Imaging Studies

A variety of radiographic imaging modalities are used to image the spine in patients with RA. These modalities include plain radiographs, computed tomography (CT) scans, myelography, a combination of CT scans and myelography, CT-angiography, magnetic resonance imaging (MRI), and plain tomography. In addition, dynamic flexion and extension views may be used to augment the information provided by any of these studies. Because the occiput–C1-2 complex is the most frequently involved region of the spine in RA, the majority of imaging studies focus attention on this area. When clinically indicated, imaging studies of the subaxial cervical spine and of the thoracic and lumbar spines should also be performed.

In a study by Younes and colleagues, 72.5% of patients who met the American College of Rheumatology criteria for rheumatoid arthritis had pathology of the cervical spine identified in at least one imaging modality (plain radiographs, MRI, or CT).

On plain radiographs, small or absent osteophytes, osteoporotic vertebrae, and eroded vertebral end plates characterize rheumatoid arthritis. In the absence of RA, degenerative changes are more marked in the lower cervical spine with advancing age. Radiographic changes at the C1-2 level are not present unless a specific process, such as RA, is affecting this region. These changes are independent of age. Bland and coworkers found that 86% of patients with classic or definite RA have evidence of cervical spine involvement on plain radiographs. These changes may frequently be asymptomatic and may not be associated with any neurologic deficit. In patients with severe polyarticular rheumatoid arthritis for more than 20 years, Santavirta and colleagues found radiographic subluxation of the cervical spine in more than 80% of patients.

The most common radiologic abnormality in RA is ventral subluxation of the atlas. The atlantodental interval (ADI) measures the distance between the ventral aspect of the dens and the dorsal ring of the atlas. In normal adult patients, this distance is less than 3 mm. An ADI of between 3 and 5 mm in an adult is abnormal and indicates a tear or insufficiency of the transverse atlantal ligament. A separation of greater than 5 mm indicates rupture or attenuation of the alar ligaments in addition to the transverse atlantal ligament. Many studies have shown a poor correlation between abnormalities of the ADI and neurologic deficits. In an innovative study, Boden and coworkers defined the dorsal atlanto-odontoid interval (AOI) as the distance between the dorsal surface of the dens and the ventral edge of the dorsal ring of the atlas measured along the transverse axis of the ring of the atlas. They demonstrated an excellent correlation between the dorsal AOI and the severity of the neurologic deficit. A dorsal AOI of less than 14 mm correlated significantly with the presence and severity of a neurologic deficit. This dorsal AOI was also found to be a good predictor of neurologic recovery postoperatively. These authors stated that the weak correlation of the ventral ADI with a neurologic deficit may be due to variations in the diameter of the atlas as well as the presence of a pannus behind the odontoid process. Weissman and associates studied 109 patients with RA and atlantoaxial subluxations for 5 years. They found that the ADI increased by more than 2 mm in 41%, remained unchanged in 40%, and decreased in 19% by more than 2 mm. Of the patients whose ADI decreased, more than 50% had developed vertical subluxation of the odontoid process. Henderson and colleagues have stated that vertical subluxation may cause a “pseudofixation” of the ADI. Interpretation of the ADI must therefore be made in conjunction with measurement of the vertical axial subluxation.

Vertical subluxation of the dens is an upward migration of the dens into the foramen magnum ( Fig. 98-1 ). In this location, the dens competes for space with the spinal cord and the brain stem. Vertical subluxation requires the lateral facet joints to be damaged. Vertical subluxation is the second most common upper cervical spine abnormality in RA, after atlantoaxial subluxation, and may accompany ventral atlantoaxial subluxation. An increase in the vertical subluxation may actually produce a decrease in the measured ventral atlantoaxial subluxation. In vertical subluxation, the presence of a rheumatoid pannus, together with the invaginated dens, may produce ventral compression of the cervicomedullary junction.

A, Plain tomogram, lateral view. Vertical subluxation of the odontoid process is clearly demonstrated. The tip of the odontoid is seen dorsal to the clivus in an intracranial position. The arch of the atlas has telescoped down the body of C2. This level of severe bony deterioration can cause the atlantodental interval to actually decrease. B, Sagittal reformation of a CT scan (same patient as in A ). Bony detail and intracranial location of the odontoid are well visualized. The ventral translation of the atlas is more apparent in this view.

