Cranial and Pelvic “Vertebrae” Are They Real Vertebrae?

Fig. 1

Re-segmentation of the craniocervical region. Embryological origin of the base of the skull and the cranial part of the cervical spine. Note the contribution of the proatlas in the formation of the occipital bone (pink and blue) (Bernard [6])

Basicranial Chondrogenesis (Figs. 2, 3, 4, and 5)

The basic basicranial skeleton appears in the form of cartilage islands in the basicranial mesenchyme. This mesenchymal tissue has two origins: the cells of the neural ridges and the paraxial somitic mesoderm [8].

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Segmentation of the chondromesoblast at 4 weeks, occipital somites and notochord

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Formation of the chondrocranium at 6 weeks

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Fusion of chondrocranium cartilage at 12–13 weeks

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Chondrocranium and its expansions (according to Mugnier [7])

The notochord, surrounded by parachordal cartilages , terminates at the level of the pituitary gland at the level of the future sella turcica, a true center of the base of the skull where we find pituitary cartilages. Rostrally prechordal cartilages (trabecular cartilage) and their lateral expansions (otic capsule and chondroethmoid) derive from the neural ridges. Thus the chondrocranium is formed from three pairs of cartilaginous foci that will fuse to form the basement of the brain: the prechordal cartilages, the pituitary cartilages, and the parachordal cartilages.

Dorsally, around the seventh week, the perinotochordal mesenchyme becomes the parachordal cartilages that become the postsphenoidal part of the base of the skull. The parachordal cartilages represent the outline of proatloid vertebrae: basipostsphenoid and basioccipital, separated by future synchondroses, characteristically modified intervertebral discs.

The skull protects the brain from the outside via calvarial and facial membranous bones. The base is the border traversed by the peripheral cranial nerves and the spinal cord. Thus, between the cartilaginous drafts circulate neurovascular structures. The expansion of the cartilaginous parts until their fusion will organize the foramina of the skull base to the input or output of these elements of the cranial cavity.

Finally, the cephalic skeleton of the fetus is in place at 3 months and includes a cartilaginous chondrocranial chassis whose anterior and posterior parts have a different origin [8, 9]. The base of the postsphenoid skull has a common somitic origin with the spine. The presphenoidal part depends on the neural ridges such as lateral expansions or capsules in relation to the sense organs.

Craniofacial Ossification (Figs. 6 and 7)

Some bones have a double origin such as the occipital bone: endochondral for its basilar part around the foramen magnum and membranous for its flat part.

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Different modes of ossification

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Synchondrosis of the base of the skull (Couly [9], Stricker [10])

The ossification of craniofacial bones has two origins: endochondral, from cartilaginous and membranous tissues, from the ectomesenchymal cells of the cephalic neural crest.

The calvarium and many bones of the facial skeleton are from membranous ossification. Ossification points appear within the ectomesenchyme constituting the embryonic skull. Ossification is centrifugal to create conjunctive boundaries between bone parts.

These junctions are synfibroses or cranial sutures which allow the passive and functional secondary [11] growth of the bones controlled by the neighboring structures (brain, eyeball, muscular tension, nasal ventilatory flow…).

The base of the skull develops as an enchondral ossification , starting from the cartilaginous base. Its growth is independent, or primary, determined genetically and under hormonal control [9, 11]. The borders between the bony parts of the base of the skull are synchondroses which are areas of growth by endochondral ossification whose structure is comparable to that of the epiphyses of the long bones. They have a bilateral growth area or mirrored “dual action epiphysis” according to Scott [12].

The occipital bone has a double origin: endochondral for its basilar part surrounding the foramen magnum and membranous for its squamous (flat) part [6].

Craniofacial Growth

Synchondroses determine the growth of the base of the skull in three planes of space. They remain active for some until the end of growth [3]. The sphenoethmoidal, intrasphenoidal, and intraoccipital synchondroses mainly involved in sagittal growth come from the base of the skull. The spheno-occipital synchondrosis contributes to the sagittal and vertical growth of the base. The latter disappears at the age of 20 and constitutes, with exosuboccipital and exobasioccipital synchondroses, evidence of the multi-vertebral origins of the basipostsphenoid and occipital bones [9].

During human evolution, the brain grows and bipedalism, subject to gravity, appears. The head is balanced on top of the column of the biped. The column pulls the occiput backwards bringing the foramen magnum horizontally. The cranial volume increases, and the basicranial angle closes. The face, very dependent on the skull base to which it is attached, involutes proportionally to the increase in brain capacity and in parallel with changing dietary constraints.

During morphogenesis, one can observe the flexion of the skull base between the basi- and presphenoid. This curvature begins at the level of spheno-occipital synchondrosis [13] and will depend on phenomena of periosteal apposition-resorption. Finally, from a phylogenetic and morphogenetic point of view, a counterclockwise rotation of the occipital bone and a clockwise rotation of the sphenoid bone are observed.

