Developmental Abnormalities of the Craniocervical Junction

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CHAPTER 218 Developmental Abnormalities of the Craniocervical Junction

The first anatomic description of “manifestations of occipital vertebrae” was attributed to Meckel in 1815 by Gladstone and Erickson-Powell.¹ Its clinical significance became appreciated after the classic radiologic studies on basilar invagination by Chamberlain in 1939.²

The term craniovertebral junction refers to the occipital bone that surrounds the foramen magnum and the atlas and axis vertebrae. Into the 1970s, surgical treatment of conditions affecting the craniovertebral junction consisted of posterior decompression by enlargement of the foramen magnum and removal of the posterior arch of the atlas and axis vertebrae. However, mortality and morbidity rates associated with this treatment were high in patients with irreducible lesions and cervicomedullary compression.³ A physiologic approach based on an understanding of craniovertebral dynamics, the site of encroachment, and stability of the craniovertebral junction was adopted at the University of Iowa Hospitals and Clinics in 1977. Since then, 6000 patients with neurological symptoms and signs secondary to an abnormality in the craniocervical region have been studied. Understanding of the pathology of these abnormalities and their treatment is simplified if one has knowledge of the bony anatomy, biomechanics, and embryology of the region.

Anatomy of the Craniovertebral Junction

Bone-Ligament Complex

The atlantoaxial complex is unique among the intervertebral joints in that it is horizontally oriented. The lateral facet joints are relatively flat and allow a pivoting motion at the atlantodental articulation, which is permitted by the special ligamentous support. The second cervical nerve exits from the cervical canal immediately adjacent and dorsal to the joint capsules. The transverse atlantal ligament is a band 3 to 5 mm thick that originates from the tubercles and the inner aspect of the lateral masses of the atlas vertebra and is in close apposition to the odontoid; this ligament allows axial rotation.

By itself, the geometry of the craniovertebral complex is meant to provide mobility at the cost of stability.⁴ However, the complex is maintained in a clamp-like vise by the craniovertebral musculature, which assists in stabilization of the spine, initiates movements within the joints, and maintains fluidity of the motion complex.

Blood Supply

The blood supply to the odontoid process is via anterior and posterior ascending vessels from the vertebral arteries, with a contribution from the carotid arteries, which form an apical arcade around the alar ligament.⁵ Thus, the blood supply of the odontoid process is vulnerable with a type II odontoid fracture.⁶

Parke and coworkers demonstrated pharyngovertebral veins with frequent lymphovenous anastomoses.⁷ This connection may provide an additional route for septic involvement of the craniovertebral complex, which can result in osteomyelitis of the bone, as well as joint effusions.

Lymphatic Drainage

Lymphatic drainage of the occipitoatlantoaxial joint complex is primarily into the retropharyngeal lymph nodes and then into the upper deep jugular cervical chain.³ These nodes also receive drainage from the nasopharynx, paranasal sinuses, and retropharyngeal area. A retrograde infection may affect the synovial lining of the craniovertebral joint complex and cause an inflammatory effusion, instability, and possible neurological deficit, thereby contributing to the so-called Grisel syndrome.⁸

Embryology and Development of Craniovertebral Junction Disorders

Congenital anomalies of the base of the skull and the atlanto-occipital region involve both the osseous structures and the nervous system. The frequent occurrence of patterns with various combinations suggests an interrelationship between if not a common cause of the origin and development of these structures.³

The bony cranial base is formed by the process of endochondral ossification in which a cartilaginous framework is first developed and subsequently resorbed, with further deposition of bone based on distorting forces such as brain and eye development.⁹^,¹⁰ The clivus is elongated by sutural growth of the spheno-occipital synchondrosis and by further sutural growth along the lateral portion of the base.

