six joints: the lumbosacral joint establishes the link with the vertebral column, and the paired hip joints with the lower limbs. The iliac bones of the pelvis are linked by three joints: a paired proximal sacroiliac joint and the pubic symphysis. The mechanisms of weight transfer from the vertebral column through the pelvis to the lower limb have been discussed previously by some authors (Fick, 1911, Kummer, 1962, Kummer, 1975, Stern and Susman, 1983, Berge, 1993, Abitbol, 1995, Sanders, 1998, Lovejoy, 2005). However, a morphological association between the shape of the pelvis and the shape of the spine in the context of sagittal balance of the trunk on the lower limbs has never been addressed. We aim to bring new insights to this complex question by using results we previously obtained on the complex composed of the vertebral column and pelvis in adults. Experimental studies using barycentrometry1 (Duval-Beaupere et al., 1992), showed the conditions required for an efficient sagittal balance of the trunk on the lower limbs. The center of gravity of the trunk (Fig. 1) is slightly anterior to the ninth thoracic vertebra and the trunk line of gravity acts anterior to the dorsal curvature but posterior to the lumbar curvature and the hip joints. The position of the line of gravity of the trunk in front of, or behind, the vertebrae and the coxo-femoral joints requires an opposing muscle force to ensure stability of the mechanical system. Failing such a harmonious weight distribution, inadequate muscular forces will be mobilized and muscular pains or compressive stresses on the vertebrae will arise. We define the efficacy of the sagittal balance of the trunk on the lower limbs in terms of minimal muscular expenditure and mechanical stress on the vertebrae and hip joints in adults.

Trunk erectness with formation of a distinct vertebral curvature entirely modifies the distribution of the weight of the head, trunk and upper limbs in relation to the vertebral, lumbosacral and hip joints. We believe that this new positioning of the vertebrae must be compatible with the maintenance of efficient balance. We propose to explore here the pelvic morphology using a sagittal pelvic variable, the angle of sacral incidence (Fig. 2), originally proposed by us in 1992 (Duval-Beaupere et al., 1992, Legaye et al., 1993, Marty et al., 1997, Boulay et al., 2006, Tardieu et al., 2008). In the sagittal plane, this angle is defined by the sacro-acetabular distance, linking the center of the sacral plate with the middle of the bicotyloïd axis, perpendicular to the center of the sacral plate. Thus, this variable represents the relative position of the centers of the sacral plate and of the acetabula. The angle of sacral incidence plays an important role in the sagittal balance of the trunk on the lower limbs since this anatomical variable, specific to each subject, is the geometric sum of the two positional variables: sacral slope (α) and pelvic tilt (β) (Fig. 2B). While standing, each individual varies these two positional variables in relation to the degree of incidence. We previously established very significant positive correlations between the degree of this angle and the degree of the lumbar curvature (Legaye et al., 1993, Legaye et al., 1998, Duval Beaupère et al., 2001, Duval-Beaupère and Legaye, 2004).

Since lumbar curvature develops in the child during infancy in association with gait acquisition (Tardieu, 2000), we hypothesize that a change in this angle also occurs during growth. In this context, by describing how the lumbopelvic complex is established during growth, this study could contribute to an understanding of the evolution of this complex in hominids in association with the acquisition of permanent bipedalism. We know that lower back mobility and the ability to develop a lordotic curvature played a central role in the origin of habitual upright walking. Now the question is when and how did the functional association between spinal curvatures and the pelvis observed in extant humans appear in hominid fossils. The first step to answer this question is to calculate the angle of sacral incidence in hominid pelves and compare these values with the range of variation in extant humans. If the fossil pelvis is associated with a complete lumbar column, we can discuss a possible functional link between spine and pelvis. If the pelvis is isolated, depending upon the value obtained, we could predict or reject the presence of a lumbar lordosis. Our closest relatives, the African great apes, exhibit an almost immobile lower spine because of the ‘entrapment’ of the lowest lumbar vertebrae between the ilia and because of the decreased distance between the last ribs and the iliac crests (Schultz, 1961). In the australopithecine fossils AL 288-1 and Sts 14, a shortening and pronounced broadening of the ilia and sacrum eliminated any restrictive contact between the lower lumbar vertebrae and the retroauricular portion of the ilia (Lovejoy, 2005). These two fossils are interesting to investigate as Sts 14 also presents a complete lumbar column. These observations will be complemented with data for the Gona pelvis belonging to Homo erectus, since it is a very well-preserved fossil specimen, as well as data for the pelvis KNM-WT 15000 from Nariokotome.

