Postoperative Cervical Sagittal Realignment Improves Patient-Reported Outcomes in Chronic Atlantoaxial Anterior Dislocation

Postoperative Cervical Sagittal Realignment Improves Patient-Reported Outcomes in Chronic... Abstract BACKGROUND Chronic atlantoaxial anterior dislocation (AAD) not only results in myelopathy, but dislocation-related kyphosis also results in cervical malalignment, which permanently affects neck function and patient-reported outcomes (PROs). OBJECTIVE To investigate the effect of kyphotic correction on realigning cervical spine and independent cervical alignment parameters, which may be correlated with an improvement of PROs. METHODS The study included 21 patients with chronic AAD-related kyphosis who underwent C1-2 reduction and correction surgery. Radiographic parameters were measured to assess cervical realignment preoperatively and postoperatively. Neck disability index (NDI), short form 12 physical component summary (SF-12 PCS), and Japanese Orthopaedic Association (JOA) scores were recorded to reveal changes in PROs. The independent parameters correlated with the improvements of PROs were analyzed. RESULTS Of the radiographic parameters, the C1-2 Cobb angle, the C2-7 Cobb angle, thoracic inlet angle, cervical tilt, and T1 slope were significantly changed from −4.0° ± 16.2°, −29.2° ± 11.2°, 73.1° ± 13.3°, 30.4° ± 8.5°, and 29.1° ± 8.8° preoperatively to −13.5° ± 8.1° (P = .005), −18.0° ± 12.0° (P < .001), 67.1° ± 11.6° (P = .042), 23.1° ± 10.3° (P = .007), and 24.0° ± 7.0° (P = .011) at last follow-up, respectively. NDI, JOA, and SF-12 PCS scores were significantly improved postoperatively. The C1-2 Cobb angle was an independent parameter correlated with the improvements in SF-12 PCS, NDI, and JOA scores. CONCLUSION Correction and reduction surgery can realign cervical spine in chronic AAD patients. The C1-2 Cobb angle was an independent parameter correlated with the improvements of PROs. Cervical spine alignment, Atlantoaxial anterior dislocation, Reduction, Kyphosis correction, Patient-reported outcomes ABBREVIATIONS ABBREVIATIONS AAD atlantoaxial anterior dislocation CG-C7 SVA center of gravity to C7 SVA CI confidence interval CMA cervicomedullary angle CVJ craniovertebral junction JOA Japanese Orthopaedic Association MD mean difference NDI neck disability index NT neck tilt PROs patient-reported outcomes SF-12 PCS the short form 12 physical component summary SD standard deviation SVA sagittal vertical axis TIA thoracic inlet angle T1S T1 slope Chronic atlantoaxial anterior dislocation (AAD) not only results in a high risk of neurological deterioration, but dislocation-related kyphosis also results in neck pain and dysfunction. AAD may result from traumatic, inflammatory, and congenital abnormalities as well as iatrogenic causes.1-3 It is commonly associated with complex deformities such as occipitocervical regional kyphosis or compensative subaxial hyperlordosis,4 which typically presents a “Swan neck” deformity. Clinical treatment indicated that occipitoaxial realignment can be accompanied with a spontaneous decrease in subaxial hyperlordosis in patients with AAD.5,6 In addition, overcorrection of the C1/2 subluxation angle will induce a decreased subaxial angle or even a compensatory kyphotic C2-7 angle. In contrast, undercorrection of the C1/2 subluxation angle may lead to insufficient improvement of C2-C7 lordosis.7 The aforementioned studies displayed the relationship of the occipitoaxial segments and subaxial spine alignment, as well as the treatment target for AAD. However, to the best of our knowledge, few studies have reported the correlation of cervical realignment and improvement in patient-reported outcomes (PROs) after reduction and kyphosis correction in chronic AAD. This study aimed to investigate the effect of a reduction and kyphotic correction of chronic AAD on realignment of cervical spine as well as to clarify the potential independent factors correlated with the improvement of PROs. Endowed with clinical experiences, we hypothesized that the C1-2 Cobb angle correction may significantly correlate with the improvements in PROs. METHODS Setting and Study Population This prospective study was performed from November 2013 to June 2015. Thirty-seven patients who underwent a reduction and kyphosis correction of AAD were routinely evaluated with cervical images. PRO questionnaires (neck disability index [NDI], the short form 12 physical component summary [SF-12 PCS], and Japanese Orthopaedic Association [JOA] score) and physical examinations were recorded