Historical Perspective

There is some evidence that rheumatoid arthritis was described in the 17th and 18th centuries.^6,7 More concrete evidence points to a period around 1800, according to a description by Landré-Beauvais, a French medical student, in his doctoral thesis.⁸ The description of rheumatoid arthritis of the cervical spine occurred much later, with a report in 1890 by Garrod.⁹

Interest increased in the 1950s and 1960s with reports describing cervical instability.^10–13 Articles on the surgical treatment of cervical instability in patients with rheumatoid arthritis followed in the 1960s and 1970s.^14–18 For the most part, C1-2 fusion with Gallie-type¹⁹ wiring and graft techniques were used early on. Brooks and Jenkins,²⁰ Wertheim and Bohlman,²¹ and Clark and colleagues²² subsequently described modified wiring techniques. Other types of C1-2 fixation emerged later with the use of the Halifax interlaminar clamp,²³ the Magerl transarticular screw technique,^24–28 and posterior C1 lateral mass–C2 pedicle screw fixation.²⁹

Foerster³⁰ originally described occipitocervical procedures in 1927. Kahn and Yglesias³¹ were the first to add iliac crest bone graft to occipitocervical fusion in 1935. Hamblen¹⁶ later described the combined use of wires and iliac crest graft for occipitocervical fusion in four patients with rheumatoid arthritis and cervical instability in 1967. In a 1976 report, Brattström and Granholm¹⁴ modified the wiring technique for occipitocervical fusion by adding methyl methacrylate. Modifications of occipitocervical fusion techniques continued in the 1980s with the emergence of the looped rod with iliac crest bone graft, as described by Ransford ³² and Flint ³³ and their colleagues and later occipitocervical plating, as described by Grob^34,35 and Smith³⁶ and their colleagues. Current use of plate or rod fixation extends to the subaxial spine, especially with fixation of the lateral masses described by Magerl and Roy-Camille.^25–27

Pathophysiology

The inflammatory process in the cervical spine mirrors the inflammatory process in other sites of the body and consists predominantly of T lymphocytes, macrophages, and plasma cells in a hypervascular synoviocyte pannus.^37,38 The inflammatory reaction has a predilection for synovial joints, and the multiple synovial joints³⁹ of the cervical spine (facets, uncovertebral, atlanto-occipital, atlantodens) are particularly affected. In contrast to the thoracic and lumbar spine, the cervical spine relies heavily on ligaments and joint congruency for stability and so is at greater risk for instability. With significant inflammation, pannus formation and erosion of the joint and capsular structures can occur. Progressive instability can result, manifesting as atlantoaxial (C1-2) instability, subaxial subluxation, cranial settling (also known as basilar invagination or atlantoaxial impaction), or a combination thereof. Rheumatoid discitis may also occur at the discovertebral junctions with noninfectious erosion of the endplates.³

Atlantoaxial instability is the most common instability pattern in the rheumatoid cervical spine and may be the result of the development of periodontoid pannus and progressive inflammatory destruction of the upper cervical spine.^39–41 Pannus formation localizes around the synovial joint formed between the transverse ligament, the posterior arch of the atlas, and the base of the odontoid. The soft tissue may compress the spinal cord and often distends and erodes the surrounding periodontoid-ligamentous structures (alar, apical, and transverse ligaments), the odontoid process (dens), and the lateral articular masses between C1 and C2.⁴² Erosion of the dens may lead to the development of occult, atraumatic odontoid fractures.⁴³ Subsequent static or dynamic instability or subluxation occurs in 50% to 70% of patients.^18,44 Most often, the subluxation is anterior (70%), but lateral, posterior, and rotational subluxations can also occur.^45,46 Anterior subluxation of 0 to 3 mm is normal in adults, subluxation of 3 to 6 mm suggests instability with disruption of the transverse ligament, and subluxation of 9 mm or more suggests disruption of the entire periodontoid-ligamentous and capsular structures with gross instability and is a clear indication for surgery.^18,47,48

The combination of periodontoid pannus buildup and instability may cause spinal cord and root impingement leading to myeloradiculopathy and sudden death. Delamarter and Bohlman⁴⁹ conducted postmortem studies suggesting that paralysis can be due to mechanical neural compression, vascular impairment of the neural structures, or both. Henderson and colleagues⁵⁰ reported that diffuse axonal injury with or without frank necrosis may irreversibly affect the spinal cord owing to mechanical damage. These findings may partly explain the smaller diameter and cross-sectional area of the spinal cord found in patients with severe disease.⁵¹ Some evidence suggests that instability promotes worsening periodontoid pannus formation and that stabilization reverses the buildup.⁴⁰

Posterior atlantoaxial subluxation is rare and should raise the possibility of an anterior arch defect of the atlas or erosion or fracture of the odontoid.⁴⁸ Patients usually present with myelopathy and posterior kinking of the cord without radiographic compression.⁵² Lateral subluxation is defined as more than 2 mm of lateral displacement of the C1-2 lateral masses and occurs in 21% of atlantoaxial subluxations.⁴⁸ Lateral subluxations occur more commonly in patients with spinal cord compression than patients without compression and are often accompanied by rotational subluxation.⁵³

Subaxial subluxation is the second most common instability pattern and results from destruction of the facet joints, interspinous ligaments, and discovertebral joints.^44,54 These pathologic changes can lead to longitudinal collapse, bony erosion, soft tissue hypertrophy, and sagittal plane instability along multiple spinal segments, causing a “stepladder”-type pattern of deformity. Concurrent spondylodiscitis may occur with pain, neural compression, and instability.

Cranial settling occurs primarily because of bone and cartilage destruction of the atlantoaxial and occipitoatlantal joints in contrast to ligamentous laxity. Although the least common of the three instability patterns, it is the most ominous form. Caudad settling of the cranium and apparent cranial migration of the odontoid are characteristic. As a result, there is an increased risk of sudden death from either static or dynamic stenosis of the foramen magnum and compression of the medulla oblongata (brainstem). Other sequelae include obstructive hydrocephalus or syringomyelia presumably from direct mechanical blockage of normal cerebrospinal fluid flow. In some cases, fixed rotation of the head may occur because of unilateral involvement of the atlantoaxial and occipitoatlantal joints.