The majority of the skull and facial bones develop by intramembranous ossification. Such development bypasses the intermediate cartilaginous stage characteristic of development of the bony cranial base.¹⁰^,¹¹

The occipital sclerotomes correspond to the segmental nerves that group together to form the hypoglossal nerve, which passes through the bone via the individual foramina.⁶^,¹⁰ The first two occipital sclerotomes ultimately form the basiocciput. The third sclerotome is responsible for the exoccipital center as it forms the jugular tubercles.¹¹^,¹² The key to understanding the craniovertebral junction is the embryology of the fourth occipital sclerotome, which in lower animals is called the proatlas. The hypocentrum of the fourth occipital sclerotome forms the anterior tubercle of the clivus. The centrum of the proatlas itself forms the apical cap of the dens, as well as the apical ligament. The neural arch component of the proatlas divides into a ventral-rostral component and a caudal-dorsal portion. The ventral portion forms the U-shaped anterior margin of the foramen magnum, as well as the occipital condyles and the midline occipital condyle. The cruciate ligament and the alar ligaments are condensations of the lateral portion of the proatlas. The caudal division of the neural arch of the proatlas forms the lateral atlantal masses of C1, as well as the superior portion of the posterior arch of the atlas.

The atlas vertebra is formed by the first spinal sclerotome. It is modified from the remaining spinal vertebrae, and the centrum separates to fuse with the body of the axis and form the odontoid process. The neural arch of the first spinal sclerotome forms the posterior and inferior portions of the atlas arch. The hypochordal bow of the proatlas itself may survive and join with the anterior arch of the atlas to form a variant in which an abnormal articulation may exist between the clivus, the anterior arch of the atlas, and the apical segment of the odontoid process.

During embryogenesis, the hypocentrum of the second spinal sclerotome disappears. The centrum forms the body of the axis vertebra, and the neural arches develop into facets and the posterior arch of the axis. Thus, the body of the dens arises from the first sclerotome, whereas a terminal portion of the odontoid process arises from the proatlas. The most inferior portion of the body of the axis is formed by the second spinal sclerotome. 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 referred to as the neural central synchondrosis.⁶^,¹³ It lies below the level of the superior articular facets of the axis and does not represent the anatomic base of the dens. This synchondrosis is present in most children younger than 3 to 4 years and disappears by 8 years of age. In most instances, the odontoid process is seen at birth but does not fuse to the base of the axis.¹⁴ The tip of the odontoid is not ossified at birth and thus is not seen on lateral radiographs. It is represented by a separate ossification center, which is usually seen at 3 years of age and fuses with the remainder of the dens by the age of 12 years.

Expansion of the posterior fossa occurs as a result of a combination of endochondral resorption, sutural growth, and bony accretion.¹⁵ Growth of the basion elongates the basiocciput and lowers the frontal margins of the foramen magnum. There is a comparably matched resorptive drift downward and backward at the opisthion as a result of downward displacement of the cerebellum, together with rotation of the occipital and temporal lobes of the brain.¹⁶

Because of the forward inclination of the top-heavy cranial end of the fetus, the stability of the craniovertebral articulation must be maintained by the geometry of the articular surfaces of the craniovertebral junction, as well as by the ligamentous attachments and, more importantly, by the heavy development of the dorsal and lateral cervical musculature, which provides a clamping action on the craniovertebral region.³^,⁴

Significant advances in recent years have occurred with the discovery of developmental control genes.9–11,15–18 Two families of regulatory genes have been implicated in the subsequent development of the sclerotomal portions of the somites during their resegmentation to form the vertebral primordia and in specification of the identity of each vertebra. Common to all these genes are phylogenetically highly conserved DNA sequences termed homeovox (Hox genes) and paired vox (Pax genes) sequences. They promote the production of proteins that modulate morphogenesis by influencing the transcription of specific downstream genes.

Teratogen-induced disturbances in Hox gene expression and mutations in Hox genes can cause alterations in both the number and identity of the cervical vertebrae forming at or near the limit of their expression domain. For example, inactivation of the Hox-D3 gene results in mutant mice with assimilation of the atlas to the basiocciput.¹⁹ The sensitivity of the occipitocervical junction to disturbances in Hox 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 development of the early nervous system. Control of resegmentation of the sclerotomes to establish the intervertebral boundaries seems to be independently regulated by two genes in the Pax family.¹⁷^,²⁰

Implications of Craniovertebral Abnormalities

A wide variety of congenital anomalies of the craniovertebral junction exist and can occur singularly or multiply in the same individual and involve both osseous and neural structures. An insult to both types of structures may occur between the fourth and seventh weeks of intrauterine life and result in a combination of anomalies consisting of failure of segmentation, failure of fusion of different components of each bone, hypoplasia, and ankylosis.