by clinical fellows before surgery and follow-up. NDI is a neck-pain-specific PRO tool,8 which was used to reflect how neck pain affects the patients’ behaviors in daily life. SF-12 PCS has been developed to provide a shorter yet valid alternative to SF-36 PCS, which was used to access patients’ general health, physical functioning, role-physical, and bodily pain.9 The JOA score is a generalized index for the assessment of objective cervical spinal cord functional status, such as ambulation, sensation, and muscular tension. Incomplete preoperative and follow-up data were excluded from the results. The investigative protocol and informed consent were approved by our hospital's Institutional Review Board. All subjects provided their informed consent, which was obtained from eligible patients, and the study was designed to conform to the Declaration of Helsinki. The inclusion criteria were patients with AAD who were older than 18 yr and who underwent reduction and kyphosis correction, C1/2 instrumentation, and arthrodesis. The exclusion criteria were AAD patients with basilar invagination, Klippel-Feil syndrome, fused occiput-C1, previous cervical surgery, tumor, and infection, as well as severe comorbidity and peripheral pathological pain. Surgical Treatment All surgeries were performed by 2 experienced surgeons (K.C., H.Y.) from our spine center. After general anesthesia, the patient was prone positioned with 10 kg Gardner-Well tongs traction to horizontally reduce AAD intraoperatively. The posterior midline incision extended from the inion to spinous process of C3. The lateral walls of C2 and posterior atlantal tubercle were exposed subperiosteally. Subperiosteal dissection continued laterally along the inferior border of C1 lamina. The hook end of Penfield was used to palpate and recognize the superior and medial walls of C2 pars, which may be referred to as the safe insertion of the C2 pedicle screw. The convergence of the medial wall of the C1 lateral mass and inferior border of the C1 posterior arch was recognized, which could be referred to as the safe insertion of the C1 pedicle screw. The pedicle screw position was confirmed by intraoperative fluorography after insertion. The rod was set into the tail of the C2 pedicle screw before a sleeve was used to hold the tail of the C2 screw. Pushing down C2 could result in C1-2 reduction, which completed the indirect decompression. All cases in this cohort were not conducted with direct decompression. The reduction result was routinely confirmed by lateral fluorography before the suture. Granular iliac cancellous bone was harvested to graft at C1-C2 interlaminally after decortication of the lamina. In one irreducible AAD case, extra transoral-releasing atlantodontoid joint was necessary to combine with the posterior approach. Finally, 16 patients underwent C1-C2 arthrodesis with a screw-rod system, and the remaining 5 patients, were fixed with screw-plate instrumentations. Postoperative Care and Follow-up After surgery, Cefazolin was administered for 24 h, and patients wore a hard cervical collar for 3 mo. The mean follow-up was not less than 24 mo. Radiographs and CT scans were taken to assess bone fusion according to the bridging bone formation between C1 and C2 lamina. Radiological Measurements All parameters were measured on cervical radiographs with upright position before surgery and at follow-up. Every figure was recorded by an average value after 2 times' quantifications to decrease measuring errors, which was assessed by 2 of the researchers who did not join the surgeries for reducing subjective potential bias (J.Z., Y.C.), as well as recording PROs. The parameters of cervical alignment10-12 including Cobb angles of C0-1, C1-2, C0-2, and C2-7, the C1-7 sagittal vertical axis (SVA), C2-7 SVA, the center of gravity to C7 SVA (CG-C7 SVA), the thoracic inlet angle (TIA), neck tilt (NT), cervical tilt, cranial tilt, and the T1 slope (T1S) were measured (Figures 1 and 2). FIGURE 1. View largeDownload slide Preoperative and postoperative lateral radiographies of an atlantoaxial anterior dislocation (AAD) case. A, The AAD case with atlantoaxial kyphosis (the C1-2 Cobb angle is subtended between line b and line c) and compensative subaxial cervical hyperlordosis (the C2-7 Cobb angle is subtended between line c and line d). B, After reduction and fusion at C1-2, the subaxial cervical spine switched to lordosis (angle subtended between line c and line d) from hyperlordosis, and the occipitoatlantal Cobb angle improved to postoperative kyphosis (the