Natural History

It is difficult to study the natural history of rheumatoid arthritis because patients are usually treated at some stage of the disease and it would be unethical to do otherwise. From studies on rheumatoid arthritis, it seems consistent that the inflammatory processes in the cervical spine begin early after the onset of rheumatoid arthritis and progress along with peripheral involvement. Atlantoaxial instability may be detected within 2 to 10 years of disease onset in most patients,⁵⁵ and there is a strong correlation between cervical spine subluxation and peripheral erosions of the hands and feet.⁵⁶ Approximately 10% of patients with cervical spine involvement eventually require surgery.⁵⁷

The natural history of rheumatoid arthritis of the spine without surgical intervention, especially in patients with myelopathy, seems to be progressive disability and risk of sudden death. In one study of 21 patients treated medically, 76% showed deterioration at an average of 6 years of follow-up. All patients in the study became bedridden within 3 years of developing myelopathy, and all died within 7 years with one third dying suddenly for unknown reasons.⁵⁸ Risk factors for progression include mutilating articular disease, history of high-dose corticosteroid use, high seropositivity, rheumatoid subcutaneous nodules, vasculitis, and male gender. Other potential but unproven risk factors for cervical involvement include high C-reactive protein level and HLA-Dw2 or HLA-B27 positivity.^59,60 As the disease progresses, pain, neurologic deficits, and sudden death are the primary risks.

Clinical Presentation

Neck pain is the most common symptom in patients with cervical spine involvement. Peripheral erosive changes similarly occur along the apophyseal joints and surrounding soft tissues and may be a source of pain. Cervical instability may cause secondary impingement of the posterior rami of the lesser and greater occipital nerves, which may lead to occipital headaches. Pain in the suboccipital region generally suggests atlantoaxial pathology or cranial settling. Middle or lower cervical pain should suggest subaxial subluxation. These are not hard and fast rules because pain localization in rheumatoid cervical disease may be poor. Subaxial involvement may also lead to painful neck deformity with loss of sagittal plane supporting structures, which may later become fixed deformities owing to postinflammatory ankylosis. Patients may complain of a “clunking” sensation in the neck with neck motion. This sensation is most common in patients with C1-2 instability, owing to spontaneous reduction of the subluxation with neck extension (known as the Sharp-Purser test).⁶¹

Progressive instability leads to decreased effective canal diameter and brainstem compression. Myelopathy and vertebrobasilar dysfunction may result because of mechanical and ischemic damage to the white and gray matter evidenced on histologic specimens by long tract demyelinization, lateral column necrosis, and focal gliosis.⁴⁹ According to Bell,⁶² C1-2 instability may lead to a phenomenon termed cruciate paralysis, characterized by upper motor neuron dysfunction of the upper extremities with paresis and paralysis and normal lower extremities similar to a mild central cord syndrome after trauma. Pathologically, there is selective injury to the decussating corticospinal tracts of the upper extremities at the level of the cervicomedullary junction with sparing of the uncrossed lower extremity pyramidal and extrapyramidal tracts.

Additional neurovascular changes may occur because of vertebral artery occlusion with decreased flow into the posterior inferior cerebellar artery and cephalad brainstem circulation. Without adequate collateral blood flow, these patients may develop Wallenberg syndrome or lateral medullary infarction. These clinical syndromes are characterized by ipsilateral cranial nerve palsies (cranial nerves V, IX, X, and XI), cerebellar ataxia, Horner syndrome (ptosis, miosis, anhidrosis, and enophthalmos), facial pain, and contralateral loss of pain and temperature sensation.⁶³ Rarely, patients may develop quadriplegia, quadriplegia with facial muscle paralysis (locked-in syndrome),⁶⁴ and sudden death.^38,58

In contrast to pain symptoms, neurologic signs are less straightforward. Myelopathy is progressive but may not be evident by loss of fine motor control, gait imbalance, or global numbness of the hands, but rather by the slow onset of deteriorating independence and becoming wheelchair bound. In many instances, hand deformities mask motor deficits in the upper extremities, and the patients’ deteriorating ambulatory status may be attributed to large joint involvement rather than myelopathy. Patients must be assessed keeping their global disease in mind. Progression of myelopathy, especially early disease, may be misinterpreted as progression of peripheral disease. A high index of suspicion is necessary in these patients to detect early myelopathy because patients do poorly without early surgical intervention.^38,58

The Ranawat grading system may provide some useful clinical information in assessing patients with neurologic deficits (Table 34–1).⁶⁵ This system classifies pain as none (grade 0), mild (1), moderate (2), or severe (3). Neurologic function falls into three classes: Class I has no neurologic deficit; class II has subjective weakness, dysesthesia, and hyperreflexia; and class III has objective weakness and long tract signs. This last class is subdivided further into class IIIA, in which patients are ambulatory, and class IIIB, in which patients have quadriparesis and are unable to walk. Casey and colleagues⁶⁶ reported that only 25% of 55 Ranawat class IIIB patients who underwent surgical decompression and stabilization had a favorable outcome. The mortality rate was 13% after 30 days and 60% by 4 years.

TABLE 34–1 Ranawat Criteria for Pain and Neural Assessment

Adapted from Ranawat CS, O’Leary P, Pellici P, et al: Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am 61:1003-1010, 1979.

Radiologic Evaluation

Plain radiographs are an effective screening tool for identifying patients with atlantoaxial instability, cranial settling, or subaxial subluxations. Standard anteroposterior, open-mouth (odontoid view), lateral, and controlled flexion-extension plain views should suffice. The flexion-extension views are the most important in detecting whether there is dynamic or static instability in the upper or lower cervical spine and allow for measurement of the anterior atlantodental interval (AADI) and posterior atlantodental interval (PADI). AADI is measured from the anterior surface of the dens to the posterior margin of the anterior ring of the atlas along a transverse axis of the atlas, whereas PADI is the distance between the posterior surface of the dens and the anterior margin of the posterior ring of the atlas.