Congenital diseases involving connective tissue, such as Morquio’s syndrome and other mucopolysaccharidoses, as well as Down syndrome, can lead to severe atlantoaxial subluxation.^3,^14,²¹ There is a high incidence of anterior and posterior spina bifida of C1 and also os odontoideum in these instances. It is possible that because of abnormal, excessive head movements in the embryo between days 50 and 53, the process of chondrification is impaired, thereby resulting in anterior and later posterior spina bifida of C1.¹⁶

Os odontoideum was previously thought to be congenital and was described as a failure of fusion between the centrum component of C1 and that of C2. However, this radiographic abnormality always has a hypoplastic dens, and the neural central synchondrosis is a definite visible entity.¹³ To be congenital, the defect would have to be below the superior slopes of the C2 facets.⁶ Os odontoideum most likely originates as odontoid trauma that may predate birth but certainly occurs before the age of 4 years, with subsequent distraction and separation of the odontoid fragments.³^,²² The superior segment is distracted upward by the apical and alar ligaments and receives its blood supply from the descending branch of the occipital artery, which courses along the apical ligament. This subsequently leads to incompetence of the cruciate ligament and further abnormalities.

Spine trauma in children younger than 8 years is mainly centered at the craniovertebral border because of the high fulcrum of neck motion.³ It results in ligamentous injuries more often than fractures. However, odontoid fractures in this age group are usually seen as avulsion injuries with separation of the neural central synchondrosis.

Anomalies and malformations of the caudal occipital sclerotomes are collectively called “manifestations of occipital vertebrae” and result in abnormal bony ridges and outgrowths of the ventral aspect of the foramen magnum.¹ At times, segmentation abnormalities of the clivus are recognized and represent failure of the last occipital sclerotome to separate from the basiocciput and clivus. Consequently, bone growth in the anterior aspect of the foramen magnum indents the ventral cervicomedullary junction with age (as the clivus expands inferiorly and dorsally).

Ongoing growth of the posterior fossa from birth into late adolescence provides a rationale for the need to monitor children who have undergone dorsal occipitocervical stabilization or ventral craniovertebral decompression. The downward growth of the brain, as well as elongation of the posterior fossa and clivus, may re-create a ventral bony abnormality later in life despite previous performance of ventral decompression at the craniovertebral junction during the first 2 decades of life.

Biomechanics

The unique anatomic configuration of the craniovertebral junction creates a distinct biomechanical behavior that differs from that of the other spinal joints. The motion characteristics of the different levels of the craniovertebral junction are due to the geometry of the opposing bones of the vertebrae and the skull base, the shape of the joints, and the arrangements of the ligaments.^4,²³^–²⁵ An intervertebral disk is absent between the occiput, C1, and C2. The ball-and-socket–shaped occiput-C1 joint allows slightly more flexion-extension than the other levels of the cervical spine do, although it is quite rigid in axial rotation and lateral bending.

The biconvex articular surfaces of the C1 and C2 joints allow gliding and wide rotation of C1 around the dens. The atlantoaxial motion segment is the most flexible motion segment in the entire spine with respect to axial rotation in that it allows a bilateral range of motion of 90 degrees. More than half of all cervical axial rotation occurs at the C1-2 motion segment, a point that should be kept in mind when considering atlantoaxial arthrodesis. In a child, the amount of anterior-posterior translation that occurs between the dens and the anterior ring of the atlas is up to 5 mm. When the transverse component of the cruciate ligament has been disrupted, the alar ligaments are still intact.²⁵ Hence, the amount of displacement remains between 5 and 6 mm until the alar ligaments become incompetent. It is only when the alar ligaments and the transverse portion of the cruciate ligament are incompetent that a separation of more than 5 to 6 mm occurs. Beyond the age of 8 years, excursion of the predental space must be limited to 3 mm.²⁶

