Article pp.208-216 du Vol.25 n°3-4 (2013)

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NOTE /NOTE

Three-dimensional analysis of the pelvi-femoral complex: its mechanism and development. Evolutionary and clinical implications*

Analyse tridimensionnelle du complexe pelvi-fémoral : son fonctionnement et sa mise en place au cours de l’ontogenèse. Dimension évolutive et applications cliniques

N. Bonneau

Abstract Bipedalism results in strong constraints on the human hip joint. This joint ensures transmission of the forces between trunk and lower limbs. This PhD work addresses questions in physical anthropology, evolutionary biology and clinical orthopaedics.

An important methodological study was conducted in order to propose accurate methods to determine the three- dimensional axes of the two neighbouring components of the human hip joint, i.e. the acetabular region and the proximal femur. Next, variations in the three-dimensional orientations of the acetabulum and the femoral neck were quantified on a sample of modern humans. To better understand the nature of these variations, a review of the biomechanical literature was performed, and ontogenetic analyses were conducted.

An integrative analysis revealed complex relationships between the biomechanical systems governing the three- dimensional orientations of the acetabulum and the femoral neck. Some forces are shared by the two systems, making coherent the covariations quantified between the axes of the acetabulum and the femoral neck. However, each system is also governed by independent forces resulting in a low concordance of these same axes in a bipedal posture. We suggest that this poor concordance in a bipedal posture may partly be due to the phylogenetic history of the human hip joint. To test this hypothesis, comparative analyses were pursued and showed that maximal concordance was obtained

for the generaHomo,Pan,GorillaandPongo in a quadrupedal posture.

Keywords Hip joint · Bipedal gait and posture · Acetabulum · Femoral neck · Hominoids

RésuméLa bipédie induit de fortes contraintes mécaniques sur l’articulation de la hanche humaine qui assure la transmission des forces entre le tronc et les membres inférieurs.

Les enjeux de cette thèse concernent l’anthropologie biolo- gique, la biologie évolutive et l’orthopédie clinique.

Un important travail méthodologique a été réalisé afin d’obtenir des méthodes fiables de détermination des axes tri- dimensionnels des deux composantes osseuses de la hanche, à savoir la région acétabulaire et l’extrémité proximale du fémur. Puis, les variations des orientations tridimension- nelles de l’acetabulum et du col fémoral ont été quantifiées sur un échantillon d’Hommes modernes. Afin de comprendre la nature de ces variations, une synthèse biomécanique et des analyses ontogénétiques ont été réalisées.

Une analyse intégrative a révélé la complexité des liens existant entre les systèmes biomécaniques gouvernant les orientations de l’acetabulum et du col fémoral. Les deux systèmes sont soumis à certaines forces identiques expli- quant les covariations quantifiées entre l’axe de l’acetabulum et celui du col fémoral. Pourtant, chaque système est influencé par des forces qui lui sont propres, responsables de la faible concordance des deux axes en station bipède.

Nous avons proposé que cette faible concordance soit imputée à l’histoire phylogénétique de l’articulation.

Afin de tester cette hypothèse une étude comparative a été menée et révèle que la concordance maximale est obte- nue pour les genresHomo,Pan,GorillaetPongoen posture quadrupède.

Mots clésArticulation de la hanche · Locomotion et posture bipèdes · Acétabulum · Col fémoral · Hominoïdes

N. Bonneau (*)

UMR 7179–Muséum national d’Histoire naturelle/CNRS, CP 55 Pavillon d’Anatomie Comparée,

57, rue Cuvier 75231 Paris cedex 5, France ; UFR STAPS–Université Paris Sud XI, Bât 335, 91405 Orsay cedex, France

e-mail : nbonneau@mnhn.fr

*Cette thèse a reçu le prix de la Société d’anthropologie de Paris 2012

DOI 10.1007/s13219-013-0087-5

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Introduction

Although numerous primates use bipedal locomotion to some degree, humans are characterized by a permanent bipedal gait and posture. Compared to quadrupeds, the human bipedal posture entails an important decrease of the base of support and a rise of the body centre of mass, two disadvantages from a biomechanical static point of view. In response to the constraints imposed by the erect posture, the skeleton of our ancestors was adaptively modified over the course of evolution. In the literature, human traits which could be functionally involved in bipedal gait and posture were identified, including hip morphological traits [1-18].

