Classification of Craniovertebral Junction Abnormalities

A wide spectrum of congenital, developmental, and acquired abnormalities exist at the CVJ and may occur singularly or in multiples in the same individual. The pathology of these abnormalities is extensive. An attempt at a working classification has been provided in Table 9.1 , but it must be appreciated that there are overlapping causes within this classification.

Embryology and Development at the Craniovertebral Junction

The bony cranial base is developed by a process of enchondral ossification, in which a cartilaginous framework is first developed and subsequently resorbed with further deposition of bone caused by distorting forces, such as brain development and the development of the eye.3 The cranial base, as well as the clivus, elongates by sutural growth at the sphenooccipital and sphenopetrosal synchondrosis. There is further sutural growth along the lateral portion of the cranial base.4 The facial bones, on the other hand, and the majority of the cranium develop by intramembranous ossification. This development bypasses the intermediate cartilaginous phase characteristic of the development of the bony cranial base.5,6

There are 42 somites that are formed by the fourth week of gestation. There are 4 occipital somites, 8 cervical, 12 thoracic, 5 lumbar, 5 sacral, and 8 to 10 coccygeal pairs.3,7,8 Each somite differentiates into an outer dermatome and inner myotome and a medial sclervertebral body. These ventromedial bilateral cells migrate toward the midline and surround the notochord. Each sclerotome will develop the fissure of Ebner, which is a central cleft that divides a loose collection of cells cranially from a dense cellular collection caudally. In this development, the cells from the fissure of Ebner migrate toward and encase the notochord to become the precursors of the intervertebral disks.9

The superior half of one sclerotome will unite with the lower half of its neighbor, thus forming the earliest manifestation of the vertebral body. The first four sclerotomes, however, will not follow this course, but instead essentially fuse to form the occipital bone and the posterior portions of the foramen magnum. Simultaneously, vascularization of the occipital bone begins, along with differentiation of the ganglia and vascular tissue. The hypoglossal artery and the first cervical arteries demarcate the caudal occipital segment. The nervous system begins to differentiate at this time.

During the fifth and sixth weeks of gestation, further differentiation of the various parts of the brain and spinal cord takes place. The roof of the fourth ventricle, however, thins out in the midline to form the foramen of Magendie and laterally the foramen of Luschka.4,8 This occurs as an opening in approximately the seventh week when a connection between the fourth ventricle and the subarachnoid space is established.

The occipital sclerotomes correspond to the segmental nerves that group together to form the hypoglossal nerve with a path through the individual foramina within the bone. The first two occipital sclerotomes ultimately form the basiocciput. The third sclerotome is responsible for the exoccipital bone, which forms the jugular tubercles. The key sclerotome in the understanding of CVJ abnormalities is the fourth occipital sclerotome, or the proatlas ( Figs. 9.1 and 9.2 ).

The hypocentrum of the fourth occipital sclerotome forms the anterior tubercle of the clivus. The centrum itself forms the apical cap of the dens and the apical ligament. The neural arch component of the proatlas divides into a rostral ventral segment and a caudal segment. The cruciate ligament and the alar ligaments are condensations of the lateral portion of the proatlas. The ventral portion of the proatlas forms the anterior margin of the foramen magnum, as well as the occipital condyle and the midline third occipital condyle. The caudal division of the neural arch of the proatlas forms the lateral atlantal masses and the superior portion of the posterior arch of the atlas.

The first spinal sclerotome forms the atlas vertebra. It is modified from the remaining spinal vertebra in which the centrum is separated to fuse with the axis body and thus forms the odontoid process ( Fig. 9.2 ). The neural arch of this spinal sclerotome proceeds to form the posteroinferior portion of the atlas arch.4 At times, the hypochordal bow, instead of disappearing, may survive and join with the anterior arch of the atlas to form a variant with an abnormal articulation, which then exists between the inferior clivus, the anterior arch of the atlas, and the apical segment of the odontoid process.2

Recent evidence with computed tomography (CT) evaluation of the atlas has shown that several ossification centers are present in the development of the atlas.2 The lateral masses must be present at birth. A complete ring of the atlas should form by 3 years of age. Abnormal development is observed with skeletal dysplasia, such as achondroplasia, spondyloepiphyseal dysplasia, and Gold-enhar syndrome, and in genetic abnormalities, such as Down syndrome.

During embryogenesis, the hypocentrum of the second spinal sclerotome disappears. The axis body is formed by the centrum, and the division of the neural arch forms from the facets and the posterior arch of the axis vertebra.10 Thus, the dens appears from the first sclerotome, whereas the terminal portion of the odontoid process arises from the proatlas. At birth the odontoid process is separated from the body of the axis vertebra by a cartilaginous band that represents a vestigial disk and is later referred to as the neural central synchondrosis. This is crucial in the understanding of the formation of os odontoideum. The neural central synchondrosis lies below the level of the superior articular facets of the axis and does not represent the anatomical base of the dens. This synchondrosis is present in most children younger than 3 to 4 years of age and disappears by 8 years of age.11 The odontoid process is observed at birth but does not fuse to the base of the axis. The tip of the odontoid is not ossified at birth and is not observed on lateral radiographs. It is represented by a separate ossification center usually observed at 3 years of age and fuses with the remainder of the dens by 12 years of age.