C0-1 Cobb angle is subtended between line a and line b). C, The C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) were negative values. D, After surgery, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were translated to normal values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Cervicothoracic parameters were significantly improved after surgery. FIGURE 1. View largeDownload slide Preoperative and postoperative lateral radiographies of an atlantoaxial anterior dislocation (AAD) case. A, The AAD case with atlantoaxial kyphosis (the C1-2 Cobb angle is subtended between line b and line c) and compensative subaxial cervical hyperlordosis (the C2-7 Cobb angle is subtended between line c and line d). B, After reduction and fusion at C1-2, the subaxial cervical spine switched to lordosis (angle subtended between line c and line d) from hyperlordosis, and the occipitoatlantal Cobb angle improved to postoperative kyphosis (the C0-1 Cobb angle is subtended between line a and line b). C, The C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) were negative values. D, After surgery, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were translated to normal values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Cervicothoracic parameters were significantly improved after surgery. FIGURE 2. View largeDownload slide Improvements in the positive C2-7 SVA, CG-C7 SVA, and C1-7 SVA. A, Preoperative compensative subaxial cervical hyperlordosis (angle subtended between line c and line d). B, The C2-7 Cobb angle (angle subtended between line c and line d) was improved postoperatively. C, Preoperative C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) are positive values. D, After reduction and kyphosis correction, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were improved and translated to neutral values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Postoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. FIGURE 2. View largeDownload slide Improvements in the positive C2-7 SVA, CG-C7 SVA, and C1-7 SVA. A, Preoperative compensative subaxial cervical hyperlordosis (angle subtended between line c and line d). B, The C2-7 Cobb angle (angle subtended between line c and line d) was improved postoperatively. C, Preoperative C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) are positive values. D, After reduction and kyphosis correction, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were improved and translated to neutral values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Postoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. Statistical Analysis SPSS Version 19.0 statistical software (IBM, Armonk, New York) was used to analyze all data, which were presented as the mean and standard deviation (SD). Patients with incomplete data were excluded in this study, and a P value less than 0.05 was considered significant. Preoperative and follow-up NDI, SF-12 PCS, and JOA score were compared by a paired t test. Associations between cervical realignment and the improvement of PROs were identified by the Pearson correlation. Multiple stepwise regression was used to distinguish the independent parameters, which may affect the PROs. RESULTS Of the 37 surgical cases, 16 (43%) were excluded due to loss to follow-up or had incomplete data, and the remaining 21 (57%) patients with an average disease course of 39.4 ± 7.8 mo were analyzed in this study. The mean age of the 12 male and 9 female patients was 48.1 ± 6.3 yr. This cohort consisted of 16 chronic traumatic AADs and 4 congenital and 1 rheumatoid AAD. One case was irreducible AAD, and the remaining 20 cases were reducible (Table 1). TABLE 1. Demographic Characteristics Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  BMI, body mass index. aValues of age, BMI, and duration of disease were presented as mean ± standard deviation. View Large TABLE 1. Demographic Characteristics Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  BMI, body mass index. aValues of age, BMI, and duration of disease were presented as mean ± standard deviation. View Large Surgical Results and Cervical Sagittal Realignment The parameters from the cervical and cervicothoracic sagittal alignments showed significant improvements after surgery and all patients achieved osseous fusion. The mean operation time was 120 min (range, 90-180 min), mean intraoperative blood loss was 260 ml (range, 100-620 ml) and mean hospital stay after surgery was 5 d (range, 3-8 d). All incisions primarily healed, and there were no instrument failures, loss of