Clinical manifestations

Presentation and course

Antecedent conditions such as trauma, neck or upper airway infection (Grisel syndrome), coughing or weight loss (tuberculosis), congenital syndromes (Stickler, Loeys-Dietz, Morquio, Down, Ehlers-Danlos), or autoimmune and inflammatory diseases (rheumatoid arthritis, systemic lupus erythematosus) should be noted.

Clinical manifestations vary based on the type of atlantoaxial dislocation. The classic findings in rotatory subluxation are neck and suboccipital pain, reduced neck range of motion, and the “cock robin” head position of torticollis. In the cock robin position, the head is tilted to 1 side, rotated to the opposite side, and flexed forward (37).

Neurologic signs are rare in rotatory subluxation because the upper cervical spinal canal is capacious and rotation of C1 on C2 does not narrow canal diameter significantly. Many patients with torticollis do not have pathologic C1-C2 rotation or fixation, so the diagnosis of atlantoaxial dislocation cannot be made simply by documenting torticollis (27). Radiologic studies are required. Note that less severe subluxations are more likely to present in a delayed fashion than more severe subluxations (45). Follow-up data are not abundant, but in a study of 77 adolescent patients at an average 14 months, neurologic function was preserved and general outcomes satisfactory from patient and parental points of view (76).

Anterior atlantoaxial dislocation due to fracture of the base of the odontoid process or disruption of the transverse ligament also presents with neck pain and reduced range of motion but is more likely to have associated neurologic deficit from spinal cord compression. Bilateral disruption of the C1-C2 articulations allows forward translation of C1 on C2. This can result in spinal cord impingement by the posterior ring of C1. Neurologic deficit may range from mild sensory changes to complete paralysis. These patients may die suddenly as C1 spinal cord injury causes respiratory paralysis. Chronic dislocation and spinal cord compression can present with mechanical neck pain and myelopathic signs (eg, hyperreflexia, proprioceptive loss).

Prognosis and complications

Prognosis depends on predisposing conditions and neurologic status at presentation. An otherwise healthy child with spontaneous rotatory subluxation should have a full recovery. Spinal malalignment and neural compression can be satisfactorily corrected with surgery. Mild to moderate myelopathy may resolve partially or completely with expeditious treatment. Severely myelopathic patients may make some recovery after decompression and stabilization but will rarely make complete recovery. Survival rates of spinal cord injury at the C1-C2 level are similar to those of spinal cord injury in the subaxial cervical spine, at least in elderly patients (69).

Patients tend to have simpler treatment and more complete recovery when managed early. Longer duration of treatment, higher rate of recurrent subluxation, failure to achieve good spinal alignment, and higher rates of halo or surgical fusion are all characteristics of chronic subluxation. This can result in higher-grade subluxations having better outcomes as they tend to present and be diagnosed more rapidly (45).

Underlying conditions and the effectiveness of their medical management have a great impact on functional recovery. Pyogenic and mycobacterial infections can usually be systemically controlled by antimicrobial drugs. Patients should be under the continued care of appropriate medical physicians.

Some predisposing conditions are associated with increased morbidity and mortality after surgical management. Rheumatoid arthritis is a classic example as these patients typically have impaired tissue quality and wound healing due to the disease process and the chronic use of steroids and other immune-modulating drugs. They have a higher rate of surgical infections and their impaired mobility increases the incidence of the common post-operative complications (deep venous thrombosis and pneumonias) and makes physiotherapy and rehabilitation more difficult (50). The presence of antibodies against citrullinated proteins (ACPA) is a significant risk factor for cervical spine instability in these patients (03).

Severe deformation at the atlantoaxial articulation distorts the vertebral arteries. Both C1 and C2 have fixed bony canals or foramina that establish the position of the vertebral arteries. Sufficient distortion can lead to vascular injury, stenosis, or occlusion. If unilateral, this may be asymptomatic, but it can also lead to ischemia, especially in the brainstem or posterior fossa (60). A vertebral artery dissecting aneurysm with resultant cerebral infarction has been diagnosed in a teenager with atlantoaxial instability and aplasia of the C1 lamina (04). Vertebral arteries are also at risk of damage during surgery (35; 61). One young patient has presented with occlusion of the posterior cerebral artery secondary to atlantoaxial dislocation (40).

Clinical vignette

A previously healthy 3-year, 10-month old girl was performing somersaults when she developed new pain and inability to straighten her neck. Her parents took her to her pediatrician who recommended ibuprofen, acetaminophen, and diazepam. She was also referred for physiotherapy. This decreased her pain but did not normalize her head position. She was subsequently referred for x-rays of her neck. She was diagnosed with rotatory subluxation of C1 on C2 and referred to a neurosurgeon. She was placed in cervical traction. After 10 days of traction, her subluxation reduced. She was placed in a hard cervical collar for 2 months and then released to normal activity.