Historically, the AADI was used to screen patients who required surgical stabilization for atlantoaxial instability based on an AADI greater than 9 mm, with AADI 0 to 6 mm suggesting instability and AADI 0 to 3 mm being normal.⁴⁸ AADI is limited by the occasional difficulty of obtaining accurate measurements in some patients because of erosive changes that distort the normal anatomic landmarks and because it has not been correlated clinically with the mass effect of retrodental pannus that may compress the spinal cord. Boden and colleagues⁶⁷ showed that PADI may be more reliable in predicting neurologic outcome because it is a more accurate indicator of the space available for the cord. Patients with a PADI of at least 14 mm were more likely to have neurologic recovery after surgical stabilization, whereas patients with a PADI less than 10 mm had no neurologic recovery. These observations can also be explained by the anatomy of the spinal cord at the C1 level because the dura requires an average space of 1 mm on the anterior and posterior sides, the cerebrospinal fluid requires 2 mm, and the cord requires 10 mm for a total space of 14 mm.⁶⁸

The open-mouth view is useful to identify lateral subluxation, defined as more than 2 mm of lateral displacement of C1-2 lateral masses, which occurs more commonly in patients with spinal cord compression than in patients without compression.^48,53 Erosive changes of the dens and C1-2 articulations may also be visualized. Taniguchi and colleagues⁶⁹ defined the atlantodental lateral shift (ADLS) as a means of assessing lateral atlantoaxial instability. Using dynamic open-mouth odontoid views (taken in maximal left and right lateral bending), ADLS is calculated by dividing the distance from the center of the dens to the medial edge of the C1 lateral mass (in the direction of lateral bending) by the distance between the medial borders of the bilateral C1 lateral masses and is expressed as a percentage. With this method, these investigators noted that in patients with rheumatoid arthritis, the ADLS averaged 14.8% compared with 6.1% in control patients. Among the subgroup of patients with rheumatoid arthritis and increased AADI, the ADLS averaged 20.6% versus 12.7% in patients without anterior atlantoaxial instability.

Posterior subluxation, although rare, may be seen on lateral radiographs of the cervical spine and should be suspected in patients with an absent or fractured odontoid process.⁵² The AADI decreases with worsening cranial settling as the arch of the atlas approaches the wider base of the odontoid process and is a potential source of mistaken radiographic improvement.

Cranial settling carries the greatest risk of neurologic deficits and sudden death, especially when superimposed on atlantoaxial instability. As a consequence, several measurement techniques have been used with varying sensitivity and specificity, based on lateral plain radiographs of the upper cervical spine (Fig. 34–1).⁷⁰ Most of these techniques assess the relationship between the tip of the odontoid, the hard palate, and the base of the skull. Traditionally, McGregor line (drawn from the posterosuperior tip of the hard palate to the caudad base of the occiput) has been widely used for its simplicity. Cranial settling occurs when the tip of the dens is more than 4.5 mm above this line.

FIGURE 34–1 Drawing of lines for measurements of basilar invagination. Chamberlain line: Odontoid tip greater than 6 mm above line. McCrae line: Odontoid tip above this line. McGregor line: Men, odontoid tip greater than 8 mm above line; women, odontoid tip greater than 9.7 mm above line. Redlund-Johnell distance: Men, less than 34 mm; women, less than 29 mm.

Erosive changes in the odontoid anatomy may make it difficult to analyze many of the measurement techniques, so Redlund-Johnell and Pettersson⁷¹ described a technique that measured the vertical line from the midpoint of the caudad margin of C2 to McGregor line. Cranial settling occurs when the distance is less than 34 mm in men or less than 29 mm in women. Ranawat and colleagues⁶⁵ described a similar technique in which the distance along the odontoid was measured from the C2 pedicle to the transverse axis of the ring of C1. This technique avoided problems with changes in odontoid anatomy and identifying the bony landmarks at the base of the skull and hard palate. Cranial settling was positive if the distance was less than 15 mm in men or less than 13 mm in women. Clark and colleagues²² defined the “station of the atlas” (Fig. 34–2), which indicates the position of the anterior ring of C1 to parts of the body of the axis divided into thirds. Normally, the atlas is adjacent to the upper third (station I) of the axis. Riew and colleagues⁷⁰ noted that none of the current radiographic measurements alone had a sensitivity, specificity, or negative or positive predictive value greater than 90% and recommended the combination of the Clark station, Redlund-Johnell criteria, and Ranawat criteria with sensitivity and negative predictive values of 94% and 91%.

FIGURE 34–2 Station of atlas is determined by dividing odontoid process into thirds in sagittal plane. Normally, anterior ring of atlas should be adjacent to cephalad third of axis (station I). If ring of atlas is adjacent to middle third of axis, mild cranial settling is indicated (station II). If anterior ring of atlas is adjacent to base of axis, it is considered evidence of severe cranial settling (station III).

(From Clark CR, Goetz DD, Menezes AH: Arthrodesis of the cervical spine in rheumatoid arthritis. J Bone Joint Surg Am 71:381-392, 1989.)

Subaxial subluxation is the second most common instability pattern and occurs secondary to inflammatory destruction of the apophyseal and discovertebral joints and supporting soft tissues. White and Panjabi⁷² defined radiographic cervical instability as 3.5 mm or more of vertebral translation and greater than 11 degrees of angular changes between adjacent motion segments, although their study is more representative of acute conditions. The space available for the cord should also be considered in these patients because critical stenosis may be present with or without instability. Boden and colleagues⁶⁷ correlated anatomic measurements with neurologic findings and reported that a sagittal diameter of less than 14 mm was considered critically stenotic in the rheumatoid subaxial spine. This is in contrast to 13 mm in cervical spondylotic patients who do not have pannus in the canal.