reduction and correction after surgery. The preoperative C1-2 Cobb angle significantly improved after surgery (−4.0° ± 16.2° vs −13.5° ± 8.1°; mean difference [MD] = −9.5°, 95% confidence interval [CI], −10.9° to 3.2° vs −16.9° to −10.0°, P = .005), as did the C2-7 Cobb angle, TIA, cervical tilt and T1S. The parameters of sagittal realignment are summarized in Table 2. TABLE 2. Pre- and Follow-up Comparisons of Radiographic Parameters Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  CI, confidence interval; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large TABLE 2. Pre- and Follow-up Comparisons of Radiographic Parameters Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  CI, confidence interval; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large Patient-Reported Outcomes NDI, JOA, and SF-12 PCS scores showed that PROs were improved at follow-up. The SF-12 PCS score improved from preoperatively to last follow-up (31.3 ± 5.1 vs 45.9 ± 1.9; MD = 14.6, 95% CI, 29.3-33.6 vs 45.1-47.1, P < .001). The NDI score decreased from 42.5 ± 4.8 before surgery to 8.2 ± 2.9 at the most recent follow-up (MD = −34.3, 95% CI, 41.3-44.8 vs 6.9-9.5, P < .001), as did the JOA score. The preoperative and last follow-up PROs are summarized in Table 3. TABLE 3. Preoperative and Follow-up Comparisons of Patient-Reported Outcomes Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  CI, confidence interval; JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large TABLE 3. Preoperative and Follow-up Comparisons of Patient-Reported Outcomes Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  CI, confidence interval; JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large Associations of Cervical Realignment With an Improvement of PROs Several parameters were associated with improvements in SF-12 PCS, NDI, and JOA scores. Specifically, we found that an improvement in the JOA score was associated with changes in the C1-2 Cobb angle, C0-2 Cobb angle, and C2-7 Cobb angle (r = −0.600, r = −0.433, and r = 0.512, respectively), improvement in NDI was associated with the changes in the C1-2 Cobb angle, C0-2 Cobb angle, C2-7 Cobb angle, C2-7 SVA, and cranial tilt (r = 0.676, r = 0.598, r = −0.612, r = −0.487, and r = −0.445, respectively). Amelioration of SF-12 PCS was relevant to the changes in the C1-2 Cobb angle, C0-2 Cobb angle, and C2-7 Cobb angle (r = −0.592, r = −0.526, and r = 0.469, respectively; Table 4). TABLE 4. Associations Between Changes of Cervical Sagittal Realignment and Improvements of Patient-Reported Outcomes Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01); The values in table were correlation coefficients with 1-tailed test. View Large TABLE 4. Associations Between Changes of Cervical Sagittal Realignment and Improvements of Patient-Reported Outcomes Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01); The values in table were correlation coefficients with 1-tailed test. View Large Multiple Stepwise Regression Analysis After controlling for the potential confounding variables, we found an improvement in C1-2 Cobb angle as an independent factor correlated with an amelioration of the JOA score (R2 = 0.360, P = .004, Figure 3A), NDI (R2 = 0.457, P = .001, Figure 3B), and SF-12 PCS (R2 = 0.351, P = .005, Figure 3C; Table 5). FIGURE 3. View largeDownload slide Correlated coefficients of the improvement in the JOA, NDI, and SF-12 PCS scores with the restoring of the C1-2 Cobb angle. A, ΔJOA was negatively correlated with the ΔC1-2 Cobb angle (P = .004). B, ΔNDI was positively correlated with the C1-2 Cobb angle (P = .001). C, T1S (P = .005) was negatively correlated with the C1-2 Cobb angle. FIGURE 3. View largeDownload slide Correlated coefficients of the improvement in the JOA, NDI, and SF-12 PCS scores with the restoring of the C1-2 Cobb angle. A, ΔJOA was negatively correlated with the ΔC1-2 Cobb angle (P = .004). B, ΔNDI was positively correlated with the C1-2 Cobb angle (P = .001). C, T1S (P = .005) was negatively correlated with the C1-2 Cobb angle. TABLE 5. The Results of Stepwise Multiple Linear Regression Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). View Large TABLE 5. The Results of Stepwise Multiple Linear Regression Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). View Large DISCUSSION Chronic AAD is frequently associated with kyphosis and result in a compensatory hyperlordosis in the subaxial cervical spine. Statistically significant preoperative negative associations were observed between the upper (C1-2) and lower (C2-7) cervical spinal sagittal