In an attempt to quantify vertical subluxation of the dens, numerous lines of craniometry and indices have been proposed ( Fig. 98-2 ). These lines are characteristically drawn between bony landmarks that are identifiable on a lateral cervical spine radiograph. The tip of the dens is then measured with respect to the various lines. A McGregor line is drawn from the hard palate to the occiput and it is probably the most traditional measure. A shortcoming of these lines of craniometry is that the hard palate, the dorsal edge of the foramen magnum, and the tip of the dens are not always visualized on routine lateral cervical spine radiographs in a patient with vertical subluxation of the odontoid. To avoid these difficulties, Ranawat and coworkers developed an index that measures the distance between the diameter of the ring of the first cervical vertebra to the center of the pedicle of the second cervical vertebra. In men and women with normal cervical spines, this distance measured 17 mm in men and 15 mm in women. No normal patients had an interval of less than 15 mm.

Common craniometry lines: McRae line (1), Chamberlain line (2), McGregor line (3).

A cervical myelogram provides an indirect visualization of the spinal cord and adjacent structures silhouetted by contrast media in the subarachnoid space. The information obtained by myelography may be augmented by a postmyelogram CT scan. Computerized myelotomography, with multiplanar reconstruction, can clearly demonstrate the important contribution of proliferative rheumatoid pannus behind the odontoid peg to ventral cervicomedullary compression. In addition, bone windows on the CT scan can demonstrate bony abnormalities.

Currently, MRI is considered the ideal study to demonstrate the level and extent of spinal cord compression. The advantages of MRI include direct imaging of the entire length of the spinal cord and the cervicomedullary junction, direct imaging in multiple planes, superior demonstration of soft tissue structures, and the lack of image degradation by bone artifact at the cervicomedullary junction ( Fig. 98-3 ). In addition, MRI is noninvasive (no intrathecal contrast is needed), can be performed on an outpatient basis, does not expose the patient to the dangers of ionizing radiation, and is generally well tolerated. A limitation of MRI is that it does not image compact bone as accurately as CT scanning does.

Sagittal T1-weighted (TR 500/TE 11) MRI image of ventral compression from a large inflammatory pannus ( white arrow ). The cervicomedullary junction is deformed and attenuated by this soft tissue mass.

Furthermore, Dickman and colleagues have shown that the transverse atlantal ligament can be consistently and clearly visualized with MRI. This determination of a loss of anatomic continuity of the transverse atlantal ligament is useful for operative planning. For patients who are unable to undergo MRI, CT scanning with multiplanar reconstructions provides better information than polytomography. It is important to visualize the neuraxis before surgery. Injecting water-soluble contrast into the lumbar subarachnoid space provides additional important anatomic information regarding the flow of cerebrospinal fluid (CSF) in the upper cervical spine region. Knowledge of the position and course of the spinal vessels, in particular the vertebral arteries, is of extreme importance in many of the surgical approaches to the craniocervical junction. CT angiography provides an excellent means of visualizing the spinal vasculature in relation to the bony anatomy of the upper cervical spine.

Dynamic views of the cervical spine, in flexion and extension, provide useful information about the degree of instability of the occiput–C1-2 complex ( Fig. 98-4 ). These flexion-extension views can be obtained on plain films, tomograms, computerized myelotomography scans, and MRI studies. Dickman and associates recommended routine lateral cervical radiographs in flexion and extension for all patients undergoing transoral surgery. Furthermore, Sharp and Purser recommended lateral flexion and extension radiographs in any patient with severe RA undergoing general anesthesia for any surgical procedure. Bell and Stearns have found MRI in flexion and extension to be very useful for demonstrating dynamic changes in spinal cord configuration. They have used this information to determine the proximal extent of fusion required and have stated that it provides an accurate and dynamic study of the relationship between the spinal cord and the surrounding bony and soft tissue structures. Additionally, upright MRI of the cervical spine can help reveal pathology that may be missed at the craniocervical junction obtained in the supine position.

A, Plain radiograph, lateral flexion view. Significant widening of the atlantodental interval (ADI) with flexion is demonstrated. The occiput-C1 complex translates forward over the C2 vertebra. B, Plain radiograph, lateral extension view (same patient as in A ). The odontoid process is well reduced in extension, with an ADI within normal limits (< 3 mm).

