Clinical and Radiographic Anatomy of the Craniovertebral Junction

The CVJ consists of the occiput, atlas, axis, and associated ligaments. The CVJ is a compromise between strength and flexibility. The bones and ligaments provide structural support for the head and protect the brainstem and upper cervical spinal cord. Concurrently, these structures allow for significant movement in flexion-extension, lateral bending, and rotational planes. The following discussion is limited to an overview of the anatomic landmarks and indices used to define abnormal relationships because the embryology and anatomy of the CVJ has been presented elsewhere in this text.

The normal relationships among the occiput, atlas, and axis have been studied and are well described. The use of CT with sagittal reconstruction and multiaxial MRI has greatly enhanced the understanding and definition of abnormal anatomic relationships at the CVJ. Various measurements have been described to delineate normal from abnormal pathologies. In other words, there are different indices for trauma, degenerative disease, cranial settling, and basilar impression (Table 92-1).

Trauma

Injury to the CVJ can manifest as ligamentous injury or fracture of the occiput, atlas, or axis. These injuries are as follows: occipital condyle fractures, atlanto-occipital dislocation (AOD), atlas fractures or C1 burst fractures, and C2 fractures of the odontoid or pars interarticularis. Radiographic criteria have been established to help assess clinical stability. Although many of these criteria are used traditionally, they are by no means standardized criteria for each type of injury.¹ Determining instability of these fractures is of primary importance in determining management.

C0-1 Fractures or Atlanto-Occipital Dislocation

In the diagnosis of AOD,vigilant clinical suspicion is most important. The deformity may reduce spontaneously because of recoil of the elastic ligamentous structures. Suspicion should be raised based on the mechanism of injury (e.g., high-velocity crash) or findings on neurologic examination (severe neurologic injury, brainstem or C1-2 level deficits), lateral cervical spine radiograph (obvious separation of the condyle-C1 joint or C1-2 prevertebral swelling), or head CT (subarachnoid hemorrhage around the brainstem or upper cervical spinal cord, or epidural/subdural blood at C1-2).^7–9

AOD is determined by measurements made from normal plain radiographs. These techniques are the Powers ratio,¹⁰ basion-axial interval (Harris),¹¹ and the Wholey dens-basion interval (Fig. 92-1). These measurements essentially infer dislocation based on measurement of structures remote from the occipital condyle–atlas joint,^10–12 which can lead to false-negative examinations and lack of interobserver reliability. It has been found that the diagnostic sensitivities for the common tests range from 25% to 50%, with false-negative rates of 50% to 75%. However, the diagnostic sensitivity of the nonstandard indicators (perimedullary blood, tectorial membrane damage, C1-2 extra-axial blood) is 63% to 75%.⁷

FIGURE 92-1 Classic determination of the atlanto-occipital dislocation. A, Power ratio is calculated by measuring distance between the basion (B) and the midpoint of the dorsal arch of C1 (C) as well as the distance between the opisthion (O) and the ventral arch of C1 (A). The normal BC/OA ratio is less than 0.9, borderline is 0.9 to 1.0, and greater than 1.0 is abnormal. Surprisingly, this measure is not sensitive to dislocations in the longitudinal or dorsal direction. B, The basion axial interval (BAI) is the distance between the basion and the rostral extension of the dorsal cortical line of the axis. In adults, the basion is between −4 mm and +12 mm. In children, it is between 0 and 12 mm. C, The basion dental interval (BDI) is the distance between the basion and the superior cortex of the dens and is less than 12 mm in normal subjects.

An increase in the measurement of the joint distance between the occipital condyle and C1 can be used to determine AOD. This is called the condylar distance. Thin-slice axial CT scanning allowed Pang et al. to calculate that the distance should be less than 4 mm in pediatric patients (Fig. 92-2). This test has been shown in the pediatric population to have a diagnostic sensitivity of 100%.⁷ Dziurzynski et al. showed that in adult patients a condylar distance greater than 2 mm was diagnostic of AOD. This has a sensitivity of 92% and specificity of 95%.¹³

FIGURE 92-2 Condyle–C1 interval. Two images are selected from the midpoint of the joint space in sagittal (A) and coronal (B) CT reconstructions. Measurements of the joint space are selected at four equidistant points. The average of the measurements in each view should be less than 4 mm in children and 2 mm in adults.