angles (r = −0.852) in this cohort, which was consistent with Wang's report,6 which described the range of Occiput-C2 angles as −35.2° to 44.8°. The C2-C7 angles were −17.4° to 77.8° in a series of 298 patients with AAD and atlas occipitalization. Other studies also discovered the negative association between the upper and lower cervical Cobb angles in normal volunteers.13,14 This reciprocal compensatory change between the upper and lower cervical spine was proposed to act as an indispensable role for maintaining horizontal gaze. Concomitant Subaxial Realignment After AAD-Related Kyphosis Correction Significant subaxial cervical realignment occurred after reduction and kyphosis correction of atlantoaxial dislocation in this study. However, insufficient or excessive reduction and kyphosis correction of AAD may induce an exaggerated subaxial lordotic or kyphotic malalignment and result in a shifting head posteriorly or anteriorly. Several studies reported these unfavorable reciprocal changes before and after occipitocervical fusion. Matsunaga et al15 demonstrated that the occurrence of these changes was related to the occipitoaxial angle created intraoperatively. Yoshimoto16 reported that excessive reduction in the atlantoaxial joint with a hyperlordotic position could lead to a subaxial kyphotic alignment. Thus, it is important that atlantoaxial joint is fused in correct neutral alignment intraoperatively. However, it was difficult for surgeons to estimate the correct neutral alignment during surgery.17 To achieve intraoperative craniocervical neutral alignment, we used Gardner-Well tong traction to maintain craniocervical straightness. In asymptomatic normal volunteers, atlantoaxial lordosis ranges from 25.6° to 28.9°, lordosis of occipital-axial angle ranges from 14.5° to 16°, and subaxial lordosis ranges from 9° to 16°.13,14 A large percentage of 75% to 80% of cervical standing lordosis was due to the C1-2 joint,18,19 while the mean occiput-C1 kyphotic segment is 2.1° ± 5.0°.18 In our series, C1-2 lordotic angle was improved to 13.5° ± 8.1° from −4.0° ± 16.2° preoperatively, and the C2-7 lordotic angle was sequentially changed from −29.2° ± 11.2° to −18.0° ± 12.0° postoperatively, which was approximately within a normal range. Association of Cervical Realignment With the Improvements in PROs In this study, most of the patients not only had severe myelopathic symptoms with preoperative low JOA scores, but also had physical and neck functional disabilities with low SF-12 PCS scores and high NDI scores. Postoperatively improved JOA, SF-12 PCS, and NDI scores reflected ameliorative myelopathy as well as physical and neck function. Gao20 operated on 44 patients with AAD, demonstrated JOA score significantly improved after surgeries and the postoperative cervicomedullary angle (CMA) significantly increased. Reiter21 found that JOA score was significantly correlated with increased CMA after reduction and symptom improvement and reported that patients with CMA less than 135° were most suitable for posterior atlantoaxial arthrodesis. Since CMA can be used to evaluate the effects of craniovertebral junction (CVJ) surgery on relieving the compression of medulla spinalis, postoperative normal CMA indicates thorough decompression surgeries. Jiang's study22 showed that immediately improved JOA scores were related to increased CMA and vice versa (Pearson's coefficient = 0.46, P < .05) and demonstrated that CVJ volume change rate was more sensitive in evaluating neurological function recovery (Pearson's coefficient = 0.63, P < .05). However, in our study, we found that the improved JOA score was correlated with improved C1-2 lordosis in chronic AAD patients. CMA was increased to normal when the C1-2 angle was reduced from dislocation status, in which the compression of the medulla spinalis was relieved. We preferred to analyze the correlation between the improvement of JOA score and the change in C1-2 Cobb angle postoperatively versus preoperatively, rather than analyze the correlation of the postoperative C1-2 Cobb angle and JOA score, because the majority of patients in this series had similar postoperative upper cervical alignment and JOA scores. Thus, it was difficult to determine a subtle change. This was why our result of a correlation of restoration of the C1-2 Cobb angle and clinical outcomes was different from Passias's report,5 in which the correlation of the JOA score was not significant with the clinical outcomes. To the best of our knowledge, no study has investigated physical and neck function-related