The neonatal pelvis has been studied by morphologists (Thomson, 1899, Le Damany, 1905; Yamamura, 1939; Boucher, 1957, Weaver, 1980, Holcomb, 1993) and has been compared with infant and adult pelves (Reynolds, 1945, Coleman, 1969, Wangermez, 1973, Bruzec and Soustal, 1984, Majo, 1992, Berge, 1993, Berge, 1995, Berge, 1996, Marchal, 1994, Williams and Orban, 2007). However, with the exception of those studied by Le Damany (1905), the neonatal and young pelves used in these studies were dried skeletons from osteological collections. In these collections, only the ossified parts of the pelves are preserved. However, much of the pelvis is still cartilaginous at this stage and osteological specimens may thus bias observations of shape in neonates. Consequently, in this study, we compare adult pelves with intact neonatal pelves that include the cartilaginous parts.

Section snippets

Human pelves

Adult and neonatal human pelves were studied. The adult sample included 51 pelves of known sex (26 male, 25 female) with no pathological history (collections of the National Museum of Natural History, the Laboratory of Anthropology of the University P. and M. Curie and the Faculty of Medicine of Paris).

The neonatal sample included 19 intact pelves of known sex (nine male and ten female) with no pathological history (collections of the National Museum of Natural History). Anatomical dissections

Data acquisition

An electromagnetic device (Fastrak System from Polhemus, distributed in France by Theta Scan) was used to record three-dimensional coordinates that retain the full geometry of 47 homologous anatomical landmarks for each pelvis. Numbering and description of the 47 landmarks are provided in Appendix A. The type of the landmarks is also given according to the classification proposed by Bookstein (1991).

To test intra-observer error using the Fastrack system, the same pelvis was measured three

Precision of measurements

The global average error value of the measurement of a point indicating intra-observer reliability was 1.28 mm (S.D. = 0.79) for the adult pelves and 1.06 mm (S.D. = 0.94) for the newborn pelves. Inter-observer error was 2.24 mm (S.D. = 1.57) for adult pelves. It was 4.00 mm (S.D. = 3.36) for newborn pelves. Given this relatively large inter-observer error, we decided to have only one person (C. T.) measure all of the newborn pelves. Thus, the error pertinent to the present analysis is the

Discussion

Our data indicate that the shape of the pelvis changes between infancy and adulthood. The main feature identified in the literature as changing from newborns to adults with gravity, the curvature of the sacrum, was not quantified explicitly but is clearly visible on the graphical representations of the mean pelves of newborns and adults (Fig. 4B) and is associated with an increased sacral slope.

Our results for the angle of incidence of the newborns were similar to those reported in an analysis

Conclusion

Our review of the reshaping of the pelvis and vertebral column during growth in humans has provided new insights in the evolution of the pelvic–vertebral complex in hominids. We compared adult and intact neonatal pelves, using, as representative of the sagittal morphology of the pelvis, the angle of sacral incidence, a parameter which is tightly correlated with the degree of lumbar curvature in adult subjects and which plays an important role in sagittal body balance. In newborns, the vertical

Acknowledgments

We thank M. Herbin, curator of the collections of comparative anatomy of the National Museum of Natural History, V. Delmas, curator of the collections of the Faculty of Medicine of Paris and F. Desmoulin, curator of the collection ‘G. Ollivier’ of the Anthropology Laboratory of Paris VI University. We specifically thank M. Haeusler for the measurement of the Sts 14 and AL 288 pelves. We are grateful to Pr. J. Dubousset for his long shared surgical and research expertise in the vertebral column

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