If the patient survives the initial injury, he or she should be immediately immobilized. The use of a halo vest to immobilize the patient has been shown to be a safe and effective treatment method to prevent delayed neurologic deterioration while the patient is stabilized and prepared for definitive treatment.¹⁴ Depending on the severity of injury, operative fixation can be performed on an elective basis.¹⁴ The instability of AOD is primarily a ligamentous injury, and therefore internal fixation and fusion is recommended for definitive treatment. If reduction of the AOD is necessary, it should be done with gentle manual manipulation under fluoroscopic guidance. If the patient has a neurologic examination to follow, the reduction can be performed with the patient under mild sedation. In the anesthetized patient, somatosensory evoked responses may provide some help in determining if reduction is affecting the patient neurologically.

C2 Fractures

C2 fractures can be broadly divided into odontoid, C2 body, and pedicle/pars fractures. Odontoid fractures are classified by the system of Anderson and D’Alonzo (Fig. 92-3).²⁴ Type 1 fractures are rare and are at the distal tip of the odontoid process. Type 2 fractures occur at the base of the odontoid where it meets the body of the axis. Type 3 fractures occur through the body of the axis. The management options for odontoid fractures depend on the type of fracture, the degree of subluxation of the cranial fragment, and the status of the transverse ligament. Type 1 and type 3 fractures are often managed by external immobilization alone, collar or halo. Type 2 fractures can be managed by immobilization or operative intervention depending on patient factors and the degree of subluxation. An increased rate of nonunion has been associated with patient age younger than 60 years and/or subluxation greater than 4 to 6 mm.^25–27 Nonunion rates can be as high as 28%. Type 2a fractures, characterized by comminution of the C2 body, are associated with lower healing rates without surgery.^28,29 C2 pars and pedicle fractures may require surgical intervention, depending on the degree of angulation and distraction between the fragments (see subsequent discussion).^27,29

FIGURE 92-3 Odontoid fracture types and management. Type 1 fractures are fractures of the tip of the dens and can be managed in a cervical collar. Type 2 fractures are fractures of the base of the dens, and treatment varies depending on age and distance of displacement. Patients with fractures with greater than 4 to 6 mm of displacement and those older than 55 years of age are less likely to heal with external immobilization and may benefit from surgical stabilization. Type 3 fractures are fractures that extend through the dens and the body of the axis and can be managed in a cervical collar.

Os odontoideum is defined as an ossicle of cortical bone in the position of the odontoid process often attached to the C2 body by a cartilaginous segment (Fig. 92-4). The cause of this remains unclear. There is some evidence to suggest that this is a consequence of old trauma, often at an early age.³⁰ It is unlikely that this is a failure of fusion during development, because the normal somite pattern of development of the axis does not normally have a site of fusion where the axis meets the body.³¹ However, os odontoideum is associated with congenital disorders, such as Down and Morquio syndromes, and spondyloepiphyseal dysplasia. Patients who have neurologic compromise are offered surgical decompression and fusion. Patients with gross instability or narrow canal diameter are also offered surgery. The treatment of incidentally found os odontoideum is controversial. Most authors recommend close follow-up, with surgery reserved for the development of symptoms or radiographic evidence of instability or progressive deformity.³¹

FIGURE 92-4 Os odontoideum is defined as an ossicle of cortical bone in the position of the odontoid process often attached to the C2 body by a cartilaginous segment. The T2-weighted MRI demonstrates hypointensity at the base of the odontoid. The dynamic radiographs demonstrate movement in flexion and extension.

Fractures of the C2 pars interarticularis are called hangman’s factures because of the similarity to those seen in judicial hangings.³² These fractures are also called C2 traumatic spondylolisthesis fractures. These fractures have been classified into three types by Effendi et al. (Fig. 92-5).^33,34 Type 1 fractures are displaced less than 2 mm and minimally angulated, and the C2-3 disc space remains intact. Type 2 fractures have a displaced and angulated body of the axis and a disrupted C2-3 disc space. Type 3 fractures are like type 2 fractures with locked C2 and C3 facets, and the body of the axis is ventrally displaced.

FIGURE 92-5 Effendi classification of C2 traumatic spondylolisthesis. Type 1 fractures are displaced less than 2 mm and minimally angulated. The C2-3 disc space remains intact. Type 2 fractures have a displaced and angulated body of the axis and a disrupted C2-3 disc space. Type 3 fractures are like type 2 fractures with locked C2 and C3 facets.