Failure of one alar ligament results in moderate rotary atlantoaxial instability.²⁷ Bilateral transection of the alar ligaments causes considerably more alterations in craniovertebral motion, and the coupling action is disturbed. The transverse atlantal ligament is the strongest and thickest ligament in the entire spine. It is the predominant stabilizer of the atlas and constrains C1 around the dens. When torn, the transverse ligament is incapable of repair. Because injury to this ligament renders C1 grossly unstable, C1-2 fusion is mandated. The largest extent of rotation occurs at the atlantoaxial joint. When rotation exceeds 40 to 50 degrees, an interlock of the lateral inferior facet of the atlas over the superior articular facet of the axis vertebra occurs. If the transverse ligament becomes deficient, the anterior arch will sublux forward and result in unilateral dislocation and an interlock at less than 40 degrees.¹³^,²⁶ Rotation of more than 30 to 35 degrees produces an angulation of the contralateral vertebral artery.²⁵^,²⁸ With greater rotation, the vertebral artery is stretched, and the ipsilateral vessel may demonstrate occlusion.²⁸^,²⁹ This phenomenon has an implication in wrestling and football injuries and in certain head rotation maneuvers performed under general anesthesia or forced chiropractic manipulations.³⁰^,³¹ There is a muscle-clamping action that takes place in vivo and produces compressive force across the cervical spine. This muscular action results in the “interlocking stiffening” that maintains alignment during rotation. When the protective muscles are relaxed or inadequately developed, as in the case of a young child under general anesthesia, the craniovertebral junction becomes inherently less stable than that in an adult.³ As muscular development occurs, there is less tendency for instability at the craniovertebral junction.

Biomechanical Comparison of Cervical Orthoses

An orthosis acts as a restraint to restrict spinal motion or immobilize the surrounding tissues. Orthoses are used as load-sharing devices to reduce the external loads applied to the spine while an injury or a fixation fusion is healing.

A halo brace is most effective at constraining cervical motion at all levels, and control of spinal motion is related to the distance of the spinal segment from the region of the rigid skull fixation.³^,²⁷ A halo brace provides the best control of motion at the craniovertebral junction, intermediate control of midcervical motion, and the least control of motion at the cervicothoracic junction. This pattern reflects snaking movements of the spine.

The soft cervical collar provides little immobilization and tends only to remind the patient to restrict motion. Molded collars, four-poster braces, sternal-occipital-mandibular immobilization, and cervicothoracic braces have intermediate effects in controlling flexion and extension, lateral bending, and axial rotation.

Classification of Craniovertebral Junction Abnormalities

A wide variety of congenital, developmental, and acquired abnormalities can occur at the craniovertebral junction, and there may be single or multiple abnormalities in the same individual. The pathology of these abnormalities is extensive.³ A working classification has been provided, but it must be appreciated that there are overlapping causes within this classification (Table 218-1).

TABLE 218-1 Classification of Craniocervical Junction Abnormalities

Epidemiology

Abnormalities of the craniovertebral junction must be suspected in infants with Goldenhar’s syndrome, skeletal dysplasias, and Conradi’s syndrome.³ It should also be suspected in infants with “torticollis.” Diseases such as Down syndrome are associated with a 14% to 20% incidence of atlantoaxial dislocation. In Morquio’s syndrome, a combination of atlantoaxial instability, os odontoideum, and cervicothoracic abnormalities occurs in 30% to 50% of individuals.^3,^14,³² The incidence of atlas assimilation is 0.25% in the general population. Many such patients have associated segmentation failure of the upper cervical spine.³³

We have reviewed syndromes cited as altering the craniovertebral junction in more than 6000 patients seen at our institution. A search of the scientific literature identified genetic syndromes that affect the craniovertebral junction. In addition, the Online Mendelian Inheritance in Man (OMIM) database was used to identify disorders of the craniovertebral junction encountered in various clinical populations. The information recorded includes systemic manifestations of the syndromes, the effect on the craniovertebral junction and cervical vertebrae, inheritance pattern, and genes or genetic loci associated with the disorder. A total of 84 syndromes have been identified that affect the craniovertebral junction.³⁴

Once the stage is set by congenital craniovertebral anomalies, the developmental and acquired phenomena may supervene and produce atlantoaxial instability and subsequently basilar invagination. This is much more common in developing countries where heavy loads are carried on the head from childhood. Thus, the erroneous diagnosis of “congenital dislocations” has been reported. Likewise, upper respiratory tract infections that lead to a stiff neck, torticollis, and ligamentous instability come to attention much later in developing countries than in places where medical attention is more readily available. For this reason, it appears that abnormalities of the craniovertebral junction are more frequently encountered in populous, less advantaged countries.