The hip joint, a diarthrosis which articulates the acetabular region with the proximal femur, occupies a central place in the locomotor skeleton. It plays an important role in body support and the transmission of the forces between the trunk and lower limbs. Consequently, the hip joint is of prime importance in the study of human evolution as additional data are needed to document and better understand the acquisition of bipedal locomotion in the human lineage. Moreover, a precise knowledge of the hip joint has important clinical implications and may help advance hip surgery and functional rehabilitation.

In this PhD work, a functional integrative analysis of the hip joint was conducted. We hypothesized that the functional integration between the two neighbouring components of the joint was favoured in the course of hip evolution resulting in joint performance and stability. A joint fulfils two main functions which are, first, the transmission of the mechanical forces and, secondly, the ability or inability to perform specific movements [19]. The joint structure, and particularly its orientation, reflects the need to ensure these two main functions. Therefore, this work focused on the orientations of the acetabulum and the femoral neck.

First, an important methodological study was conducted in order to propose accurate methods to determine the three- dimensional axes of the two osseous neighbouring components of the human hip joint, i.e. the orientations of the acetabulum and the femoral neck. Based on these three-dimensional methods, variations in the orientations of these two components were analysed before exploring co-variations between them in order to evaluate the degree of functional integration at the hip joint.

Three-dimensional methods for the morpho- functional analysis of the hip joint

Methods for the determination of the three-dimensional orientation of both the acetabulum and the femoral neck

In the literature the orientations of both the acetabulum and the femoral neck have frequently been quantified using

angles such as the anteversion and the inclination [20-32].

These parameters allow no more than a partial description of the global orientation of the two components as they describe their orientations in only a single plane of the three-dimensional space. Currently, with the rapid development of three-dimensional imaging, it becomes increasingly important to use accurate three-dimensional orientation which provides more informative data. Thus, we first developed accurate methods for the quantification of the three- dimensional orientation of the two neighbouring components of the hip joint.

Concerning the acetabulum, the use of a three-dimensional axis perpendicular to the plane that passes along the osseous rim had been proposed by Calandruccio [33]. However, the osseous rim is not regular (Fig. 1) and the anterior indentation described by different authors [34-38] was a problem in the direct application of Calandruccio’s method. More precisely, the problem concerned the unknown nature of this indentation: is the anterior rim dysplasic and the orientation of the posterior rim the functional one? Or does the anterior part of the rim have a functional meaning and has to be included in the determination of the three-dimensional orientation of the acetabulum? To answer this question, anatomical dissections on fresh hip joints were performed at the“Centre du Don des Corps” (Paris Descartes, France) in order to quantify the three-dimensional orientation of the labrum, a fibrocartilage known to fill up inequalities of the bony rim. Our results provided evidence that the osseous acetabular rim is better represented by two planes, an anterior and a posterior plane, rather than by a single plane (Fig. 1) [39]. As for the labrum, its three-dimensional orientation was precisely described in relation to the orientations of the anterior and the posterior parts of the osseous rim: in healthy middle-aged individuals, the orientation of the labrum is closer to the orientation of the anterior rim which forms an important angle with the posterior one; in aging individuals, the angle between the anterior and the posterior parts of the osseous rim decreases and the labrum takes an intermediate position between these two parts. These results revealed the functional meaning of the anterior rim and it was concluded that the quantification of the three-dimensional orientation of the acetabulum has to con- sider the total osseous rim. Based on our results the three- dimensional orientation of the labrum can be predicted with an error of 2° using a predictive equation based on the orientations of the anterior and the posterior parts of the osseous acetabular rim [39]. This study has important implications in paleo-anthropology, as no soft tissues are preserved, and in a clinical context for the improvement of the surgical techniques.

Concerning the proximal femur, numerous authors pointed out the difficulty to determine the true femoral neck axis. However, the femoral axis was frequently identified visually only on two-dimensional views. Some authors

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attempted to propose more objective methods (e.g. [21]), however they were difficult to apply in three dimensions.

To our knowledge, a single study, the one of Kim and col- laborators [40], proposed a semi-automatic three- dimensional method. However, this method used the geometric centre of the femoral head even though Kingsley and Olmsted [21] demonstrated that the centre of the head was not necessary always positioned in line with the neck axis.