Computed tomography (CT), especially with intrathecal contrast medium, is a valuable addition to plain radiographs in delineating the bony anatomy and identifying cord compression and cranial settling. The degree of medullary compression on CT scans has been shown to correlate with myelopathy.⁴⁰ Static or dynamic magnetic resonance imaging (MRI) is the best option, however, to assess the soft tissues and to look for the presence of periodontoid pannus (Fig. 34–3) and spinal cord or brainstem compression.^73–75 MRI is also useful for postoperative evaluation of the periodontoid pannus, which has been shown to decrease after stabilization.⁴⁰ Myelopathic signs correlate with MRI findings⁷⁵ of a cervicomedullary angle of less than 135 degrees (normal 135 to 175 degrees). This angle measures the intersection of vertical lines drawn along the anterior surface of the brainstem and the cord on sagittal MRI.

FIGURE 34–3 Illustration showing forward subluxation of atlas on axis, pannus formation around odontoid process, and osseous erosions. There is severe compression of spinal cord between pannus anteriorly and arch of atlas posteriorly.

(From Boden SD, Dodge LD, Bohlman HH, et al: Rheumatoid arthritis of the cervical spine: A long term analysis with predictors of paralysis and recovery. J Bone Joint Surg Am 75:1282-1297, 1993.)

Nonsurgical Treatment

Although life expectancy is lower in patients with rheumatoid arthritis, many are living longer with their disease because of more aggressive medical therapy that has slowed disease progression with fewer side effects.⁵⁹ Only a few of these patients eventually need surgical stabilization. Patients with early cervical disease and intermittent pain without radiographic instability or myelopathy can be managed with a soft cervical orthosis or trials of physical therapy. Medication options include nonsteroidal anti-inflammatory drugs (NSAIDs); oral steroids (prednisone); and disease-modifying antirheumatic drugs (DMARDs) such as methotrexate, gold, sulfasalazine, hydroxychloroquine, penicillamine, and azathioprine.

In recent years, biologic agents such as tumor necrosis factor (TNF)-α and interleukin-1 antagonists have become increasingly available. The addition of antiresorptive osteopo-rosis therapy may improve vertebral bone strength in patients with rheumatoid arthritis.⁷⁶ Patients should be followed closely for neurologic or radiographic changes. Cervical collars provide support, warmth, some pain relief, and a feeling of stability; however, rigid collars are often poorly tolerated, especially in patients with temporomandibular disease, dental problems, and skin sensitivity, and may have further detrimental effects by blocking spontaneous reduction of anterior atlantoaxial subluxation in extension.

Surgical Management

Operative Procedures

Atlantoaxial (C1-2) Instability

Posterior fusion is considered the standard procedure using sublaminar or interspinous wires, hook-claw constructs, or transarticular screws. Gallie¹⁹ and Brooks²⁰ wiring techniques require the presence of the posterior arch of C1, supplemental bone graft, and external immobilization. Claw-type constructs such as the Halifax clamp are rarely used today because of biomechanical limitations and better options. Transarticular screw fixation is popular because of its multidirectional rigidity, but it requires intraoperative fluoroscopy and preoperative axial imaging to visualize the vertebral artery anatomy. Direct screw fixation of the C1 lateral masses and C2 pedicles, pars, or lamina has been described more recently.^29,88,89

Wire Techniques

Stand-alone wiring techniques have largely been replaced by transarticular screw or direct screw-rod fixation techniques. Wiring techniques are frequently used as adjuncts to other fixation, particularly for securing bone graft material to help facilitate fusion. In addition, a thorough knowledge of these methods is necessary because their use may be required as a “bailout” in patients with anatomy unfavorable to other techniques.

The Gallie wiring technique plus bone graft was described in 1939 for fracture fixation in the cervical spine.¹⁹ Sublaminar wire fixation is obtained on the C1 ring and around the C2 spinous process (Fig. 34–4). The authors recommend a modification of the Gallie technique. The patient’s head is placed in a tong-type holder for rigid positioning. Intraoperative imaging should be used to determine the final position of the head and neck and to confirm adequate reduction of C1. The chin should be tucked to open the space between the occiput and C1 to facilitate passage of sublaminar wire. An occiput-to-C2 fusion may be safer with or without a C1 laminectomy in cases of an inadequate posterior space available for safe wire passage of an unreducible C1 ring.

FIGURE 34–4 A and B, Modified Gallie-type wiring for posterior C1-2 arthrodesis.

A posterior exposure is used, remaining close to the midline with no more than 1.5 cm lateral dissection on the C1 ring to avoid the vertebral artery and the venous plexus between C1 and C2. Cobb elevators are used to expose subperiosteally the base of the occiput to the caudad aspect of the C2 lamina at a minimum. Small curets can be used to develop the plane under the C1 ring for wire passage. A loop is created with a 20-gauge wire with the tip contoured for safe passage under the C1 ring. A nerve hook is used to engage the loop and pull it through approximately 2 cm. The free ends of the 20-gauge wire are fed through the loop, and the wire is cinched down tightly onto the C1 ring at the midline. Alternatively, sutures may be passed underneath C1 with a Mayo needle placed in a reverse manner with the blunt end from caudad to cephalad.

Wires are placed within the suture loops and passed underneath the lamina as the sutures are withdrawn caudally. A bur hole is made at the base of the C2 spinous process, and a second 20-gauge wire is passed through the hole and looped beneath the spinous process and through the hole again to provide stress distribution. Two rectangular blocks of corticocancellous iliac crest bone graft can be harvested and placed over the laminae of C1 and C2 on either side of the midline. The grafts should be near full–thickness to allow for tightening of the wires with less risk of breaking through the fragile bone. The wires are tightened over the graft while watching closely to prevent wire breakthrough. Cancellous chips can be placed around the bone blocks and especially on the ring of C1, where nonunions tend to occur. A drain is typically used, and the wound is closed in layers. If no supplemental internal fixation is used, a halo vest may be needed postoperatively to help maintain reduction. Care must be taken when tightening the wires in the unusual case of a C1 ring that is posteriorly partially dislocated because this tends to subluxate the C1 ring posteriorly. The authors suggest a Brooks technique in this situation.