It is also valuable to order a preoperative dual-energy x-ray absorptiometry (DEXA) scan to evaluate for possible osteopenia and osteoporosis. In nonurgent cases, patients who may undergo surgical intervention should be placed on teriparatide for a period of at least 1 month prior to surgical intervention. Teriparatide has been shown to significantly increase the insertional torque of pedicle screw purchase during fusion surgery in osteoporotic patients. Anecdotal reports suggest that fusion rates may also increase, although clinical studies are still under way.

Operative Indications

As a general rule, the presence of myelopathy or a progressive neurologic deficit continues to be a strong indication for surgical intervention in patients with rheumatoid changes of the cervical spine. Likewise, intractable pain is an indication for operative intervention. A much more controversial topic is whether a patient with markedly abnormal radiographs, in the absence of pain or a progressive neurologic deficit, should undergo surgery. Numerous authors believe that radiologic evidence of an impending neurologic deficit is an indication for surgery. Pellicci and associates believe that radiographic evidence of disease progresses to a greater degree than does neural involvement. As such, they believe that no fusion should be recommended on the basis of a radiographic abnormality or radiographic deterioration alone. Others have supported this more conservative viewpoint. In an intermediate position, Boden and colleagues stated that only patients with a neurologic deficit underwent surgery in their series. Nevertheless, they recommended surgery for patients, with or without a neurologic deficit, if certain radiographic criteria were met.

Crockard reviewed his results with 55 severe end-stage RA patients (Ranawat grade IIIB). He found that those patients who are bed-bound for more than 3 months fare extremely poorly, regardless of whether surgical intervention is undertaken. In addition, with these Ranawat grade IIIB patients, mortality rates are unacceptably high in many cases. Therefore, one must question the previously held view that the presence of a myelopathy in a long-term, bed-bound Ranawat grade IIIB patient is an absolute indication for surgery.

Specific Regions of the Spine

Lower Cervical Spine

As with abnormalities of the upper cervical spine, the presence of subaxial subluxations of the lower cervical spine varies greatly in reported series. Subaxial subluxation is a gradual process in which there is a forward displacement of one or more vertebral bodies on the vertebral body immediately below ( Fig. 98-5 ). The rheumatoid process attacks the zygapophyseal facet joints and the uncovertebral joints, weakens the supporting ligaments, and erodes the intervertebral discs. These effects loosen the various intervertebral fixations and permit luxation between adjacent vertebral bodies. Subaxial subluxations are usually reducible by traction; however, the reduction is difficult to maintain. Classically, subaxial subluxation is a translation of one vertebra in relation to an adjacent vertebra of greater than 3.5 mm on a lateral cervical spine radiograph. Boden and associates found that the diameter of the subaxial sagittal spinal canal reflected the presence and degree of a neurologic deficit more often than did the percentage of vertebral body slip. In addition to the bony luxations, compression from epidural rheumatoid granulations has been reported.

A, Plain radiograph, lateral flexion view. Multiple subaxial subluxations are seen with neck flexion, producing a “staircase” effect. The vertebral body translates forward with respect to the immediate subjacent vertebral body. Vertical subluxation of the odontoid process is also seen in this view. B, Plain radiograph, lateral extension view (same patient as in A ). Neck extension causes a marked correction in the degree of subaxial subluxations. There is no change in the relationship between the atlas and the axis with neck motion.

Subaxial subluxations are usually late developments in the aggressive forms of RA. The severity of these subaxial subluxations is also closely related to the duration of rheumatoid disease. When compared with patients with atlantoaxial subluxations, the incidence of neurologic deficits is higher in patients with subaxial subluxation, and the final results are poorer.

Typically, subaxial subluxations show a “staircase” appearance with multiple subluxations observed sequentially in the cervical spine. Subaxial subluxations may result in nerve root impingement from foraminal narrowing. The presence of a subaxial subluxation should be suspected when bizarre weakness of the hands is observed in a patient with RA. This may be difficult in patients with long-standing disease who already have crippling deformity of the hands. This subaxial spinal cord involvement may cause myelopathy and may explain why some patients do not respond to surgical decompression at the craniocervical junction. The most common site for subaxial subluxation is at the C3-4 level; however, it often occurs at multiple levels, and these typically lack osteophytes.

