Rheumatoid arthritis as a risk factor for a narrow C-2 pedicle: 3D analysis of the C-2 pedicle screw trajectory

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1 J Neurosurg Spine 9:17 21, 2008 Rheumatoid arthritis as a risk factor for a narrow C-2 pedicle: 3D analysis of the C-2 pedicle screw trajectory MASAHIKO MIYATA, M.D., MASASHI NEO, M.D., PH.D., HIROMU ITO, M.D., PH.D., MAKOTO YOSHIDA, M.D., SHUNSUKE FUJIBAYASHI, M.D., PH.D., AND TAKASHI NAKAMURA, M.D., PH.D. Department of Orthopaedic Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan Object. Vertebral artery (VA) injury is a potentially serious complication of C-2 pedicle screw (PS) fixation. Although this surgery is frequently performed in patients with rheumatoid arthritis (RA), few studies have compared the risk of VA injury in patients with and without RA. In this study, the authors compare the morphological risk of VA injury relating to C-2 PS fixation in patients with and without RA. Methods. A total of 110 3D CT images of the cervical spine including the axis were evaluated. Fifty patients with RA and 60 patients without RA were included in the study. The maximum PS diameter (MPSD) that could be used at C-2 without breaching the cortex was measured in 3D using a computer-assisted navigation system. A narrowpedicle carrier was defined as a patient with an MPSD of 4 mm or less. Results. In the RA group, 42 of 100 MPSDs were 4 mm, and 30 of 50 patients (60%) were narrow-pedicle carriers. In the non-ra group, 10 of 120 MPSDs (8%) were 4 mm, and 8 of 60 (13%) patients were narrow-pedicle carriers. The MPSD, the anteroposterior (AP) diameter of C-3, and the ratio of MPSD to the AP diameter of C-3 were significantly smaller in the RA group than in the non-ra group. Multiple logistic regression analysis showed that RA and narrow C-3 AP diameter were significant risk factors for a narrow-pedicle carrier. Conclusions. Rheumatoid arthritis is a significant risk factor for a narrow C-2 pedicle. When performing PS placement at C-2, particularly in patients with RA, thorough preoperative evaluation of the bone architecture is very important for avoiding inadvertent injury to the VA. (DOI: /SPI/2008/9/7/017) KEY WORDS axis pedicle screw rheumatoid arthritis vertebral artery injury P EDICLE screw fixation at C-2, first described by Leconte 21 for the treatment of traumatic spondylolisthesis of the axis, is a widely accepted technique that is often performed in atlantoaxial fixation, occipitocervical fixation, or multiple segmental fixation. This procedure has been extended recently to treat cervical lesions such as traumatic injury, cervical or occipitocervical instability, degenerative spondylosis, kyphotic deformity, RA, and destructive spondyloarthropathy 1 3,8,9,16,20 because of its high biomechanical strength. 17 Posterior atlantoaxial fixation using lateral mass screws at C-1 in combination with PSs at C-2 has become popular recently, 15,16 and this technique provides comparable stability to transarticular screw fixation. 19 However, several complications have been associated with this procedure, including screw penetration into the Abbreviations used in this paper: AP = anteroposterior; CI = confidence interval; MPSD = maximum pedicle screw diameter; OR = odds ratio; PS = pedicle screw; RA = rheumatoid arthritis; VA = vertebral artery; VB = vertebral body. spinal canal and VA injury. Previous studies of anterior cervical decompression or atlantoaxial transarticular fixation show that VA injury may cause massive bleeding, cerebellar or brainstem infarction, and, at worst, death. 5,11,12, 22,24,29,30 If one VA is aplastic or hypoplastic, injury to the contralateral dominant VA may have lethal consequences. Therefore, thorough anatomical knowledge, deliberate preoperative planning, and a refined operative technique are necessary when screw placement is intended around the VA. 25,26 The VA is divided anatomically into 4 segments: the V1 segment originates from the subclavian artery and extends to the C-6 transverse process, and the V2 segment extends from the C-6 to C-2 transverse processes. 6 Although several anatomical variations of the V2 segment have been reported, the VA usually enters the C-6 transverse foramen. 10 In the middle and lower cervical spine, it is relatively easy to evaluate the relationship between the VA and the pedicle on conventional, 2D reconstruction CT images, because the V1 segment is outside the C-7 vertebra, and the V2 segment usually runs vertically from C-6 to C However, the VA bends sharply within the substance of the axis, and 17