A Brooks-type modification of the Gallie technique uses bilateral sublaminar wires beneath C1 and C2 (Fig. 34–5). Positioning and exposure are as described for the Gallie technique. A laminotomy may be done between C2 and C3 to facilitate wire passage, a 20-gauge wire is looped, and the looped end is threaded beneath the lamina of C2 and C1 on either side of the midline. Near full–thickness corticocancellous iliac crest bone grafts are harvested and placed on the lamina of C1 and C2. The grafts should be contoured to fit snugly to reduce the risk of graft slippage. Alternatively, a full bone block may be used with a space in the caudad end to fit around the C2 spinous process. Decortication is unnecessary and risks weakening the lamina. The wires are tightened down in a longitudinal fashion over the bone block on either side. This fixation may provide more rotational stability over the Gallie technique because of fixation on both sides of the midline. A halo vest may be used at the discretion of the surgeon based on the need for maintaining reduction and the adequacy of intraoperative fixation.

FIGURE 34–5 A and B, Brooks-type wiring for posterior C1-2 arthrodesis. Sublaminar wires are passed under C1 and C2 and are tightened down over wedge-shaped, sculpted corticocancellous grafts. Shaping of grafts minimizes chance of graft displacement into canal.

Transarticular Screw Fixation

The technique of transarticular screw fixation provides the most rigid fixation for atlantoaxial fusion and can be used in conjunction with wire techniques to provide three-point fixation (Figs. 34-6 and 34-7).²⁵ It rigidly fixes the C1 and C2 facets, minimizing the need for postoperative external immobilization, which is desired in these patients with fragile skin. Careful preoperative assessment with a CT scan is necessary to define the vertebral artery anatomy adequately. It also ensures that the C2 isthmus is wide enough to accept at least a 3.5-mm screw and that the lateral mass of C1 is reduced and aligned with the superior facet of C2. Other considerations that may preclude the use of this technique include significant cranial settling with collapsed lateral masses, irreducible subluxations, substantial osteoporosis and osteopenia, comminuted fractures of the atlas and axis vertebrae, and an anomalous vertebral artery.

FIGURE 34–6 A and B, Transarticular screw technique for C1-2 arthrodesis.

FIGURE 34–7 A 52-year-old woman with long-standing rheumatoid arthritis has neck pain without evidence of frank myelopathy. A and B, Flexion and extension lateral cervical spine radiograph shows C1-2 instability. There is incomplete reduction in extension. C, Sagittal MRI shows pannus around dens. This is likely blocking complete reduction in extension. There is still enough space available for the spinal cord, however, as can be seen on this image. D and E, Lateral intraoperative fluoroscopic view of C1-2 (D) and postoperative lateral radiographic view (E) after transarticular screw placement and modified Gallie-type wiring with bone grafting for posterior C1-2 arthrodesis.

Patient positioning is the same as with the wire techniques described earlier, but the arm attachment from the tongs to the operating table should be radiolucent to aid visualization with intraoperative fluoroscopy. A longer incision may facilitate angling of the drill guide and screw placement. It is common to use percutaneous stab wounds around the level at the T2-6 spinous process to achieve the correct angle for screw placement. The starting point for drill placement is 3 mm above the C2-3 facet articulation and 2 to 3 mm lateral to the medial border of the C2 facet. The drill guide should be aimed 0 to 10 degrees medially and toward the dorsal cortex of the anterior arch of C1.

Palpation of the medial wall of the pedicle through a laminotomy between C1 and C2 should be considered. Biplanar fluoroscopic images should be obtained before inserting the starting Kirschner wire and during drilling to ensure that the wire hugs the superior cortex of the isthmus to avoid the vertebral artery inferiorly. The vertebral artery is inferior on lateral views and parallel or slightly lateral to the cord on anteroposterior views. The tip of the wire should end about 3 mm short of the anterior cortex of C1 to avoid passing the drill into the oropharynx. Current instrumentations are cannulated and make it easier to place screws. Usually a 3.5-mm or 4.5-mm cannulated screw measuring 40 to 44 mm is adequate. Ideally, wires are drilled on both sides before placing the screws bilaterally. A Gallie-type posterior fixation technique with autologous iliac crest bone graft is used to supplement the fixation. External immobilization devices should be prescribed based on the strength of the construct and bone quality. In many cases, a soft collar is all that is required.

Posterior C1-2 Intra-articular Screw Fixation

A variation is the use of a C1-2 intra-articular interference screw, as described by Tokuhashi and colleagues.⁹⁰ In this technique, posterior dissection exposes the C1-2 joints bilaterally. The joint capsule is dissected off the bone and retracted superiorly with the greater occipital nerve. When placing a screw on one side, atlantoaxial subluxation is reduced and maintained by application of a Halifax interlaminar clamp to the contralateral side. A 1-mm Kirschner wire is inserted directly into the C1-2 joint, and a cannulated tap is used to prepare the site for insertion of the cannulated 5.6-mm or 6.5-mm titanium interference screw. These screws are typically 8 mm or 10 mm long. The procedure is performed on the opposite side. Finally, corticocancellous bone graft is fashioned to fit the intralaminar space and is secured beneath bilateral Halifax clamps. Patients are placed in a cervical collar postoperatively.

In a more recent study, Tokuhashi and colleagues⁹¹ used this technique in 22 patients with rheumatoid arthritis. All patients reported significant improvement in pain, and all patients who were Ranawat class IIIA or above improved neurologically by 2-year follow-up. Atlantoaxial reduction was maintained, and bony fusion was noted in all patients, although four patients eventually had changes in alignment of the subaxial cervical spine (none of which required surgical intervention).