Subaxial subluxations may be present at the time of surgery for an upper cervical instability. The caudal extent of the instrumentation and fusion must therefore be carefully selected to consider incorporation of segments with a significant subaxial subluxation. In an autopsy study of nine patients with severe end-stage RA, Henderson and colleagues found subaxial compression present in eight of the nine patients. More commonly, subaxial subluxations may occur after fusion operations in the upper cervical spine. As a result, it is essential that patients who undergo upper cervical fusions be followed closely with lateral cervical spine radiographs both for evidence of an acceptable bony fusion and for the development of subaxial subluxations. Kraus and coworkers found a much higher incidence of subaxial subluxations in patients whose upper cervical fusion incorporated the occiput. They postulated that this was because of a longer lever arm that results in higher forces generated at the lower cervical levels and that leads to a subaxial subluxation. Subaxial cervical subluxations in RA patients have been associated with quadriplegia, sudden death, and other neurologic complications resulting from damage of the spinal cord or from interference with the flow of the vertebral arteries.

The most accurate radiographic imaging study currently available to detect the site and type of spinal cord compression in subaxial subluxation of the rheumatoid spine is MRI. All patients with subaxial subluxations and atlantoaxial subluxations with neurologic deficits or vertical subluxations of the dens should have an MRI study, if possible. In patients who cannot undergo an MRI study, a myelogram followed by a postmyelogram CT scan should be obtained.

Surgical Management of the Rheumatoid Spine

Many different operations have been recommended for patients with RA of the spine ( Fig. 98-6 ). The various options include a dorsal cervical fusion of C1-2, an occipitocervical fusion, a transoral approach, ventral and dorsal approaches to the subaxial cervical spine, and various combinations of these approaches. With the advent of spinal instrumentation techniques, surgeons have a wealth of different treatment options available to treat RA patients. In addition, nonoperative modalities including traction and halo-vest immobilization, as well as adjuvant medical therapies such as steroids, nonsteroidal anti-inflammatory drugs, penicillamine, and methotrexate, enter into the decision-making process.

Algorithm for care of the patient with rheumatoid arthritis.

Most RA patients never develop spinal instability and never require spine surgery. As previously described, large studies of patients from rheumatology clinics have demonstrated that the clinical course of RA is usually benign. However, the natural history of the disease is that a certain proportion of affected patients eventually require surgery. Pellicci and colleagues followed 106 patients for more than 5 years and found that diligent use of a supportive collar does not alter the natural history of the disease. Similarly, More and Sen have stated that the realistic treatment goals achieved by conservative measures are pain abatement and reduction of inflammation. The natural history of the disease is not altered. Pellicci’s study also documented that rheumatoid involvement of the cervical spine does not appear to shorten life expectancy. These findings are most likely a result of the small number of RA patients who develop cervical myelopathy. When cervical myelopathy is established, the natural history without surgical intervention is grave. In addition, the development of a subaxial subluxation or a vertical subluxation in a patient with a preexisting atlantoaxial subluxation has been found to be a poor prognostic sign. The factors that influence the treatment of upper cervical lesions in RA are reducibility of the abnormality with traction, the type of compressive lesion (whether of a bony or a soft tissue component), and the direction and mechanics of the spinal cord or brain stem compression.

There is a general agreement among the majority of neurosurgeons and orthopaedic spine surgeons that intractable pain, progressive neurologic deficit, and the presence of myelopathy are indications for surgical intervention. On the other hand, there is considerable disagreement over surgery for the “risk of instability,” which is usually construed by a variety of criteria analyzing radiographic imaging studies of the upper cervical spine.

With appropriate operative indications, the treatment of an isolated atlantoaxial subluxation is a dorsal C1-2 fusion. In these cases, the occiput should not be incorporated into the fusion because the higher complication rate, lower fusion rate, and morbidity associated with the decreased range of neck motion all mitigate against this procedure.

If vertical subluxation of the dens is present, or a combination of a vertical subluxation with an atlantoaxial subluxation is present, an occipitocervical fusion may be required. To determine whether an occipitocervical fusion alone is adequate, or a ventral decompression is necessary, cervical traction, in addition to the dorsal stabilization, may be used to determine whether the subluxation is reducible. Transoral decompression may also be deemed necessary if significant soft tissue rheumatoid granulation—that is, a rheumatoid pannus—is responsible for compression of the spinal cord.