The posterior fossa expansion occurs because of enchondral resorption, sutural growth, and bone accretion. The growth of the basal aspect of the clivus elongates the basiocciput and thus lowers the front of the foramen magnum. Synchondrosal growth occurs until 16 to 18 years of age. This is comparably matched by the resorptive drift downward and backward at the opisthion because of the cerebellar downward displacement, together with the rotation of the occipital and temporal lobes of the brain. The bony abnormality and hindbrain herniation syndrome are significant here. The lack of posterior fossa volume results in herniation of the cerebellar tonsils through the foramen magnum, resulting in tonsillar ectopia.1,12

Significant muscular development takes place dorsal and lateral to the cervical spine to provide for the large top-heavy cranial end of the fetus.4 The stability of the CVJ articulation, at its forward inclination, is dependent on maintaining the geometry of the articular surfaces and the ligamentous attachments, but more importantly the heavy musculature. Thus, it can be observed that ideal fusion at the CVJ should be dorsal. In addition, the dorsal musculature does not become fully supportive until 8 to 10 years of age.

The discovery of developmental control genes has led to advances in the understanding of the CVJ. There are two families of regulatory genes that have been implicated in the development of the sclerotomal parts of the somites during their resegmentation to form the specific identity of each vertebra.6,13 They promote proteins that modulate morphogenesis by influencing the transcription of specific downstream genes. Teratogen-induced disturbance of HOX gene expression and mutation in the HOX genes can cause alterations in the identity or number of the cervical vertebrae that are formed. Inactivation of the HOXD3 gene results in mutant mice with assimilation of the atlas to the occipital bone.14 The sensitivity of the occipitocervical junction to disturbances in this gene expression might prove to be the underlying cause of malformations in this region. PAX genes are expressed in diverse cell types and contribute to the development of the early nervous system. Control of resegmentation of the sclerotomes to establish vertebral boundaries seem to be independently controlled by two regulatory genes in the PAX family. This, together with asymmetrical disturbance of para-axial mesoderm cells and a possible lack of communication across the embryonic midline, could cause asymmetric fusion patterns.15 It is possible that the fusions occur before or at least during chondrification of the vertebra. These authors have suggested that the aforementioned mechanisms are likely to be responsible for observed patterns in the Klippel-Feil syndrome that affect the CVJ.

Implications of Craniovertebral Abnormalities

Table 9.1 provides a practical classification of the most frequently encountered congenital craniovertebral anomalies, which are divided into those that are present at birth (congenital) and those that have an abnormal embryology leading to symptomatic abnormalities during early childhood and into adulthood (developmental abnormalities).1 The immediate relevance of this classification is the understanding of the basis of abnormalities that occur with atlas assimilation and basilar invagination, and, more importantly, their natural history. Thus, a wide variety of abnormalities exist. These may occur by themselves or involve both the osseous and neural structures. It appears that insult to these structures may occur between the fourth and seventh week of intrauterine life, resulting in a combination of abnormalities consisting of failure of segmentation, failures of fusion of different components of each bone, hypoplasia, and ankylosis.

There is a high incidence of both anterior and posterior spina bifida of the atlas (C1), as well as os odontoideum in connective tissue diseases, such as mucopolysaccharidosis, Down syndrome, and Morquio syndrome. This results subsequently in atlantoaxial subluxation. It is possible that because of the excessive abnormal head movements in the embryo between the 50th and 53rd day, the process of chondrification becomes impaired, resulting in both anterior and posterior spina bifida at C1.4 This has been alluded to in the discussion of the development of the atlas. Spinal trauma in children younger than 8 years of age is mainly centered at the CVJ because of the high fulcrum of neck motion. This results in ligamentous injuries more than fractures. However, odontoid fractures in this age group are usually observed as avulsion injuries with separation of the neural central synchondrosis.1

The growth of the posterior fossa, especially the clivus, continues past late adolescence and provides a rationale for the need to continue observing children who have undergone occipitocervical stabilization or a craniovertebral decompression. The downward growth of the brain and the elongation of the posterior fossa and the clivus may re-create a ventral bony abnormality later in life, despite a satisfactory previous ventral decompression at the CVJ performed during the first two decades of life. We have observed this to occur, although infrequently, in our patients with ventral or dorsal posterior fossa decompression.

In considering the epidemiology affecting the CVJ, it is important to keep in mind that infants with Golden-har syndrome, skeletal dysplasias, and Conradi syndrome will have abnormalities at the CVJ. It should be suspected also in infants who present with torticollis. Diseases such as Down syndrome have a 14 to 20% incidence of atlantoaxial dislocation.16 Once the stage is set by congenital craniovertebral abnormalities, developmental and acquired phenomena may supervene, producing atlantoaxial instability and subsequently basilar invagination. This is more common in developing countries, where heavy loads are carried on the head from childhood. An erroneous diagnosis of “congenital dislocations” thus appears in the literature. Likewise, upper respiratory infections can cause stiff neck, torticollis, and ligamentous instability and may come to attention later in developing countries than in places where medical attention is readily available. For this reason, it seems that abnormalities of the CVJ are more frequently encountered in populous and less advantaged areas of the globe.

Marin-Padilla and Marin-Padilla in 1981 demonstrated that the basichondrocranium of fetuses with hindbrain malformations, such as Chiari syndrome, is shorter than normal and elevated in relation to the axis of the vertebral column.17 The shortness of the basichondrocranium of these fetuses is attributed to the underdevelopment of the occipital bone, especially noticeable in the basal component. The defect results in a small posterior fossa, inadequate to contain the developing nervous structures at that region. Unfortunately, this information, though provided in the literature, received very little attention. The elongation of the odontoid process, referred to as a “dolicho-odontoid process,” is explained by the depression at the basiocciput, resulting in a secondary form of basilar impression observed in clinical Chiari I malformations. These changes have been reproduced experimentally in pregnant hamsters by a single dose of vitamin A given early in the morning of the eighth day of gestation, thus producing the typical Chiari malformations as well as the axial skeletal dysraphism.18