Posterior C1-2 Screw-Rod Constructs

Several methods of posterior C1-2 rigid instrumentation have been described more recently. Harms and Melcher²⁹ reported a technique involving placement of 3.5-mm polyaxial screws directly into the lateral mass of C1 and into the pars interarticularis or pedicle of C2 bilaterally (Fig. 34–8). Vertical rods are attached to these screws followed by bone grafting to obtain arthrodesis. This method allows for direct manipulation and reduction of C1 on C2 as needed. The advantages of this technique include the theoretical decreased risk to the vertebral artery compared with C1-2 transarticular screws. Bleeding from the venous lakes covering the C1 lateral masses can easily be encountered and is a disadvantage of this technique. This bleeding is usually minimized by meticulous subperiosteal dissection and can typically be controlled by absorbable gelatin sponge (Gelfoam). Either technique requires an intimate knowledge of the anatomy by the operating surgeon aided by good fluoroscopic technique.

FIGURE 34–8 A and B, Posterior C1-2 fixation technique with polyaxial screws and rods. Screws are placed into the lateral masses of C1 and into the pedicles of C2.

For posterior C1-2 screw-rod constructs, first the C1-2 joint is identified because this serves as the anatomic landmark for accurate placement of the C1 lateral mass screw. Removing a small amount of the caudal part of the C1 posterior arch with a bur aids in visualizing the C1 screw starting point. The C2 nerve root can be gently retracted caudally for visualization. The screw is placed in the center of the lateral mass, first using a high-speed bur to create a dimple so that the drill bit does not skid while drilling. The pilot hole is drilled straight or slightly convergent and parallel to the C1 posterior arch in the sagittal direction. The drill hole is typically 18 to 22 mm, which should be confirmed with fluoroscopy. A longer screw than this is needed because the polyaxial screw head needs to be elevated off of the cortex of the lateral mass to accommodate rod fixation.

The entry point for the C2 pedicle screw is in the upper and medial quadrants of the isthmus surface. The direction of the pilot hole is approximately 20 to 30 degrees in a convergent and cephalad direction. The medial border of the C2 pars interarticularis can initially be palpated with a small elevator to help with accurate placement of C2 screws. A typical length for C2 pedicle screws would be 22 to 28 mm, which would again be confirmed with fluoroscopy. In their study, Harms and Melcher²⁹ did not wire in grafts for their fusion technique; however, this is an option to augment the stability of the screw-rod construct and to help insure a successful arthrodesis (see Fig. 34–7).

An alternative to the C2 pedicle or pars screw is placement of an intralaminar C2 screw (Fig. 34–9). As described by Wright,⁸⁸ this technique provides excellent fixation of C2 with virtually no risk of injury to neurovascular structures. Exposure is as described earlier for the placement of C1 lateral mass and C2 pedicle screws. Placement of the C1 lateral mass screws is done by the previously described technique. For placement of the C2 intralaminar screws, a high-speed bur is used to open a small cortical window at the cranial end of the junction of the C2 spinous process and lamina. A hand drill is used to drill the intercortical space of the contralateral lamina to a depth of approximately 30 mm, while maintaining alignment of the drill with the exposed dorsal aspect of the lamina.

FIGURE 34–9 A and B, Posterior C1-2 fixation with placement of C1 lateral mass screws and C2 intralaminar screws. A, Axial CT scan through C1 showing location of lateral mass screws. B, Axial CT scan through C2 lamina showing bilateral intralaminar screws. Because of the technique required for insertion, the screws are not in exactly the same axial plane.

After palpation of the drill tract with a ball tip probe, a 4 × 30 mm polyaxial screw is inserted. A starting hole is drilled in the contralateral side at the caudal junction of the spinous process and lamina, and using the same technique, an intralaminar screw is inserted. Care must be taken when inserting the screws to maintain the angle of insertion slightly more shallow than the angle of the lamina, to ensure that any cortical breach occurs dorsally, rather than ventrally into the spinal canal. The polyaxial screw heads from C1 and C2 are connected with a rod. In some instances, because of the angle of the screws relative to one another, offset connectors may need to be used to facilitate rod insertion. The laminae of C1 and C2 may be decorticated, and corticocancellous bone graft may be applied (and wired into place if desired).

A more recent biomechanical study examined the relative stability of several C1-2 screw-rod constructs in an odontoid fracture model.⁹² Using cadaveric specimens, C1 lateral mass screws were placed and connected to C2 intralaminar screws, C2 pars screws, or C2 pedicle screws. Insertional torque for C2 pedicle screws and intralaminar screws was similar, and both of these were significantly higher than pars screws. Pullout strength was greatest for pedicle screws. In intact models, intralaminar screws provided superior resistance to axial rotation compared with pars screws and similar resistance to pedicle screws. After experimentally induced odontoid fracture, pars and pedicle screws were superior in resisting lateral bending. Although similar to the intralaminar technique, pedicle screws overall provided the greatest stability of C1-2 in all planes, particularly after experimental odontoid fracture. Lapiswala and colleagues⁹³ noted similar results with C2 intralaminar screws providing less resistance to lateral bending than either C2 pedicle screws or C2-C1 transarticular screws. In their study, all posterior constructs, when supplemented with posterior cable fixation, provided similar stiffness in flexion-extension and axial rotation.

Occipitocervical Fusion

The technique of choice to treat patients with cranial settling or fixed atlantoaxial subluxations causing posterior cord impingement from the ring of C1 is occipitocervical fusion.^52,80,94 In the latter case, an occiput-to-C2 fusion with a C1 laminectomy is preferred. Patient positioning is the same as with the wire techniques described earlier. The base of the occiput from the external occipital protuberance is exposed with caudad extension to the level of the subaxial spine to be fused.

Wiring and Graft Technique

The wiring and graft technique uses corticocancellous bone blocks wired to the occiput and laminae (Fig. 34–10).^52,80,94 The prominent bony protuberance (inion) that is present approximately 2 cm below the external occipital protuberance is the site of wire fixation (approximately 5 to 7 cm from the base of the skull). A 2-mm diamond bur is used to make unicortical holes to form a tunnel with a bridge of superficial cortical bone on each side of the midline. The holes are connected with a towel clamp between the inner and outer tables of the skull. A 20-gauge wire is passed through the tunnel and looped back under and out again to wrap around the bony bridge. A second wire is passed beneath the C1 lamina (if it has not been removed) and looped onto itself to cinch down on the lamina. A wire is passed transversely through the base of the C2 spinous process and looped around and passed back through to distribute stress. Other interspinous or sublaminar wires can be used in more caudad segments as needed. Long, thick corticocancellous iliac crest grafts are harvested, typically 9 to 10 cm in length and 1.5 cm wide.