The superficial skeleton (upper skull) exhibits membranous ossification and adaptive growth under the influence of extrinsic forces such as encephalic expansion on the calvarium resting on the basicranial base. Facial growth depends on the growth of the base of the skull in its middle and anterior part. The flexion phenomena of the base of the skull affect the sagittal maxillomandibular balance [14].

The chondroethmoid emits extensions that support facial intra-membranous ossification. The mesethmoid (future nasal septum) and ectoethmoid (future lateral masses) [9] are at the origin of the vertical sutural growth and by the nasofrontopremaxillary and palatal facial sagittal thrust [10, 15]. Laterally, the otic capsules emit ventral extensions: the cartilages of Meckel and Richert. Meckel’s cartilage will serve as a guardian of mandibular morphogenesis (Fig. 5).

Facial growth is equally dependent on the manducatory and ventilatory functions. Normal mandibular growth is dependent on that of the middle level of the face via the dental occlusion (the relationship between the maxillary (upper) and mandibular (lower) teeth when they approach each other). The nasal breathing flow also has a considerable influence on the growth of the middle floor of the face and maxillomandibular harmony.

Thus vertebral and facial growths are linked within the base of the skull as the vertebral column is postsphenoidal and as the face is presphenoidal. Moreover, in clinical practice, there are many facial asymmetries related to basicranial and/or vertebral asymmetry (Fig. 8).

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Facial asymmetry following a congenital torticollis

Conclusion

If the center of gravity of the head is just behind the turcica sella area [16], we can consider that it separates the vertebral column at the back from the face in front. Indeed, the postsphenoidal portion of the base of the skull and the craniocervical vertebral junction is of somitic origin. The ossification is of endochondral type through synchondroses, essentially basicranial intervertebral discs. The ventral part of the skull base contributes significantly to the morphology of the face. Morphological growth abnormalities are associated with each other: facial scoliosis, asymmetries of the skull base, cervical postural disorder, vertebral or pelvic abnormalities.

Formation, Growth, and Aging of the Pelvic Ring

The pelvic ring includes the sacrum (constituted by the fusion of the five sacral and the four coccygeal portions) and the two coxal bones (articulating with the sacrum at the level of the sacroiliac joints, considered as quite immobile and coming from the fusion of the three bones: ilium, ischium, and pubis). At this articulation with the inferior limb, the pelvic girdle is not detached from the spine, as opposed to the scapula at the origin of the superior limb due to the disappearance of the basilar bone (Fig. 9).

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Comparison of pelvic and thoracic (superior and inferior) limb girdles

Phylogenesis

With man’s evolution to bipedalism, there is an increase of the angle of pelvic incidence, which expresses the size of the pelvis and the sacrococcygeal angle, which measures the curvature of the sacrum.

Tardieu [17] made a 3D study of the pelvic ring of hominoid fossils, 19 newborns and 50 adults. She was interested in the evolution of the shape of the hip bone and the sacrum during the acquisition of walking and, as we will see later, during growth. This analysis focussed on the angle of pelvic incidence [18] and also an original angle, entitled the “ bow angle” or iliopubic angle , formed by a mid-sacral endplate to a midacetabular line and a line from the mid-acetabulum to the anterior aspect of the pubis (Fig. 10). This angle, which measures the anteroposterior width of the pelvis, increases during primate evolution to bipedalism as well as pelvic incidence that evaluates the width of the pelvis at its middle part.

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Iliopubic angle (1), pelvic incidence (2), ilioischial angle (3), sacrococcygeal angle (4)

According to Tardieu [17], as for Morvan [19], the iliac wings widen and become sagittalized (Fig. 11) in the evolution of bipedalism. The pelvis thus widens in the anteroposterior direction (from where the pelvic incidence increases) (Fig. 12), towards the front (where the iliopubic angle increases) and finally opens superiorly to facilitate the viscera and the trunk.

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Sagittalization of left iliac wings from gibbon to homo sapiens on superior view

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Pelvic incidence increases with sacrocotyloid distance in lateral (a) and frontal (b) views (Tardieu [17] and Morvan [19])

The sacrum evolves by curving forward. Abitbol [20] uses the angle between the sacral curvature along the anterior wall of the body of the S1 and the anterior wall of L5. The sacrococcygeal angle (Marty [21]) is traced between a line perpendicular to the upper endplate of S1 and a second perpendicular to the endplate of S5; this angle increases with the acquisition of bipedalism (Fig. 13), according to Tardieu [17]. The widening and sagittalization of the iliac wing, and the curvature of the sacrum in the acquisition of bipedalism parallel with the increase of lumbar lordosis are explained by the action of the extensor muscles (lumbosacral mass, glutes, and hamstrings) but also, especially for the sacrum, by the tension of strong ligaments such as sacrospinal ligaments (Figs. 14, 15, and 16). Finally, to complete this work (Tardieu [17]), we are reminded of the study performed on the pelvic ring of Lucy, the Australopithecus africanus, three million years old: where the pelvis is tilted backwards, with a small pelvic incidence and shape and orientation of the intermediate iliac wings between chimpanzee and Homo sapiens (Fig. 17).