score improvement after AAD surgery except neurological functional amelioration. We found that improvement in NDI and SF-12 PCS correlated well with an improvement in C1-2 Cobb angle due to the restoration of upper cervical lordosis. To maintain horizontal gaze in the existing C1-2 anterior dislocation and kyphosis, subaxial cervical segments have to be switched to the hyperlordotic status to support the head, and cervical extensor muscles work more energetically as well, which result in musculoskeletal dysfunction and neck pain.23,24 Neck pain is a common clinical symptom and is relevant to health-related quality of life.25 When kyphotic C1-2 segments were changed to lordosis, the compensatory hyperlordotic C2-7 segments were improved to physiological lordotic status, which may result in normal cervical alignment. With the changes in our series, the postoperative neck pain-related NDI score and physical-related SF-12 PCS improved significantly. Changes Between Preoperative and Postoperative C2-7 SVA In our previous study, C2-7 SVA, which reflects the shifting of head and neck, was tightly correlated with improved NDI after realignment of cervical spinal tuberculotic kyphosis.26 C2-7 SVA is the distance between a plumb line dropped from the centroid of C2 and another vertical line dropped from the posterosuperior corner of C7. The normal value of C2-7 SVA was distributed in a narrow range (16.8 ± 11.2 mm), which was measured from asymptomatic volunteers.18 In current study, we found that the preoperative C2-7 SVA were larger than the normal range in the majority of cases and then decreased closely to normal values after C1-2 reduction and kyphosis correction. However, the improvement of C2-7 SVA was not correlated with JOA score or SF-12 PCS. Tracing this question from its source, we found that some patients had negative preoperative C2-7 SVA, and others had positive preoperative C2-7 SVA (Figures 1 and 2). Thus, the values of C2-7 SVA in some cases were counteracted for each other when analyzing all of the values together. This may also contribute to small values of preoperative and postoperative C2-7 SVA and no significant difference between preoperative and postoperative C2-7 SVA values. Thus, an improvement in C2-7 SVA was not the significant factor associated with PROs in this cohort. Limitations There were some limitations in this study. First, although this was a prospective study, of the recruited 37 patients, 43% patients (16/37) were lost to follow-up, which might potentially confound the study results. In addition, the remaining 21 (57%) cases consisted of a small sample that may not result in powerful statistical results. However, since chronic kyphotic AAD cases are not so common in clinical work, this is the first study to assess sagittal realignment of cervical spine of AAD and its correlation with the improvements in PROs. In addition, correction of the C1-2 Cobb angle was an independent factor to improve PROs. Thus, a multicenter, large sample study is required in future studies. Second, the instruments used in this study had not been strictly controlled, which may generate clinical heterogeneity. Third, 95.2% (20/21) of the procedures were performed using only the posterior approach, while 4.8% (1/21) were conducted by combined approaches with anterior release and posterior reduction. It was difficult to evaluate the confounding factors from different approaches in this study. Furthermore, it was a 2-dimensional analysis based on lateral radiographs, while biases of rotational dislocation had not been considered. CONCLUSION Dislocation-related kyphosis correction surgery not only realigned the atlantoaxial segments but also concomitantly realigned subaxial cervical spine in patients with chronic AAD. Cervical realignment significantly improves PROs. The C1-2 Cobb angle is an independent parameter correlated with the improvement in PROs, which enlightens spine surgeons to pay more attention to correct C1-2 dislocation-related kyphosis in patients with AAD. Disclosures The present study was financially supported by the grants of China Scholarship Council (2017-3109/201708260068), National Natural Science Foundation of China (81460405), 5511 Innovation-driven Program of Jiangxi Province Department of Science and Technology (20165BCB18017), and Key Program of Jaingxi Provincial Department of Science and Technology (20152ACB21024). The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Subin B, Liu JF, Marshall GJ, Huang HY, Ou JH, Xu GZ. Transoral anterior decompression and fusion of chronic irreducible atlantoaxial dislocation with spinal cord compression. Spine . 