FIGURE 34–10 Technique of posterior occipitocervical fusion. A, Bur hole is made in nuchal bony ridge, staying between cortical table. B, 20-gauge wires are passed down; looping the wire through a second time improves the grip and distributes the stress. C, Near full–thickness corticocancellous grafts are harvested from ilium. D, Grafts are wired in place as shown. Cancellous bone is also packed in crevices.

(Modified from Werthein SB, Bohlman HH: Occipitocervical fusion: Indications, technique, and long-term results in thirteen patients. J Bone Joint Surg Am 69:833-836, 1987.)

For occiput-to-C2 fusions, a single block of graft may be used with the caudad end fashioned to fit around the C2 spinous process. A 1.5-mm drill bit is used to place holes through the graft. The wires are threaded through the graft with the cancellous side facing the exposed skull and laminae. The concavity of the central part of the iliac crest facilitates excellent contact between the occiput and the laminae. In severely osteopenic patients, a wire mesh may be placed over the cortical side of the graft to prevent the wires from cutting through the graft.⁵² The wires are tightened down cautiously to prevent breakage or cutting through the graft. Cancellous bone chips may be added to the construct. A drain is typically used, and the wound is closed in layers. Without adjuvant fixation, most patients are managed in a halo vest postoperatively, but a two-poster brace or other cervical orthosis may be used based on the stability of the construct.

Occipitocervical Plating

Occipitocervical plating provides more rigid fixation compared with wiring techniques,^34,36,95,96 even in patients with significant osteoporosis. Early instrumentation consisted of acetabular reconstruction plates,³⁶ but current improvements are more versatile and incorporate plate-rod hybrid constructs (Fig. 34–11). It may be technically challenging to produce the correct amount of contour required at the base of the skull. In longer fusions, it is recommended that fixation is achieved in C2 and in the lower vertebrae before fixation into the skull because the more distal fixation points require more precise anatomic locations. C2 fixation can be done with pedicle screws, transarticular screws, or intralaminar screws (described earlier). Because of their inferior pullout strength, C2 pars screws should not be used unless the fusion is to be carried down into the subaxial cervical spine.

FIGURE 34–11 A 46-year-old woman had a long history of rheumatoid arthritis diagnosed when she was a young girl. She has had chronic neck pain but developed worsening neck pain over the past 6 weeks with increasing numbness of her arms and some truncal numbness. Some weakness of the upper extremities was evident on physical examination. A and B, MRI shows severe cord compression primarily at C2-3 level. She has multiple levels of subluxation in subaxial spine including C7-T1. C and D, Anteroposterior and lateral postoperative plain films after posterior decompression at C2-3 followed by long occipitocervical fusion with bone grafting and posterior instrumentation. Screws were placed in pedicles of C7 and T1 for maximum fixation and osteoporotic bone.

Fixation to the skull requires knowledge of the venous sinus anatomy to avoid bleeding complications. Screws should be placed distal to the transverse sinus, which lies at the level of the external occipital protuberance. The thickness of the skull decreases laterally away from the midline and closer to the foramen magnum.⁹⁷ Unicortical fixation is adequate in the thicker areas of the skull, but bicortical fixation can be performed safely. Two to three screws should be used on each side of the midline. A 2-mm diamond bur is used to minimize the chance of a spinal fluid leak, which is common when using more aggressive carbide burs. The holes are tapped, and 3.5- to 4.5-mm screws 6 to 12 mm in length are placed. In case of a spinal fluid leak, bone wax may be sufficient to stop the leak; otherwise, placing the screw usually tamponades the leak. There does not seem to be any adverse effect from breaching the inner table. The head and neck are immobilized in a two-poster brace or a halo vest in patients with osteoporotic bone and questionable fixation. Patients are typically changed to a soft collar for comfort after 8 weeks.

Contoured Loop and Rod Technique

The contoured loop and rod technique was first proposed by Ransford and colleagues in 1986³² and is used with segmental wiring to provide occipitocervical fixation.^32,98–100 The exposure is similar to that described earlier for plate fixation. Wires are placed in the occiput and beneath the lamina of C1 and the subaxial vertebrae. Earlier constructs relied on a horseshoe-shaped loop of threaded stainless steel rods. The horizontal limb should be approximately 3.5 to 4 cm wide, and the length of the occipital portion of the loop should be 2.5 to 3 cm. More recent constructs use a custom-contoured threaded titanium loop with titanium-threaded cables, which allows for postoperative MRI.

Resection of the Odontoid

Mild to moderate cervicomedullary compression can be treated with posterior C1 laminectomy and occipitocervical fusion as described earlier. The pannus resorbs with stabilization.⁴⁰ Anterior decompression may be needed, however, to treat an irreducible anterior extradural compression of the cervicomedullary junction by pannus or a severely migrated odontoid.^101,102 The transoral approach is associated with an increased risk of infection with mouth flora; the high retropharyngeal approach is a good alternative in many patients.¹⁰³ Supplemental posterior fusion is required unless there is a solid prior posterior fusion mass. In case of a prior posterior fusion, resection of the odontoid without grafting suffices. In cases without prior posterior fusion, anterior strut grafting with iliac crest or fibula is required between C2 or C3 and the clivus, followed by posterior occipitocervical fusion. Posterior stabilization may be staged depending on the medical status of the patient. Thorough preoperative assessment is necessary and includes swallowing and respiratory function considerations, dental assessment, and the presence of a mobile temporomandibular joint to allow about 2.5 to 3 cm of opening.