Viewpoints in the management of vertical subluxation of the dens are divergent, as has been shown in numerous studies published by Menezes and coworkers and Crockard and associates Menezes and coworkers maintain that it is the reducibility of a vertical subluxation that is the primary determinant of whether a transoral decompression is necessary. They determined that in 80% of their patients, an adequate reduction of the vertical subluxation could be achieved with traction and, therefore, only a dorsal occipital cervical fusion was necessary. Despite the reducibility, all 45 patients in this series were symptomatic because of compression of the cervicomedullary junction. In addition, these authors have stated that decompression of the cervicomedullary junction, via a transoral approach, is necessary for irreducible lesions. They found that all patients with greater than 20 mm of penetration of the dens through the foramen magnum were unable to have their deformity reduced with cervical traction and required a transoral decompression. Dickman and colleagues have also recommended a transoral decompressive procedure for irreducible craniovertebral junction compression. Both Menezes and coworkers and Dickman and colleagues have recommended that the ventral decompressive surgery should be performed first and subsequent dorsal internal fixation later. Transoral surgery involves the resection of the dens, the ventral arch of the atlas, the ventral longitudinal ligament, the apical ligament, the alar ligament, the transverse atlantal ligament, and the tectorial membrane. As such, the spine is destabilized after this procedure, necessitating a dorsal fusion. Menezes and Van Gilder have described the advantages of the transoral approach to irreducible craniovertebral junction pathology. These include performing surgery in an avascular midline plane, accessibility to both bony and soft tissue pathology, and performing surgery with the patient’s head in an extended position (which decreases brain stem angulation and compression during the surgery). This approach allows for exposure from the lower half of the clivus to the C2-3 interspace. These authors emphasized the need for a tracheotomy in all transoral surgeries.

Crockard and colleagues have stressed the contribution of a ventral compressive agent, the rheumatoid pannus, to be as important as any bony deformity in the development of spinal cord compression. Crockard and Grob stated that the overall results of dorsal cervical surgery alone for patients with cervical myelopathy have been unsatisfactory with excessively high morbidity and mortality rates. For patients with an established myelopathy in whom the pannus has been demonstrated to contribute to the cervicomedullary junction compression, Crockard performs a transoral decompression with a dorsal occipitocervical fusion in a single one-stage operation with the patient in the lateral position. Traditional skull traction is may be used preoperatively, but the head is held in the Mayfield retractor with a tilt table, which, in effect, functions like skull traction. In Crockard’s experience, this one-stage procedure has led to fewer complications and better long-term results than either a two-stage operation or a dorsal fixation procedure alone. Performing both operations at a single sitting avoids the discomfort of prolonged bed rest and the complications associated with prolonged immobilization. In most patients, Crockard has not found it necessary to perform a tracheotomy.

The surgical management of the craniocervical junction can vary. Since the 1990s, we have noticed an increasing number of cases that can be treated by a dorsal alone approach. In addition, appreciable morbidity is apparent following transoral surgeries in these often frail, elderly RA patients. As a result, our operative approach has been to favor posterior treatments whenever feasible.

As with the operative approaches to vertical subluxations, treatment of subaxial subluxations of the cervical spine is varied. Simpson and coworkers have stated that surgery for subaxial subluxations involves a dorsal fusion and that the role of ventral surgery is unclear in this condition. Santavirta and colleagues have indicated that reduction of the bony subluxation with a fusion is not adequate in patients with spinal cord compression from subaxial subluxation because rheumatoid granulation tissue in the sublaminar space may continue to compress the neural elements. Therefore, they recommend laminectomy in addition to this fusion procedure. King has stated that a dorsal decompression may relieve the spinal cord compression. It may also, however, worsen spinal instability. At present, the optimal surgical treatment for subaxial subluxation of the rheumatoid cervical spine is unclear.

Due to frequently encountered osteopenia/osteoporosis and lower fusion success rates in RA patients, we have increasingly performed anterior-posterior (AP) surgeries for subaxial subluxation patients with multilevel anterior discectomies and posterior stabilizations. Alternatively, studies have advocated the use of teriparatide pre- and postoperatively to address issues in bone quality and fusion. Posterior decompressions may or may not be necessary as a part of the surgeries depending on a careful review of the preoperative imaging studies.