2 M. Miyata et al. this loop can limit the space available for placement of PSs at C-2. The VA loop is sharp in ~ 80% of individuals. 14 Unlike in the middle and lower cervical spine, the anatomical relationship between the axis and the VA is complicated. Therefore, a 3D approach is necessary for evaluating the C- 2 pedicle. Pedicle screw fixation at C-2 is frequently performed in patients with RA. The cervical spine is a commonly affected portion of the spinal column because of the large number of synovial joints. 28 Rheumatoid involvement of the cervical spine generally begins early in the disease process and progresses in parallel with peripheral involvement. Specific patterns of rheumatoid cervical involvement include atlantoaxial subluxation, superior migration of the odontoid, and subaxial subluxation. Without surgical intervention, patients with RA and myelopathy tend to have a high mortality rate. 23 Therefore, surgical treatment, including spinal fixation, should be considered for the rheumatoid cervical spine despite the difficulty of screw insertion. In this study, we evaluate the morphological risk of VA injury relating to C-2 PS fixation with a 3D approach, and compare the risk in patients with and without RA. Methods A total of 110 3D CT images of the cervical spine, including the axis, were evaluated. The population consisted of 39 men and 71 women, and the mean age was 61.5 years (range years). The patients were grouped according to whether they had RA. There were 50 patients in the RA group, of which 7 were men and 43 were women, with a mean age of years (range years). Of the 60 patients in the non-ra group, 32 were men and 28 were women, with a mean age of years (range years). The proportion of men and women differed significantly between the 2 groups (p 0.001, Fisher exact test), but the age of the patients did not (p = , Mann Whitney U-test). All patients with RA included in this study fulfilled the revised criteria of the American College of Rheumatology. 7 All patients with RA had Stage 2 or greater RA (Steinbrocker classification). Thirteen patients underwent cervical spine surgeries including occipitocervical fusion in 10 patients, atlantoaxial transarticular screw fixation in 2, and other surgery in 1 patient. All patients in the non-ra group had cervical spine diseases and underwent conservative or operative treatment. The original diagnosis was cervical degenerative disease in 50 patients, bone metastases not involving the upper cervical spine in 6, whiplash injury in 2, and other conditions in 2. Patients with fractures, infections, congenital anomalies, or previous cervical surgery were excluded from the study. Twenty-six patients underwent cervical spine surgeries including cervical laminoplasty (18 patients), anterior cervical fusion (3), posterior cervical fusion (2), and other surgeries (3). Computed Tomography Studies All patients underwent CT scanning using a multidetector CT. All images were reconstructed with a slice thickness of 1 mm and reconstruction interval of 1 mm. The trajectories of the C-2 PSs were evaluated using 3D images reconstructed by a computer-assisted navigation system (StealthStation TRIA plus, Medtronic, Inc.). The C-2 pedicle was defined as the portion beneath the superior facet and anteromedial to the transverse foramen. 13 The screw trajectory was set to insert from the posterior aspect of the inferior articular process through the isthmus and pedicle into the VB without penetrating the superior articular facet. The MPSD that could be inserted through the pedicle of the axis without breaching the cortex was measured to the nearest mm (Fig. 1). 