Biological basis

Etiology and pathogenesis

Atlantoaxial dislocation occurs as the result of the application of force to the C1-C2 complex such that the biomechanical limits of the bones and ligaments are exceeded. The odontoid process of C2, transverse ligaments of the cruciate ligament spanning the anterior aspect of the ring of C1 and restraining the odontoid process and the alar ligaments are the key structures defining the movement of the atlantoaxial complex. The C1-C2 joint provides a significant percent of the rotational movement of the cervical spine (44). C1 can rotate on C2 an average of 43 degrees each way. The subaxial cervical spine provides the rest of rotational movement, but less all combined than C1-C2 alone.

Atlantoaxial dislocation may be congenital. When oblique or asymmetric, C1 and C2 joints are prone to slippage, with spondyloptosis, vertical dislocation, or lateral tilt common (54; 55). Therefore, the 3-dimensional anatomy of these joints must be assessed both pre- and post-operatively (57). Insufficiency of the transverse ligament or the odontoid process (such as os odontoideum) is more often associated with reducible atlantoaxial dislocation, whereas spinal segmentation defects leading to abnormal occiput to C1, C1-C2, or C2-C3 articulations will more likely result in nonreducible atlantoaxial dislocation (53). Certain syndromes may predispose individuals to atlantoaxial dislocation, including those with anomalies of skeletal configuration, osseous tissues, or collagen. Primary conditions are Goldenhar syndrome, spondyloepiphyseal dysplasia, Morquio syndrome, occipitalization of the atlas, and chromosomal anomalies, especially trisomy 21 (82; 62).

More rarely, high-energy trauma can result in vertical atlantoaxial dislocation by a distracting mechanism that also can lead to atlantooccipital dislocation. This has a high likelihood of injury to the spinal cord or vertebral arteries and has a poor prognosis (47). This presents on CT or MR as increased space between the C1 and C2 lateral masses (21).

Anterior traumatic atlantoaxial dislocation results from hyperflexion injuries and is associated with rupture of the transverse ligament (39). This injury is more intrinsically unstable than rotatory subluxation.

Inflammation from upper respiratory tract infections or otolaryngologic procedures combined with sudden movement from sneezing or abnormal protective postures of the neck can lead to atlantoaxial rotatory subluxation. This is a classic cause of nontraumatic torticollis in the pediatric population and is known as Grisel syndrome, an uncommon and incompletely understood condition that occurs after surgery (usually involving ear, nose, or throat) or upper respiratory infection (13; 43). Subluxation has been reported in a 17-year-old girl several months after a bout of tonsillitis (66).

These structures can fail in the normal person during high-energy traumatic events such as motor-vehicle accidents or athletics. Atlantoaxial dislocation may also occur under more normal physiologic stresses when the strength and stability of the complex has been compromised by destructive processes such as infection (Grisel syndrome, tuberculosis), autoimmune joint diseases (rheumatoid arthritis), or connective tissue disorders (Marfan syndrome, Ehler-Danlos syndrome). Nearly 30% of patients with Paget disease and 40% of those with rheumatoid arthritis may experience dislocation at the craniovertebral level (08), and in fact rheumatoid disease is the most common cause of atlanto-axial subluxation (28).

Atlantoaxial dislocation occurs when the forces applied to the C1-C2 articulation exceed the biomechanical limits of the bones and ligaments that define physiologic movement. This can occur in the normal spine or in pathologically weakened states.

Congenital or acquired conditions that result in underdevelopment or weakness of bones, ligaments, or joint capsules may have pathologic movement between C1 and C2. Patients with Stickler, Loeys-Dietz, Marfan, Morquio, Down, or Ehlers-Danlos syndromes have ligamentous laxity and increased incidence of atlantoaxial dislocation (24; 26; 25). The suggestion has been made that atlantoaxial instability may cause Chiari malformation (17). This hypothesis has been met with much discussion and remains speculative, but the association is well recognized (29; 83; 30; 20). Regardless of causation, surgery to decompress and stabilize the craniovertebral junction ensures the anatomic integrity of the foramen magnum and unimpeded flow of CSF (09). A report of atlantoaxial dislocation in two 14-year-old identical twins without history of trauma supports the concept of a congenital etiology without associated syndrome (72).