Although that our results finally disagreed with the mea- surements of Kingsley and Olmsted [21], it was neverthe- less important to develop a method which uses only the femoral neck itself, rather than external structures [41].

In a first approximation, the femoral neck was modelled based on a circular cross-sectional cylinder as it had been suggested in the literature [42-44]. However, a re-

examination of the complex three-dimensional architecture of the proximal femur provided evidence that this model was too simplistic as the femoral neck showed a strong asymmetric structure: the cortical bone is thicker in the inferior part of the neck than the superior part, and the medial trabecular system observed in the inferior part of the neck demonstrates a different orientation compared with the aci- form trabecular system crossing the superior part. Accord- ing to these observations, a method based on a three- dimensional geometric model using successive ellipses was developed (Fig. 2). This model reproduces the antero- posterior flattening of the neck, and the narrowing at the middle of the neck. It results in an accurate determination of the three-dimensional axis of the femoral neck with an intra-observer measurement error equal to 2° [41].

Fig. 1 The osseous acetabular rim is limited by the anterior and posterior horn tips (indicated by A and D). The osseous rim is divided in an anterior part (from B to A and D to C) and a posterior part (from B to C). The osseous acetabular rim is not regular as an indentation in the anterior rim is observed. The three-dimensional orientation of the labrum, a fibrocartilage known to fill up inequalities of the bony rim (illustrated in hatched areas), was quantified on fresh cadavers and our results provided evidence that the three orientations of the anterior rim (VA), the posterior rim (VP), and the labrum (VL) are aligned in a same plane. In healthy middle-age individuals the orientation of the labrum is closer the orientation of the anterior part that the posterior part implying that the anterior rim has a functional meaning /Le rebord acétabulaire osseux s’étend de la corne antérieure à la corne postérieure (A et D). Ce sourcil est divisé en une partie antérieure (de B à A et de D à C) et une partie postérieure (de B à C). Le rebord acétabulaire n’est pas régulier notamment à cause de la présence d’une indentation dans le sourcil antérieur. L’orientation tridimensionnelle du labrum (figuré en hachuré), un fibrocartilage comblant les irrégularités du sourcil osseux, a été quantifié sur une série de cadavres frais et nos résultats ont montré que les trois orientations du rebord antérieur (VA), du rebord postérieur (VP) et du labrum (VL) sont alignées dans un unique plan. Chez des individus d’âge moyen et en bonne santé, l’orientation du labrum se rapproche de celle du rebord osseux antérieur montrant que le rebord antérieur à une réelle signification fonctionnelle

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Superimposition of data

Once three-dimensional methods were developed, comparisons between different individuals and species were performed, raising the question of the positional reference.

According to the disciplines, the available material, and the authors, the anatomical planes of reference used to define the position of pelves and femora changed resulting in difficult comparisons between studies [26]. However, more important is that the superimposition of bones based on anatomical planes does not take into account the inter-individual variability of the landmarks used to define these planes. For example, the superimposition of pelvises using the Lewin- neck plane [23] is blind of the inter-individual variations of the anterior superior iliac spines and the superior points of the pubic symphysis, which defined this plane. Yet, these variations influence the position of the pelvis in the space and, consequently, the measurement of the acetabular orientation. We also noted that the use of the Lewinneck plane for the pelvis superimposition needs the reassembly of the three pelvic bones. Yet, we demonstrated the effect of reassembly

on pelvic shape thus complicating this procedure [45]. A Generalized Procrustes Analysis [46,47] traditionally used in geometric morphometrics was used here to optimize the bone superimposition. A custom-designed function was developed in the Rmorph library [48] for the freeware R v.2.11.0 [49] leading a passive superimposition of functional structures with no homology, using homologous landmarks [41,45]. The use of geometric morphometric methods for the establishment of the reference space has the advantage to, first, minimize the effect of the inter-individual variations of the homologous landmarks used in the superimposition, thus rendering the process more objective, and secondly, to provide tools for the precise quantification and analysis of these variations. Questions concerning the reference space/plane are of principal importance in a clinical context, especially in the development of accurate techniques for computer-assisted surgery for total hip arthroplasty.