33 We defined a narrow pedicle as having an MPSD of 4 mm, considering the fact that cervical PSs mm in diameter are generally available. A narrow-pedicle carrier was a patient with an MPSD of 4 mm or less. The AP diameter of the C-3 VB was measured to the nearest mm and used as an index of spinal body size. The AP diameter of C-3 was defined as the distance between the sagittal and axial midpoints of the anterior and posterior walls of the VB. The screw/vertebra ratio was defined as MPSD divided by the AP diameter of C-3. Statistical Analysis We compared parametric variables (MPSD, C-3 AP diameter, and screw/vertebra ratio) using the unpaired Student t-test, and nonparametric variables using the Mann- Whitney U-test. Frequency analysis was performed with the chi-square test and the Fisher exact test. Univariate logistic regression analysis was performed. The dependent variable was whether the patient was a narrow-pedicle carrier or not, and the independent variable was whether the patient had RA or not. Age, sex, and the AP diameter of C-3 were added as independent variables for multiple logistic regression analysis. Statistical significance was established at p 0.05, and analyses were performed using open-source R statistical software (www. r-project.org, GNU Project, Free Software Foundation). Results In the RA group, the mean MPSD was 4.7 mm (range 1 7 mm) and 42 of 100 MPSDs were 4 mm. The mean AP diameter of C-3 was 16.3 mm (range mm) and the mean screw/vertebra ratio was In the non-ra group, the mean MPSD was 6.4 mm (range 2 9 mm) and 10 of 120 MPSDs (8%) were 4 mm. The mean AP diameter of C-3 was 17.2 mm (range mm) and the mean screw/vertebra ratio was The incidence of MPSDs 4 mm differed significantly between the 2 groups (p 0.001). The MPSD, AP diameter of C-3, and screw/vertebra ratio were significantly smaller in the RA group than in the non-ra group (Table 1). These results indicate that narrow C-2 pedicles are common in RA patients even after VB size is taken into consideration. When men and women were analyzed separately, the MPSD and screw/vertebra ratio were significantly smaller in the RA group than in the non-ra group. In the non-ra group, the MPSD was significantly larger in men than in women, and the screw/vertebra ratio did not differ significantly. In contrast, in the RA group, MPSDs tended to be smaller in men, and the screw/vertebra ratio was significantly smaller in men than in women (Table 1). These results indicate that the sex difference in pedicle size is relat- 18

Rheumatoid arthritis as a risk factor for a narrow C-2 pedicle FIG. 1. Images demonstrating trajectory planning for a C-2 PS in a 75-year-old woman with RA.

3 Rheumatoid arthritis as a risk factor for a narrow C-2 pedicle FIG. 1. Images demonstrating trajectory planning for a C-2 PS in a 75-year-old woman with RA. The maximum screw diameter that could be inserted through the pedicle of the axis without breaching the cortex was measured to the nearest millimeter. ed to the body size in the non-ra group; in the RA group, however, the C-2 pedicle in men is small compared to the body size. The frequency distributions of narrow pedicles in each group are shown in Table 1. The frequency of narrow-pedicle carriers was significantly higher in the RA group than in the non-ra group (p 0.001). The incidence of narrowpedicle carriers was 60% in the RA group and 13% in the non-ra group. There was a significant difference between the 2 groups in the incidence of narrow-pedicle carriers. (p 0.001) Univariate logistic regression analysis indicated that RA was a significant risk factor for being a narrow-pedicle carrier (crude OR 9.75, 95% CI , p 0.001). Even after adjusting for age, sex, and the AP diameter of C-3, the presence of RA remained significant (adjusted OR 10.0, 95% CI , p 0.001). The AP diameter of C-3 was also a significant risk factor (adjusted OR 0.601, 95% CI , p = ; Table 2). Discussion The course of the VA in the axis is quite unique and variable. The VA makes a sharp lateral turn just below the superior articular facet of the axis in about 80% of individuals. 