Inflammatory or autoimmune processes such as rheumatoid arthritis and Reiter syndrome cause destructive changes at the joints and bone-ligament interfaces and compromise the strength of the joint, allowing pathologic movement at C1-C2 under normal stress or low-energy trauma. An example of the latter is heading a soccer ball, manifest in 1 adult by acute upper neck pain and transient quadriplegia requiring surgical fixation of C1-C2 (79). Many neoplasias can metastasize to the spine. Lung, breast, and prostate are the most common. They present with suboccipital and neck pain, and possibly atlantoaxial instability (73). Neurologic deficit is less common than in other areas of the spine because the spinal canal is relatively large at this level.

Neck trauma causing a fracture at the base of the odontoid can lead to a fibrous non-union of the odontoid to the body of C2. Called os odontoideum, it can lead to chronic instability and a delayed presentation of atlantoaxial dislocation (32). Progressive myelopathy or chronic seizures may result from old, unrecognized fractures of the odontoid process with atlantoaxial dislocation; surgery may be curative (01; 05). A retro-odontoid “pseudotumor” may be seen radiographically and associated with atlantoaxial instability and quadriparesis. It is thought to be due to buckling of the posterior longitudinal ligament and may disappear spontaneously following surgery (63). This is in contrast to ossification of the ligament, which is a much more formidable surgical problem (18).

More rarely, severe cervical dystonia may lead to atlantoaxial rotatory subluxation. One case report describes operative reduction and fixation of C1-C2 combined with deep-brain stimulation to ameliorate the underlying problem (74).

Epidemiology

Atlantoaxial dislocation may occur in the general population as a result of trauma or in increased prevalence in a variety of conditions, as discussed previously. It appears to be most commonly encountered in adolescents, often the result of falls (49). One such person was injured by carrying heavy loads on her head, as part of routine farm work (46).

Atlantoaxial dislocation is a long-recognized problem in rheumatoid arthritis patients. Estimates of the incidence of atlantoaxial dislocation in these patients vary from 12% to 40% (34; 41). Improved medical therapies for chronic rheumatoid management may have decreased the incidence of atlantoaxial disease causing neurologic deficit or requiring surgical intervention. This is hopefully the case, for surgery remains challenging (10).

Less than 1% of spinal metastases are found at C1 and C2 (12).

Spinal tuberculosis (Potts disease) occurs in less than 1% of all tuberculosis cases and in 6% of tuberculosis cases that have any extrapulmonary manifestation (02). Of all cases of Potts disease, less than 1% involve the craniocervical junction (Sinha et all 2003).

Prevention

Atlantoaxial dislocation is a low-frequency, unpredictable event. It is not particularly amenable to preventative measures other than the usual safety precautions for the activities of daily living.

Differential diagnosis

Neck pain and deformity may also result from spasmodic torticollis. This results from pathologic contraction of the sternocleidomastoid muscle. The cervical spine is not dislocated in this disorder. Note that a significant percentage of pediatric patients with acute acquired torticollis do not have pathologic C1-C2 fixation and will likely normalize without traction, rigid bracing, or surgery (27).

Kyphosis secondary to Larsen syndrome in the adult may be associated with atlantoaxial dislocation and further complicated by cord compression, neck pain, and spastic quadriplegia (52).

Trauma resulting in a unilateral facet dislocation in the subaxial cervical spine (that is, C3-T1) may also result in neck pain and asymmetry in posture. Less rotation occurs at the subaxial articulations, so the degree of rotation is usually less than may be seen in atlantoaxial rotatory subluxation.

Although rare, atlantoaxial dislocation with compression of the upper cervical spinal cord can mimic acute ischemic stroke (75).

Diagnostic workup

Patients presenting with new neck pain or torticollis should undergo a physical exam to evaluate for any neurologic deficit.

Laboratory tests are not useful in diagnosing atlantoaxial dislocation, except those relevant to diagnosing suspected predisposing conditions.

Clinical diagnosis is principally confirmed by imaging studies. Anteroposterior and lateral cervical spine x-rays are rapid, widely-available, and will usually provide the diagnosis.

The atlanto-dens interval (ADI) can be measures on the lateral view. It should be 2 to 3 mm in adults and 4 mm or less in children. Lateral flexion-extension views can be helpful as they give dynamic information. Most commonly, atlantoaxial instability will result in excessive anterior movement of C1 on C2 in forward flexion. The dens and transverse ligaments are the critical structures restraining anterior subluxation, so excess movement suggests pathologic weakening of 1 or both of these structures. Diagnosis can be difficult in children; the condition is uncommon in this age range, and the developing spine exhibits anatomic characteristics that differ from those of adults (31).

Computed tomography is increasingly used in the routine evaluation of new cervical spine complaints. It provides the most detailed imaging of the bony anatomy. Because dislocation can occur in different planes, pre- and post-operative multiplanar CT scanning is important (57). Three-dimensional CT has proven to be especially helpful in this context (43).