These three-dimensional methods provide accurate tools to perform a morpho-functional analysis of the hip joint in order to better understand the functioning and the development of this joint. First, analyses performed of each component of the joint are described, and second, results derived from the integrative analysis are presented.

Morpho-functional approach of the human hip joint

The pelvic component of the hip joint: the acetabular area

The three-dimensional analysis of the orientation of the labrum based on 20 fresh cadavers (10 women and 10 men, aged from 56 to 93 years old, collected at the“Cen- tre du Don des Corps”; Paris Descartes, France) shed light on a plane which was never described before: the three orientation vectors of the anterior and posterior parts of the osseous rim, and the labrum form an unique plane which is perpendicular to the axis including the points corresponding to the continuation of the iliac crest and the ischiatic axis on the acetabular rim (Fig. 1) [39]. A review of the biomechanical literature concerning the acetabular region was useful to interpret these results. In a first approximation, the acetabulum is frequently considerate as a ball and socket joint. In reality, variations from this simplistic model have been described and implications in the acetabular biomechanics have been demonstrated. First, the general horseshoes- shaped structure of thefacies lunataoptimizes the stress distribution along the contact surface and refocuses the peak of maximal constraints to the centre of the surface rather than close to its edge [50]. Moreover, rather than a sphere this surface correspond to an arched dome [51-53]. The compli- ance of acetabular bone and cartilage allows deformations Fig. 2 The three-dimensional orientation of the femoral neck was

quantified using a three-dimensional model based on successive cross-sectional ellipses / L’orientation tridimensionnelle du col fémoral a été quantifiée grâce à un modèle géométrique utilisant des ellipses successives

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of this arched dome undergoing high constraints, e.g. during the one-legged stance of the walking. Under low loads, e.g.

the swing phase, the femoral head contacts the acetabular surface in its antero- and postero-superior parts while under high loads the acetabular roof and the horns of the facies lunatacome in contact with the femoral head [54- 59]. The incongruity between the acetabular roof and the femoral head favours not only the stress distribution along the articular surface but also the circulation of synovial fluid [60]. Finally, the acetabulum is integrated in a highly struc- tured mechanical system, the one of the pelvic girdle.

Indeed, the place and the functioning of the acetabulum should be observed in relation to the trabecular network which is known to translate the main orientations of the constraints passing though the pelvis [61-63]. A three- dimensional analysis of this network visualizes three less constrained areas between the main trabecular systems (Fig. 1). The two points defined in our work as being the landmarks limiting the anterior and the posterior parts of the osseous acetabular rim (B and C in Fig. 1) as well as the anterior horn tip of thefacies lunata (A in Fig. 1) are clearly localized at these less constrained areas. We also observed that the plane formed by the three orientations of the anterior rim, the posterior rim, and the labrum is precisely adjusted to these areas [39]. During aging, the compli- ance of the acetabular tissues decreases and the structure is affected. Our results demonstrated a closing of the angle between the anterior and the posterior parts of the osseous rim, as well as an alteration in the relationships between the acetabular orientation and the global trabecular network of the hip bone [39].

An ontogenetic analysis of the hip bone based on a sample of medical scanner data of 54 children (23 girls and 31 boys) aged from 0 to 18 years old, allowed us to better understand the relationships between the acetabular development and the pelvic trabecular network. Data collection on children free of skeletal pathologies was performed by Dr.

Gorincour at the Hospital La Timone (Marseille, France).

According to our observations, the architecture of the acetabular region is strongly correlated with the hip bone development mainly controlled by the triradiate cartilage [64-67].

Constraints passing though the pelvic girdle seem to have direct effects in growth speed and orientation of the three flanges of the triradiate cartilage. Forces arriving at the lower lumbar vertebrae are transmitted through the sacro- iliac surfaces before running both along the arcuate lines and the greater sciatic notch. A part of the forces are transmitted to the lower limbs while another part transit through the ischium and the pubis before being distributed both in the superior and the inferior parts of the obturator foramina.

This detailed observation of the pelvic trabecular network showed that the three flanges of the cartilage are not submitted to the same constraints. We suggested that these differ-

ences explain the irregular morphology of the osseous acetabular rim, as each flange of the tri-radiate cartilage growths in a specific direction and thus forms a part of the rim with its own orientation [39]. According to this developmental model, we suggested that the pelvic shape can directly influence the final acetabular orientation. In this way the different acetabular orientations between adult men and women could be explained partly by the pelvic shape difference.