Decisions of treatment of C2 pars fractures are primarily guided by degree of subluxation of C2 on C3. A type 1 fracture without significant ligamentous injury can be treated with immobilization. A halo ring can be used to achieve reduction by extension and capital flexion, reversing the mechanism of fracture. When significant ligamentous injury exists, care must be taken with the use of traction to avoid iatrogenic separation of C2 and C3. In type 2 or 3 fractures, if there is displacement greater than 3 mm, operative intervention may be indicated for reduction and fixation.^25,34,35

C2 transverse process fractures do not cause instability, but potential injury to the vertebral artery is an area of concern. It is unclear whether aggressive imaging or treatment of these injuries affects patient outcomes, and decisions should be individualized depending on patient symptoms and anatomy.³⁶

Degenerative Disease

Abnormalities of bone metabolism, degeneration of synovial joints, or abnormal stresses placed on the CVJ can result in basilar impression. The principles of diagnosis and treatment remain the same, regardless of the cause.

Rheumatoid arthritis (RA) is the most common degenerative disorder of the CVJ. RA is characterized by destruction of synovial joints. The disease is estimated to affect 0.8% of the Caucasian adult population in the United States, about 2.2 million people. The cervical spine is the second most commonly involved region of the body.³⁷ The degenerative changes seen in the cervical spine are progressive in nature. Translational subluxation of C1-2 occurs first, followed by vertical subluxation of C1 on C2.^38,39 Compression of the spinal cord and brainstem occurs as the lateral mass joints are eroded by inflammatory synovitis and the odontoid ascends through the atlas and the foramen magnum (Fig. 92-6). Oda et al. found a predictable progression of transverse subluxation to reducible vertical subluxation to irreducible vertical atlantoaxial subluxation.³⁸ Fujiwara et al. redemonstrated this progression and also noted an association between the severity of RA and the progression of subluxation. Patients with less severe RA develop transverse subluxation, those with RA of moderate severity develop a combination of transverse and vertical subluxation, and those with more severe RA develop vertical subluxation.³⁹ Basilar impression is the ascension of the odontoid process into the posterior cranial fossa and is defined by an abnormal position of the dens with respect to the foramen magnum. As the dens ascends into the posterior fossa, variable symptoms, which include but are not limited to myelopathy and lower cranial nerve deficits, develop. Although motor weakness and sensory changes due to myelopathy are the most common signs, the earliest sign of spinal cord dysfunction is posterior column function.⁴⁰

FIGURE 92-6 Basilar impression. This MRI demonstrates the ascension of the odontoid with compression on the medulla and upper cervical spine.

Determination of transverse C1-2 instability is performed using the anterior dental interval (ADI) (Fig. 92-7A). An ADI greater than 3 mm is considered to be abnormal.⁴¹ Vertical subluxation is measured using the Ranawat method. The vertical distance between the center of the pedicles on the axis to a line connecting the ventral and dorsal arches of the atlas is measured (Fig. 92-7B). If this distance is less than 13 mm in men and 15 mm in women, vertical subluxation is diagnosed.³⁸

FIGURE 92-7 Assessment of horizontal and vertical translation of C1 on C2. A, Horizontal translation is measured using the atlantodental interval (ADI). This is a measurement of the line extending from the dorsal arch of C1 to the ventral cortex of C2. It should be less than 3 mm in adults and 4.5 mm in children. B, Vertical translation or subluxation is measured by drawing a line connecting the midpoints of the arch of C1 and then measuring the distance of the perpendicular line between this line and the pedicle. Vertical subluxation exists if this distance is less than 15 mm in males and 13 mm in females. This measurement was described by Ranawat.