The axial source views combined with sagittal and coronal reformats visualize the fractures and malalignments. Three-dimensional reconstructions from fine-cut bone-window axial source images can also be helpful.

Dynamic CT scanning is finding increased use as well (42).

Magnetic resonance imaging provides the best imaging of soft tissues. Areas of interest are spinal ligaments, joint capsules, the spinal cord, CSF, and any pathologic growths such as solid tumors or tissue pannus (most commonly seen in rheumatoid arthritis). MR is very useful for evaluating new neurologic deficit.

Table 1. The Fielding and the White and Punjabi Classifications of Rotatory Atlantoaxial Dislocation

(11; 80)

Management

Dislocations are classified as reducible (full or partial) or irreducible and treated accordingly (36). Rotatory atlantoaxial dislocation is initially treated with traction followed by external immobilization with a hard cervical collar for 1 to 3 months. Surgery is reserved for cases that do not reduce with traction. Early diagnosis and initiation of traction may reduce the duration of traction needed (37). Persisting mechanical neck pain due to damage to the C1-C2 articulations may also be an indication for fusion. Surgical techniques to correct dislocation or instability and basilar invagination continue to be advanced (06; 06; 16; 56). Over-distraction during occipitocervical fusion may result in displacement of the brainstem, with inadvertent traction on cervical nerves IX, X, AND XI (78). Surgical intervention proceeds better with an understanding of 3-dimensional anatomy. Three-dimensional CT scans and Cartesian coordinates have been used in the assessment of odontoid defects, and 3D printed models used pre- and intraoperatively (14; 59).

Traumatic atlantoaxial dislocation may be managed with surgery or traction and subsequent immobilization with a hard cervical collar or halo (23). A typical management strategy for pediatric patients would be halter or tong in-line cervical traction followed by halo or cervicothoracic brace fixation. Patients who fail to reduce in traction or have recurrent subluxation after external fixation are taken for surgical fusion, which can involve anterior, posterior, or endoscopic approaches (45; 81). Following initial immobilization, range-of-motion exercises are prescribed until normal motion is re-established (33). Chiropractic manipulation may understandably carry some risk (15).

Management of tuberculosis-related atlantoaxial dislocation is controversial. Some argue for surgical decompression and stabilization as the most rapid and definitive method of protecting the spinal cord and restoring spinal stability (68). Others present evidence that the majority of these patients can be successfully treated with rigid external immobilization and anti-tuberculous medication. This has even been used in cases of neurologic deficit (22). With or without surgical intervention, 12 to 15 months of anti-tuberculosis medications should be prescribed.

Rheumatoid atlantoaxial dislocation may be better treated with surgical stabilization than observation, even in patients with neck pain only and no neurologic deficit. Mortality, pain relief, and neurologic function were all improved in 1 long-term follow up comparing the 2 (71). Atlantoaxial subluxation may be an independent marker for increased mortality in rheumatoid patients (51).

Patients with hypermobility (Down syndrome, Marfan syndrome) may be at higher risk for sudden high cervical spinal cord injury from pathologic atlantoaxial movement (38). Although not an immediate indication for upper cervical fusion, these patients should be assessed carefully for pathologic movement and considered for surgical stabilization before any neurologic symptoms are present. Although such conditions may increase surgical morbidity and mortality rates, good results can be achieved with proper case selection and technique (70). In the future, it may be possible to prevent the development of atlantoaxial instability by treating its primary cause; enzyme replacement therapy in Morquio disease is 1 example (48).

Outcomes

Syringomyelia, recognized in some patients with or without Chiari malformation, may be improved (ie, volume of syrinx reduced) with posterior reduction and fixation of basilar invagination/atlantoaxial fusion (65; 64; 77). Occipito-cervical fusion is employed in congenital cases, but may be complicated by delayed redislocation (58). Complications of surgery (eg, wound infection, high cervical myelopathy, velopharyngeal insufficiency, incomplete canal decompression, torticollis, and scoliosis) may require reexploration (67). Although difficult, reoperation for failed stabilization may lead to significant recovery (19).

Special considerations

Pregnancy

Pregnancy does not have a significant influence on the incidence of atlantoaxial dislocation. Pregnancy does not affect treatment paradigms except in the event that surgical treatment is deemed necessary, the risks of anesthesia to the fetus should be evaluated and explained to the patient.

Anesthesia

Patients with cervical spine instability are at risk for new or worsened spinal cord injury during endotracheal intubation. Direct laryngoscopy requires anterior translocation of the jaw. This can cause anterior subluxation of C1 on C2 in a patient with compromised ligaments or bones. The anesthesia team should obviously be made aware of this concern. Patients with cervical spine instability or significant cervical myelopathy from cord compression should usually undergo fiber-optic intubation.