The femoral component of the hip joint: the proximal part of the femur

Compared to the acetabular region, the architecture of the proximal femur is rather dependent on the forces induced by the muscular system. The femoral neck is developed, on the one hand, from theperiosteumwhich forms the cortical bone, and on the other hand, from two growth plates–the capital epiphysis and the apophyseal plate of the greater trochanter – which form the trabecular bone [68,69].

These different growth sources are strongly influenced by the action of the muscles surrounding the pelvi-femoral complex. The abductor muscles of the hip, such as theglu- teus medius and the tensor facia latae, play an important role in the growth of both the periosteum and the growth plates [9,70-74]. Moreover, the growth orientation and speed of the apophyseal plate of the greater trochanter, frequently underestimated in hip biomechanical models, are also influenced, on the one hand, by the action of the ilio- tibial tract in relation to the knee extensors and thevastus lateralis[73,74], and on the other hand, by the action of the adductor muscles such as the quadratus femoris, and the obturator internus and externus. As both modeling and remodeling of the femoral neck are influenced by this muscular environment, inter-individual variations in the muscle insertions [75,76] may play a role in the femoral neck orientation. Moreover, differences in the load-bearing behavior in relation to habitual activities (cultural, sportive, profes- sional, etc) may influence the muscular activity level and thus the final femoral neck orientation. The great variation in the orientation of the femoral neck observed in a sample of 91 femora coming from both the SIMON collection (University of Geneva, Switzerland) and the collection of the National Museum of Natural History (Paris, France) can thus be explained by this biomechanical system being submitted to the muscular environment [41]. This sample included 43 right femora and 48 left femora from 50 specimens of modern Homo sapiens (21 women and 29 men) aged from 18 to 87 years old. Using this sample, a significant effect of sex (p < 0.001) and age (p = 0.03) on the three-dimensional orientation of the femoral neck was observed [41]. Moreover, we demonstrated in an additional study that the femoral neck is submitted to constraints induced by limited space available inside the maternal

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intrauterine cavity during prenatal development [77]. This mechanism could contribute to the great variability of the femoral neck orientation at birth.

Functional integrative analysis of the hip joint

The biomechanical synthesis regarding both the acetabular region and the proximal femur revealed complex relationships between the biomechanical systems governing the three-dimensional orientations of the acetabulum and the femoral neck. The forces induce by the body weight and passing through the hip joint, but also forces induced by muscles attached both on the pelvis and the femur such as the abductor muscles, make the two neighboring structures interdependent. It can explain the significant covariations (p < 0.001) quantified between the axes of the acetabulum and the femoral neck in the sample of 57 individuals (26 women and 31 men) studied both at the University of Geneva (Switzerland) and the Paris Museum (France) (Fig. 3) [78]. Patterns of covariation between the three-

dimensional vectors of orientation of the acetabulum and the femoral neck were quantified using both the RV coeffi- cient of Escoufier [79,80] and the two block partial least- squares (2B-PLS) [81-83] method. However, each system depends on proper forces. The biomechanics of the acetabular region is mainly related to the osseous morphology of the pelvic girdle while the biomechanics of the femoral neck is strongly influenced by muscular activity. This observation was key to understand the low level of concordance observed in the transverse plane between the axis of the femoral neck and the one of the acetabulum obtained on this same sample of 57 individuals [78]. The poor concordance resulting in an uncovered femoral head at its antero- superior part in a bipedal posture has already been observed in the literature [84-86] and has been correlated to some pathologies, such as premature osteoarthritis [86,87].

We suggested that the low level of concordance between the three-dimensional axis of the acetabulum and the three- dimensional axis of the femoral neck in a bipedal posture may partly due to the phylogenetic history of our species.