Many indices are used to screen for basilar impression from plain radiographs. These indices use bony anatomic landmarks and are the Clark station, McRae line,⁴² Chamberlain line,⁴³ McGregor line,⁴⁴ Redlund-Johnell criterion,⁴⁵ Ranawat criterion,⁴⁶ Fischgold-Metzger line,⁴⁷ and Wackenheim line.⁴⁸ Riew et al. evaluated the sensitivity and specificity of these standard screening measurements.⁴⁹ The most sensitive measurement (the test with the fewest false-negative results) is the Wackenheim line, at 88%, and the Clark station, at 83%. The Redlund-Johnell criterion is the most specific measurement (fewest false-positive results) at 76%. The Redlund-Johnell measurement has the highest positive predictive value (PPV) of 68%. The Wackenheim line has a positive predictive value of 48%. The Fischgold-Metzger line has a negative predictive value of 100%. The McRae line has the lowest negative predictive value of 75%. The study also found that identification of bony landmarks is difficult and precludes accurate application of these measurement techniques in many cases. Riew et al. recommend a combination of tests to screen for basilar invagination: the Clark station, the Redlund-Johnell criterion, and the Ranawat criterion (Fig. 92-8).

FIGURE 92-8 Measurements of basilar impression. A, The Clark station is determined by dividing the C2 body into three equal parts. If the ventral arch of C1 travels into the region of station II or station II itself, basilar invagination is suspected. B, The Redlund-Johnell criterion is measured by drawing a line from the tip of the hard palate to the rim of the occiput. A second line is drawn from the midpoint of the caudal margin of the body of C2. Basilar invagination is diagnosed if the measurement is less than 34 mm in men and 29 mm in women. The Ranawat classification is described in Figure 92-7B. The combination of these measurements should be used to screen for basilar invagination, and if suspected, an MRI should be performed to evaluate for evidence of neurologic compression.

The goals of treatments of basilar impression are to decompress the brainstem and spinal cord and reestablish support for the head. Decompression of the neural elements can be achieved either directly or indirectly. Indirect decompression is performed via closed reduction through the use of traction and manual manipulation. Long-standing lesions are unlikely to be reducible. However, a trial of craniocervical traction is warranted. Use of a halo ring provides multiple points of skull fixation and allows for fixation to the thoracic vest once the deformity is reduced. Traction is started with a weight of approximately 5 pounds (2.3 kg) and is increased as necessary. Attempted reduction is generally limited for 5 to 7 days because the likelihood of further benefit is limited after this period, and complications related to immobilization increase.³⁷ Special beds have been designed to help prevent complications of immobilization.

The ventral rheumatoid pannus often resolves once the C1-2 junction is fused, which can indirectly decompress the brainstem and spinal cord.^50,51 However, occasionally a ventral transoral approach needs to be used to obtain adequate decompression.^52–56 Intraoperative image guidance may be used to help with the decompression in a region where anatomic landmarks have been distorted.^57–59

Congenital Disorders

CVJ abnormalities are common in a number of congenital disorders. These disorders can be broadly grouped as connective tissue disorders (Down syndrome); Klippel-Feil syndrome; osteochondrodysplasias (e.g., achondroplasia); mucopolysaccharidoses (e.g., Morquio and Lesch-Nyhan syndromes); and skeletal dysplasias (i.e., osteogenesis imperfecta); as well as other disorders of development: Goldenhar syndrome, Conradi syndrome, and Klippel-Feil triad.^60–64 The incidence of atlantoaxial subluxation is about 20% in Down syndrome⁶⁵ and 50% in Morquio syndrome.⁶⁶ The anatomic abnormalities produced by these disorders and the natural history of these can help guide treatment decisions. The following will review the more common disorders of Down syndrome, Morquio syndrome, and achondroplasia to help delineate some concepts. Description and management of other mentioned syndromes can be found in the listed references.^37,67–70

CVJ abnormalities in these patients have variable causes. C1-2 subluxation is likely related to ligamentous laxity that is a common consequence of connective tissue disorders, such as Morquio syndrome and Lesch-Nyhan syndrome, and it is also a component of Down syndrome. Aberrant ossification of the dens occurs; this could be due to ligamentous laxity and disturbances in blood supply during development because of inordinate mobility.^71,72 Patients with skeletal dysplasias, such as osteogenesis imperfecta, have abnormal collagen deposition, resulting in brittle bones that easily develop multiple microfractures. Accumulation of these microfractures leads to ascension of the dens and medial skull base, causing basilar invagination.⁷²