14 When performing PS fixation at C-2, a small difference in the location of the VA loop may make a great difference in the amount of space available for screw insertion through the pedicle of the axis. In view of the intricate anatomical relationship between the axis and the VA unlike in PSs in the middle and lower cervical spine it is difficult to design an ideal C-2 PS trajectory and measure MPSD using conventional reconstructed CT images. We consider that a 3D approach is essential for evaluating the anatomical relationship between the course of the VA and the intended screw trajectory. Accurate evaluation of the intended screw trajectory can be accomplished using a computer-assisted navigation system. 33 Although C-2 PS fixation is frequently performed in 19

4 M. Miyata et al. TABLE 1 Summary of data obtained in RA and non-ra groups* Group RA (50 Non-RA Parameter Patients) (60 Patients) p Value MPSD (mm) men women C-3 AP diameter (mm) screw/vertebra ratio men women no. w/ narrow pedicles bilat 12 2 unilat 18 6 none * All measurement data are expressed as means standard deviations. Statistical significance is assessed with the Student t-test unless otherwise noted. Mann Whitney U-test. patients with RA, few studies have compared the risks of VA injury related to the morphological characteristics of patients with and without RA. In this study, the screw/vertebra ratio and MPSD were found to be significantly smaller in the RA group than in the non-ra group. Multiple logistic regression analysis demonstrated that both VB size and the presence of RA were significant risk factors for a narrow C-2 pedicle. The high frequency of narrow C-2 pedicles in RA patients may be caused by gradual changes of the VA groove in the axis resulting from softening of bone or destruction of the facet joint. 4 In their cadaveric CT study, Karaikovic and colleagues 18 reported that the mean outer pedicle widths of the axis in male and female cadavers were 6.9 and 6.5 mm, respectively. In our patients, the pedicle widths in the non-ra group were smaller than those reported by Karaikovic et al., and may relate to ethnic differences in body size. Xu et al. 32 showed that the C-2 pedicle is significantly larger in men than in women, which is consistent with our observations in the non-ra group. However, in our RA group, narrow C-2 pedicles were more frequently observed in men than in women, although the number of men with RA was small. In a radiographic study in 194 patients with RA, Weissman et al. 31 noted that men have a greater risk of advanced upper cervical involvement, which may explain our results. Our results strongly suggest that closer attention should be paid to the bone architecture of the axis in patients with RA. In C-2 PS placement, the course of the VA through the axis can limit the space available for placement of the screw through the pedicle of the axis. It should be kept in mind that C-2 PS placement in patients with RA entails more risk than in patients without RA. 18 Preoperative evaluation of the screw trajectory is important for avoiding inadvertent VA injury. The computer-assisted navigation system was very helpful in surgical planning. Conclusions In this study we demonstrated that RA is a significant TABLE 2 Summary of multiple logistic regression analysis of risk factors for having a narrow pedicle* Variable OR 95% CI p Value RA* sex (female) age (per additional yr) C-3 AP diameter (per 1-mm increase) * For this analysis, RA = 1 and non-ra = 0; female = 1 and male = 0. Indicates statistical significance. risk factor for a narrow C-2 pedicle. When performing C-2 PS fixation, particularly in patients with RA, thorough preoperative evaluation of the bony structures of the axis is important for avoiding inadvertent VA injury. Three-dimensional assessment with a computer-assisted navigation system is useful for comprehension of the bone architecture and surgical planning. Disclaimer No benefits in any form have been, or will be, received from a commercial party related directly or indirectly to the subject of this manuscript. References 1. Abumi K, Ito M, Kaneda K: Surgical treatment of cervical destructive spondyloarthropathy (DSA). Spine 25: , Abumi K, Shono Y, Taneichi H, Ito M, Kaneda K: Correction of cervical kyphosis using pedicle screw fixation systems. Spine 24: , Abumi K, Takada T, Shono Y, Kaneda K, Fujiya M: Posterior occipitocervical reconstruction using cervical pedicle screws and plate-rod systems. Spine 24: , Apfelbaum RI: Atlantoaxial screw fixation. J Neurosurg Spine 3: 510, 2005 (Author reply) 5. 