1995; 20( 11): 1233- 1240. Google Scholar CrossRef Search ADS PubMed  2. Sim FH, Svien HJ, Bickel WH, Janes JM. Swan-Neck deformity following extensive cervical laminectomy. J Bone Joint Surg Am . 1974; 56( 3): 564- 580. Google Scholar CrossRef Search ADS PubMed  3. Fasset DR, Clark R, Brockmeyer DL, Schmidt MH. Cervical spine deformity associated with resection of spinal cord tumors. Neurosurg Focus . 2006; 20( 2): 1- 7. 4. Passias PG, Wang S, Kozanek M, Wang S, Wang C. Relationship between the alignment of the occipitoaxial and subaxial cervical spine in patients with congenital atlantoxial dislocations. J Spinal Disord Tech . 2013; 26( 1): 15- 21. Google Scholar CrossRef Search ADS PubMed  5. Passias PG, Wang S, Zhao D, Wang S, Kozanek M, Wang C. The reversibility of swan neck deformity in chronic atlantoaxial dislocations. Spine . 2013; 38( 7): E379- E385. Google Scholar CrossRef Search ADS PubMed  6. Wang S, Passias PG, Cui L et al.   Does atlantoaxial dislocation influence the subaxial cervical spine? Eur Spine J . 2013; 22( 7): 1603- 1607. Google Scholar CrossRef Search ADS PubMed  7. Kato Y, Itoh T, Kanaya K, Kubota M, Ito S. Relation between atlantoaxial (C1/2) and cervical alignment (C2-C7) angles with Magerl and Brooks techniques for atlantoaxial subluxation in rheumatoid arthritis. J Orthop Sci . 2006; 11( 4): 347- 352. Google Scholar CrossRef Search ADS PubMed  8. Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity. J Manipulative Physiol Ther . 1991; 14( 7): 409- 415. Google Scholar PubMed  9. Ware JE, Kosinski M, Keller SD. SF-12: How to Score the SF-12 Physical and Mental Health Summary Scales . 2nd ed., Boston, MA: The Health Institute, New England Medical Center; 1995. 10. Kim KN, Ahn PG, Ryu MJ et al.   Long-term surgical outcomes of cervical myelopathy with athetoid cerebral palsy. Eur Spine J . 2014; 23( 7): 1464- 1471. Google Scholar CrossRef Search ADS PubMed  11. Lee SH, Kim KT, Seo EM, Suk KS, Kwack YH, Son ES. The influence of thoracic inlet alignment on the craniocervical sagittal postoperative sagittal realignment in kyphotic cervical tuberculosis balance in asymptomatic adults. J Spinal Disord Tech . 2012; 25( 2): E41- E47. Google Scholar CrossRef Search ADS PubMed  12. Scheer JK, Tang JA, Smith JS et al.   Cervical spine alignment, sagittal deformity, and clinical implications: a review. J Neurosurg Spine . 2013; 19( 2): 141- 159. Google Scholar CrossRef Search ADS PubMed  13. Nojiri K, Matsumoto M, Chiba K et al.   Relationship between alignment of upper and lower cervical spine in asymptomatic individuals. J Neurosurg . 2003; 99( 1 Suppl): 80- 83. Google Scholar PubMed  14. Sherekar SK, Yadav YR, Basoor AS, Baghel A, Adam N. Clinical implications of alignment of upper and lower cervical spine. Neurol India . 2006; 54( 3): 264- 267. Google Scholar CrossRef Search ADS PubMed  15. Matsunaga S, Onishi T, Sakou T. Significance of occipitoaxial angle in subaxial lesion after occipitocervical fusion. Spine . Spine (Phila Pa 1976). 2001; 26( 2): 161- 165. Google Scholar CrossRef Search ADS PubMed  16. Yoshimoto H, Ito M, Abumi K et al.   A retrospective radiographic analysis of subaxial sagittal alignment after posterior C1–2 fusion. Spine . 2004; 29( 2): 175- 181. Google Scholar CrossRef Search ADS PubMed  17. Kuntz C, Levin LS, Ondra SL, Shaffrey CI, Morgan CJ. Neutral upright sagittal spinal alignment from the occiput to the pelvis in asymptomatic adults: a review and resynthesis of the literature. J Neurosurg Spine . 2007; 6( 2): 104- 112. Google Scholar CrossRef Search ADS PubMed  18. Hardacker JW, Shuford RF, Capicotto PN, Pryor PW: Radiographic standing cervical segmental alignment in adult volunteers without neck symptoms. Spine . 1997; 22( 13): 1472- 1479. Google Scholar CrossRef Search ADS PubMed  19. Jackson RP, McManus AC. Radiographic analysis of sagittal plane alignment and balance in standing volunteers and patients with low back pain matched for age, sex, and size: a prospective controlled clinical study. Spine . 1994; 19( 14): 1611- 1618. Google Scholar CrossRef Search ADS PubMed  20. Gao F, Wang Q, Liu C, Xiong B, Luo T. Individualized 3D printed model-assisted posterior screw fixation for the treatment of craniovertebral junction abnormality: a retrospective study. J Neurosurg Spine . 2017; 27( 1): 29- 34. Google Scholar CrossRef Search ADS PubMed  21. Reiter MF, Boden SD. Inflammatory disorders of the cervical spine. Spine . 