Treatment of these lesions is guided by symptoms and the syndrome involved. For example, many children with Down syndrome have asymptomatic increased ADIs and atlanto-occipital hypermobility.^73,74 The usual measurements of CVJ instability may not apply to patients with Down syndrome. Large cohort studies have not demonstrated increased rates of neurologic injury in children with Down syndrome and abnormal ADIs as compared with their peers without abnormal ADIs. These studies also do not demonstrate a protective effect of restricted activity.^74,75 Reduction and stabilization of the CVJ is probably not indicated unless the patient has clear signs of brainstem or upper cervical spinal cord compression.^73,76

Morquio syndrome and other skeletal dysplasias are often found to have an os odontoideum and ligamentous laxity.⁷⁷ The cartilaginous os odontoideum deforms with flexion and extension. Radiographically, C1-2 instability manifests as changes in the ADI and is a late finding in affected children. By the time this is seen, myelopathy is nearly always present. These patients benefit from prophylactic fusion prior to the onset of myelopathy. The ideal age for this operation has not been determined. Ransford et al.⁷⁷ suggest that the surgery be performed at 4 years of age unless myelopathic signs develop earlier. Dorsal occipitocervical fusion can result in complete ossification of the dens, which supports the role of ligamentous laxity in the formation of os odontoideum.⁷²

The treatment of patients with congenital disorders of the CVJ varies depending on the syndrome, symptomatology, and relevant anatomy. The natural history of the disorder takes precedence in treatment and also the particular anatomy of the lesion. Traction should be used if there is a suspicion that the lesion is reducible. Use of a halo ring allows for application of corrective forces and subsequent fixation when reduction is completed. If a lesion proves to be irreducible, either after a trial of reduction or radiography, surgery is indicated to decompress the brainstem and spinal cord and to stabilize the CVJ.

Infection: Atlantoaxial Rotatory Subluxation and Fixation

Infection may lead to a rare syndrome termed atlantoaxial subluxation or atlantoaxial rotary fixation. It was originally described by Bell⁷⁸ in 1830 but was named after Grisel,⁷⁹ a French otolaryngologist who described this syndrome after upper respiratory infection. It is more common in children who present with torticollis and the head in a “cock-robin” position. There is no clear mechanism of pathogenesis for this entity, although it is associated with infection, trauma, head and neck surgery, RA, Down syndrome, Morquio disease, and other congenital cervical anomalies.⁸⁰ Battiata et al.⁸¹ hypothesize a baseline ligamentous laxity along with an inflammatory response to an infectious process. Pang et al. hypothesize that rather than ligamentous laxity, there is increased friction of the C1-2 joints.⁸⁰

The diagnosis is made by the clinical presentation along with findings of rotation of C1 on C2 seen on axial CT imaging. It is important to differentiate the presentation from muscular torticollis that has other etiologies. Pang et al. have used a dynamic CT scanning protocol to diagnose and grade the degree of pathologic “stickiness” of C1 on C2.^80,82 Type I shows movement of less than 20% with movement of the head away from the affected side. Type II is less sticky, and C1 moves on C2 greater than 20%. Type III allows movement of C1 on C2 past midline but still remains abnormal compared with normal controls. MRI can be performed to evaluate for infectious etiology.

Primary treatment of atlantoaxial rotary fixation involves traction and muscle relaxants. Traction can be performed using a head halter. Once a reasonable amount of clinical reduction has been achieved, the patient can be placed in a cervical collar and treated with muscle relaxants for 2 weeks. Any infection needs to be treated completely to help prevent recurrence.⁵⁴ Patients whose condition does not reduce or continues to recur may need more aggressive treatment. Closed reduction under general anesthesia can be used in selected cases. Operative C1-2 fixation and fusion can be used to permanently prevent recurrence. Surgical intervention is controversial. None of the patients in Menezes’ series of 52 patients required fusion.⁵⁴

The outcomes of treatment have recently been shown by Pang et al.⁸³ to be associated with the degree of rotary fixation seen with dynamic CT imaging. Patients with type I disease were more likely to have difficult reductions and recurrences than those with type III disease. Patients with type I disease were also more likely to require surgical correction. Delay in treatment also was associated with difficulty in reduction.