Indeed, the hip joint of modern humans evolved during

Fig. 3 In a bipedal posture, as illustrated in A, the human hip joint demonstrates a poor concordance between the axis of the acetabulum and the axis of the femoral neck, more especially in the transverse plane (C). In this illustration are represented the orientations of both the acetabulum and the femoral neck in the frontal plane (B) and the transverse plane (C) based on a sample of 57 individuals. Mean orientations appear in solid lines and inter-individual variations in dotted lines /La hanche humaine démontre une faible concordance entre l’axe de l’acétabulum et l’axe du col fémoral en station bipède (comme figuré en A) et plus particulièrement dans le plan transverse (C). Dans cette illustration ont été représentées les orientations de l’acetabulum et du col fémoral d’un échantillon en vue frontale (B) et en vue transverse (C) de 57 individus. Les orientations moyennes apparaissent en lignes pleines et les variations inter- individuelles en lignes pointillées

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several million of years from an ancestral joint which was adapted to different functions related to locomotion and obstetrical demands of the last common ancestor. In the course of evolution by natural selection the morphology of the hip joint progressively evolved in the human lineage in relation to the acquisition of the permanent bipedal gait and posture, while respecting the new obstetrical constraints induced by the increase in brain volume of newborns. How- ever, this evolution remained the result of evolutionary tinkering with the existing pieces [88] as it is based on a preexisting joint whose architecture imposes a number of physical limits. Thus, although a perfect concordance between the three-dimensional orientations of both the acetabulum and the femoral neck in a bipedal posture, increas- ing the level of congruence of the articular surfaces, would be expected in order to optimize the function of the hip joint in the context of bipedal locomotion, reality shows that, on the one hand the phylogenetic history, and on the other hand the evolutionary compromise induced by the implication of the joint in other functions lead to a different mean shape.

In order to better understand the evolutionary framework and the effect of the locomotor behavior on the hip morphology, a comparative study of the joint was performed in Hominoids. The study included 66 specimens ofHomo sapiens, 48 ofPan(troglodytesandpaniscus), 36 ofGorilla (gorilla and beringei) and 22 of Pongo pygmaeus con- served in the collections of the National Museum of Natural History (France), the Anthropological Institute and Museum (Switzerland), the Institut Royal des Sciences Naturelles de Belgique (Belgium) and the Royal Museum for Central Africa (Belgium). Results demonstrated the complexity of the compromise between mobility and stability required for hip joint efficiency. Regarding Orangutans, the great mobility of the lower limbs is ensured in part by a shallow acetabulum and a very open femoral neck. In contrast, the hip joint of Gorillas has to support high loads and thus needs stability: a deep acetabulum and a closed femoral neck were observed. Comparison of the relationships between the three-dimensional orientation of the acetabulum and the orientation of the femoral neck on the hominoid sample demonstrated that the best concordance between the three- dimension axis of the acetabulum and the three- dimensional axis of the femoral neck is always obtained in quadrupedal posture regardless the habitual locomotor behavior used by the different genders or species. A total concordance of the hip joint in quadrupedal posture appears natural in the genera Gorilla and Pan as they spend an important part of their time in this posture. However, this concordance of the human hip joint in a quadrupedal posture on an inclined plane [89], rather than in a bipedal posture, is surprising further suggesting that the shape of the human hip joint is constrained by its quadruped ancestry.

Conclusion

In summary, using new thee-dimensional methods developed to accurately determine the orientation of the two neighbouring components of the hip joint, this work provided a better understanding of the functioning and the development of both the acetabular region and the proximal femur. One of the most unexpected results is that the quadrupedal origin of our species is recorded in the three-dimensional orientations of the hip joint.

Both stability and mobility are required to have an effi- cient hip joint. Currently, we are developing a study concerning the three-dimensional hip joint mobility, and more precisely the nature of the exact three-dimensional relationships between the acetabulum and the proximal femur during the maximal range of motion.

AcknowledgmentsFirstly, I would like to thank the Société d’Anthropologie de Paris for awarding me the price 2012.

I am grateful to Christine Tardieu and Olivier Gagey who supervised my PhD and Anthony Herrel for his helpful comments. I benefited from the morphometric facility of the Paris Museum (UMS 2700 CNRS –MNHN: ‘‘Plate- forme de Morphométrie’’) and a special thank is made for Michel Baylac. Finally, I thank all the curators of the collections visited for this work: Didier Berthet, Emmanuel Gilis- sen, Mark Herbin, Robert Kruszynski, Christine Lefèvre, Georges Lenglet, Philippe Mennecier, Geneviève Perréard, Marcia Ponce de León. Lastly we are grateful to the reviewers who provided helpful comments on this work.

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