Subaxial Fusion

Subaxial subluxations may be fixed or mobile. The fixed types may be best treated with anterior decompression and fusion. Strong consideration should be given to supplemental posterior fixation because anterior column instability may occur from graft resorption or settling into the osteoporotic vertebral bodies. Mobile subluxations are best treated with traction to realign the spine and posterior instrumented fusion. As noted earlier, a better reduction may be obtained when positioning of the head is done gently with the patient under anesthesia.

Wiring Techniques

Posterior wiring and autogenous bone grafting may provide stable fixation at a high fusion rate. The authors use the triple wire technique described by McAfee and Bohlman (Fig. 34–12).¹⁰³ The first 20-gauge wire is woven in a figure-of-eight fashion through holes drilled into the base of the spinous processes of the involved vertebrae. This is the midline tethering wire. The wire is typically looped onto itself after passing through the spinous process to help distribute stress; 22-gauge wires can then pass individually through the same holes to loop around the spinous processes at the ends of the segments to be fused. The ends of these wires pass through drill holes in the rectangular corticocancellous iliac crest autografts. The wires are tightened down on the graft to force the graft against the laminae. Decortication is unnecessary. The wound is closed in layers over a drain. A two-poster cervical brace is used for 6 to 8 weeks to allow solid fusion.

FIGURE 34–12 A-C, Bohlman triple-wire technique for posterior cervical arthrodesis.

Lateral Mass Plating and Screw and Rod Constructs

Lateral mass plating and screw and rod constructs typically provide excellent fixation of the subaxial spine. Several modifications exist in the way the screws are angled in the lateral mass.^25–28 According to An and colleagues,²⁶ 15 degrees of superior angulation and 30 degrees of lateral angulation best avoids violating the facet joints and the nerve roots. All the techniques avoid the vertebral artery, which lies anterior to the lateral mass. The starting point is 1 mm medial to the center of the lateral mass. Current instrumentations come with standard drill kits. The screws average 14 to 18 mm, depending on the size of the patient. The C7 lateral mass is thin and may require pedicle screw placement or supplemental posterior wiring between the C6 and C7 spinous processes as described earlier. Fluoroscopy is helpful in placing C7 pedicle screws if the shoulders are not in the way, but a C7 laminotomy provides direct palpation of the medial wall of the pedicle for safer screw placement. A 25- to 30-degree medial angulation is recommended.²⁶ Pedicle screw fixation of all involved levels of the cervical vertebrae has been described frequently in other patient populations but has limitations of pedicle size and risks to the vertebral artery.¹⁰⁴

Thoracolumbar Disease

In contrast to the cervical spine, rheumatoid disease of the thoracic and lumbar spine leads to severe neurologic symptoms less frequently and has received less attention. Cases of thoracic myelopathy, lumbar radiculopathy, and cauda equina syndrome have been reported, however, and seem to be due to bony destruction leading to instability and subluxation with or without the presence of pannus or nodules.^107–109 Radiographic findings include poorly defined margins of the vertebral endplates and a relative lack of osteophytes.^110,111 Involvement of the facet joints may lead to spondylolisthesis and instability on flexion-extension films. Heywood and Meyers¹¹⁰ postulated that the pathologic process in the lumbar spine begins with synovitis of the facet joints causing functional incompetence, allowing anteroposterior and lateral translation. This synovitis is followed by discitis, which may start as an enthesopathy at the junction of the endplate and disc, resulting in loss of disc height and contributing further to instability. In the thoracic spine, the disease may also spread directly into the spine via the costovertebral joints. Nerve root impingement may be due to spinal instability and direct impingement from rheumatoid pannus.¹¹⁰

To correlate radiographic findings with clinical symptoms, Kawaguchi and colleagues¹¹¹ studied 106 patients with rheumatoid arthritis and found that 40% of patients complained of back pain, 18% had leg pain and 12% exhibited symptoms of neurogenic claudication. They reported abnormal radiographic findings in 57% of patients, with disc space narrowing the most frequent finding, in 37% of patients; coronal plane deformity in 28%; spondylolisthesis in 23%; and endplate or facet erosion in 20%. Finally, Kawaguchi and colleagues¹¹¹ noted a high percentage of osteoporosis, particularly in patients on steroid therapy. Using MRI, Sakai and colleagues¹¹² reported a 45.2% incidence of lumbar involvement in rheumatoid arthritis and described two distinct patterns of disc destruction: narrowing, in which the disc space progressively collapsed, and ballooning, in which changes in the endplates give the illusion of increasing disc height. Additionally, they found that the degree of lumbar involvement related to the severity of peripheral joint involvement.

The literature regarding surgical treatment of lumbar involvement is sparse. One more recent study retrospectively compared outcomes of 19 patients with rheumatoid arthritis who underwent posterior lumbar decompression and fusion with a matched control group of patients without rheumatoid arthritis.¹¹³ Given the small number of patients in the study, there were no significant differences in complications, fusion, or patient satisfaction between the two groups. Two patients with rheumatoid arthritis showed evidence of loosening of pedicle screws on postoperative radiographs, however, and one patient underwent noninstrumented fusion owing to severe osteoporosis noted intraoperatively. None of the control patients had any hardware complications. In addition, there was a trend toward more wound complications in the rheumatoid arthritis group.

Summary

Most patients with rheumatoid arthritis of the cervical spine can be managed nonoperatively. These patients should be monitored closely, however, because the progression of disease may be silent, and the clinical findings are nonspecific. Screening flexion and extension lateral radiographs should be obtained periodically before neurologic symptoms develop and before any planned surgical procedure that may require general anesthesia, intubation, or manipulation of the cervical spine. The benefits of early detection and surgical intervention in patients with progressive cervical instability cannot be overemphasized, and the current trend is to perform prophylactic fusion before the development of cranial settling or frank neurologic symptoms.^39,51,80 Otherwise, mortality and morbidity significantly increase as patients become less functional and develop Ranawat class III criteria.^{51,58,65,79,103} Although surgery in patients with quadriparesis may provide some neurologic and functional recovery, the results are not as predictable as with early surgery.