Tumors

Tumors of the CVJ produce signs and symptoms of neural element compression and mechanical instability (pain and progressive deformity). The treatment of these tumors depends on prognosis, symptoms, and anatomic configuration. The most common presentations of adults are myelopathy, radiculopathy, and occipitocervical pain.⁸⁴ The presentations of children in descending frequency are occipitocervical pain, paresthesias or dysesthesias of the hands, cranial nerve palsies (most commonly diplopia), and myelopathy.⁸⁵ The most commonly encountered tumors in this region are chordomas and meningiomas, but other primary tumors—osteoblastoma, eosinophilic granuloma, plasmacytoma, chondrosarcoma, and Ewing sarcoma—also occur. Metastatic tumors, including breast tumors and paragangliomas, have also been encountered.^84–86

Treatment of patients with CVJ tumors involves decompression of neural structures and then determining if surgery has destabilized the CVJ to the point that fusion is necessary. The first step is to determine the direction of the surgical approach. Piper and Menezes divide the axis into four zones that help guide the surgical approach for tumor resection (Fig. 92-9).⁸⁴ Zone 1 tumors are in the ventral midline involving the axis, atlas, and lower clivus and are best accessed by the transoral approach, with or without division of the palate or the mandible. Zone 2 tumors are more ventrolateral and often involve the lateral mass of C1 and C2. They are best accessed using a retropharyngeal approach. Zone 3 tumors are located dorsal to the lateral mass and may extend into the occipital condyle or dorsal fossa. These tumors are best accessed using a far lateral approach. However, this approach may not be good for later instrumention of the spine. Zone 4 tumors are in the dorsal midline and are resected through a standard midline approach.⁸⁴

FIGURE 92-9 Surgical approaches and anatomic zones for tumor resection at the craniocervical junction as described by Menezes and Piper. Zone 1 tumors are in the ventral midline involving the axis, atlas, and lower clivus and are best accessed by the transoral approach, with or without division of the palate or the mandible. Zone 2 tumors are more ventrolateral and often involve the lateral mass of C1 and C2. They are best accessed using a retropharyngeal approach. Zone 3 tumors are located dorsal to the lateral mass and may extend into the occipital condyle or dorsal fossa. These tumors are best accessed using a far lateral approach. However, this approach may not be good for later instrumention of the spine. Zone 4 tumors are in the dorsal midline and are resected through a standard midline approach.

Determining the need for stabilization of the spine and timing of that stabilization is not entirely straightforward. It can be helpful to think about the area of resection to give some criteria for stabilization.

Deformity Reduction

Reduction of deformity can be performed by either closed or open methods depending on the anatomic configuration. Successful closed reduction with axial traction can sometimes obviate the need for open ventral decompression, or in some cases of trauma, such as traumatic spondylolisthesis, closed reduction can potentially obviate the need for surgical intervention. Closed reduction is achieved with the use of axial traction with a halo fixator. In some cases, manual manipulation under fluoroscopic guidance is used for reduction. The halo is applied carefully, and the force of pin application is tailored to patient age and underlying pathology. Children younger than 2 years of age or with underlying pathology affecting the skull may not be candidates for a halo ring, and the use of a custom-built Minerva device may be preferable. Children 2 to 4 years of age should have an eight-point halo fixation with an MRI-compatible device. The pins should be tightened to between 1 to 1⅓ pounds of torque.⁹⁰ The maximum pin torque is 4 pounds for children who are 5 years of age. Traction should be initiated with low weight (4 pounds) in 5-year-old children, and it should not exceed 7 pounds.⁵⁴ Halo application and traction are performed under general anesthesia or moderate sedation in some cases. Fluoroscopy, plain radiographs, or even CT or MRI may be used to determine if reduction has been achieved.⁹¹

Patients who have long-standing degenerative disorders or tumors are generally not candidates for preoperative reduction. These patients require direct surgical decompression via the appropriate surgical route. This can be aided with the use of computerized stereotactic navigation.^58,92 After the decompression, reduction of the deformity can be achieved by direct manipulation and appropriate shaping of implants and postoperative immobilization.

Summary

Surgical pathology of the CVJ is quite complex. Treatment of traumatic causes of deformity in primarily guided by clinical suspicion and identification of instability followed by stabilization. Management of degenerative disease is guided by the natural history and symptomatology. Congenital abnormalities also are guided by the natural history of the disease and symptoms. Tumor management is guided by tumor location and management of subsequent instability related to tumor debulking. Although technically challenging, appropriate preoperative consideration of the biologic, biomechanical, and pathophysiologic factors associated with CVJ surgery increases the likelihood of a favorable clinical outcome.