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5 Rheumatoid arthritis as a risk factor for a narrow C-2 pedicle 13. Ebraheim NA, Fow J, Xu R, Yeasting RA: The location of the pedicle and pars interarticularis in the axis. Spine 26:E34 E37, Goel A, Gupta S: Vertebral artery injury with transarticular screws. J Neurosurg 90: , Goel A, Laheri V: Plate and screw fixation for atlanto-axial subluxation. Acta Neurochir (Wien) 129:47 53, Harms J, Melcher RP: Posterior C1 C2 fusion with polyaxial screw and rod fixation. Spine 26: , Jones EL, Heller JG, Silcox DH, Hutton WC: Cervical pedicle screws versus lateral mass screws. Anatomic feasibility and biomechanical comparison. Spine 22: , Karaikovic EE, Daubs MD, Madsen RW, Gaines RW Jr: Morphologic characteristics of human cervical pedicles. Spine 22: , Kuroki H, Rengachary SS, Goel VK, Holekamp SA, Pitkänen V, Ebraheim NA: Biomechanical comparison of two stabilization techniques of the atlantoaxial joints: transarticular screw fixation versus screw and rod fixation. Neurosurgery 56: , Kwon BK, Vaccaro AR, Grauer JN, Beiner JM: The use of rigid internal fixation in the surgical management of cervical spondylosis. Neurosurgery 60 (1 Suppl):S118 S129, Leconte P: Fracture et luxation des deux premieres vertebres cervicales, in Judet R (ed): Luxation Congénénitale de la Hanche. Fractures du Cou-de-pied Rachis Cervical. Actualités de Chirurgie Orthopédique de l Hopital Raymond-Poincaré. Paris: Masson et Cie, Vol 3, 1964, pp Madawi AA, Casey AT, Solanki GA, Tuite G, Veres R, Crockard HA: Radiological and anatomical evaluation of the atlantoaxial transarticular screw fixation technique. J Neurosurg 86: , Matsunaga S, Sakou T, Onishi T, Hayashi K, Taketomi E, Sunahara N, et al: Prognosis of patients with upper cervical lesions caused by rheumatoid arthritis: comparison of occipitocervical fusion between C1 laminectomy and nonsurgical management. Spine 28: , Neo M, Fujibayashi S, Miyata M, Takemoto M, Nakamura T: Vertebral artery injury during cervical spine surgery: a survey of more than 5600 operations. Spine 33: , Neo M, Matsushita M, Iwashita Y, Yasuda T, Sakamoto T, Nakamura T: Atlantoaxial transarticular screw fixation for a high-riding vertebral artery. Spine 28: , Neo M, Sakamoto T, Fujibayashi S, Nakamura T: A safe screw trajectory for atlantoaxial transarticular fixation achieved using an aiming device. Spine 30:E236 E242, Sakamoto T, Neo M, Nakamura T: Transpedicular screw placement evaluated by axial computed tomography of the cervical pedicle. Spine 29: , Shen FH, Samartzis D, Jenis LG, An HS: Rheumatoid arthritis: evaluation and surgical management of the cervical spine. Spine J 4: , Smith MD, Emery SE, Dudley A, Murray KJ, Leventhal M: Vertebral artery injury during anterior decompression of the cervical spine. A retrospective review of ten patients. J Bone Joint Surg Br 75: , Weidner A, Wahler M, Chiu ST, Ullrich CG: Modification of C1 C2 transarticular screw fixation by image-guided surgery. Spine 25: , Weissman BN, Aliabadi P, Weinfeld MS, Thomas WH, Sosman JL: Prognostic features of atlantoaxial subluxation in rheumatoid arthritis patients. Radiology 144: , Xu R, Nadaud MC, Ebraheim NA, Yeasting RA: Morphology of the second cervical vertebra and the posterior projection of the C2 pedicle axis. Spine 20: , Yoshida M, Neo M, Fujibayashi S, Nakamura T: Comparison of the anatomical risk for vertebral artery injury associated with the C2-pedicle screw and atlantoaxial transarticular screw. Spine 31: E513 E517, 2006 Manuscript submitted November 22, Accepted March 28, Address correspondence to: Masahiko Miyata, M.D., Department of Orthopaedic Surgery, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto , Japan. miyatch@kuhp.kyoto-u.ac.jp. 21

Morphometric Anatomy of the Atlas and Axis Vertebrae

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