1998; 23( 24): 2755- 2766. Google Scholar CrossRef Search ADS PubMed  22. Jiang YW, Xia H, Wang ZY et al.   Variation of craniocervical junction volume as an effective parameter for basilar invagination treatment. Eur Rev Med Pharmacol Sci . 2015; 19( 10): 1754- 1760. Google Scholar PubMed  23. Park JH, Kang SY, Lee SG, Jeon HS. The effects of smart phone gaming duration on muscle activation and spinal posture: pilot study. Physiother Theory Pract . 2017; 33( 8): 661- 669. Google Scholar CrossRef Search ADS PubMed  24. Khayatzadeh S, Kalmanson OA, Schuit D et al.   Cervical spine muscle-tendon unit length differences between neutral and forward head postures: biomechanical study using human cadaveric specimens. Phys Ther . 2017; 97( 7): 756- 766. Google Scholar CrossRef Search ADS PubMed  25. Lippa L, Lippa L, Cacciola F. Loss of cervical lordosis: what is the prognosis? J Craniovert Jun Spine . 2017; 8( 1): 9- 14. Google Scholar CrossRef Search ADS   26. Pan Z, Luo J, Cao K et al.   Debridement and reconstruction improve postoperative sagittal alignment in kyphotic cervical spinal tuberculosis. Clin Orthop Relat Res . 2017; 475( 8): 2084- 2091. Google Scholar CrossRef Search ADS PubMed  Acknowledgments We thank the reviewers and editors for their helpful comments on this article, and thank Sun Kyu Choi (who is a biostatistician works at Yonsei University College of Medicine) for his statistical suggestions. Copyright © 2018 by the Congress of Neurological Surgeons http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

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Copyright © 2018 by the Congress of Neurological Surgeons
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Abstract

Abstract BACKGROUND Chronic atlantoaxial anterior dislocation (AAD) not only results in myelopathy, but dislocation-related kyphosis also results in cervical malalignment, which permanently affects neck function and patient-reported outcomes (PROs). OBJECTIVE To investigate the effect of kyphotic correction on realigning cervical spine and independent cervical alignment parameters, which may be correlated with an improvement of PROs. METHODS The study included 21 patients with chronic AAD-related kyphosis who underwent C1-2 reduction and correction surgery. Radiographic parameters were measured to assess cervical realignment preoperatively and postoperatively. Neck disability index (NDI), short form 12 physical component summary (SF-12 PCS), and Japanese Orthopaedic Association (JOA) scores were recorded to reveal changes in PROs. The independent parameters correlated with the improvements of PROs were analyzed. RESULTS Of the radiographic parameters, the C1-2 Cobb angle, the C2-7 Cobb angle, thoracic inlet angle, cervical tilt, and T1 slope were significantly changed from −4.0° ± 16.2°, −29.2° ± 11.2°, 73.1° ± 13.3°, 30.4° ± 8.5°, and 29.1° ± 8.8° preoperatively to −13.5° ± 8.1° (P = .005), −18.0° ± 12.0° (P < .001), 67.1° ± 11.6° (P = .042), 23.1° ± 10.3° (P = .007), and 24.0° ± 7.0° (P = .011) at last follow-up, respectively. NDI, JOA, and SF-12 PCS scores were significantly improved postoperatively. The C1-2 Cobb angle was an independent parameter correlated with the improvements in SF-12 PCS, NDI, and JOA scores. CONCLUSION Correction and reduction surgery can realign cervical spine in chronic AAD patients. The C1-2 Cobb angle was an independent parameter correlated with the improvements of PROs. Cervical spine alignment, Atlantoaxial anterior dislocation, Reduction, Kyphosis correction, Patient-reported outcomes ABBREVIATIONS ABBREVIATIONS AAD atlantoaxial anterior dislocation CG-C7 SVA center of gravity to C7 SVA CI confidence interval CMA cervicomedullary angle CVJ craniovertebral junction JOA Japanese Orthopaedic Association MD mean difference NDI neck disability index NT neck tilt PROs patient-reported outcomes SF-12 PCS the short form 12 physical component summary SD standard deviation SVA sagittal vertical axis TIA thoracic inlet angle T1S T1 slope Chronic atlantoaxial anterior dislocation (AAD) not only results in a high risk of neurological deterioration, but dislocation-related kyphosis also results in neck pain and dysfunction. AAD may result from traumatic, inflammatory, and congenital abnormalities as well as iatrogenic causes.1-3 It is commonly associated with complex deformities such as occipitocervical regional kyphosis or compensative subaxial hyperlordosis,4 which typically presents a “Swan neck” deformity. Clinical treatment indicated that occipitoaxial realignment can be accompanied with a spontaneous decrease in subaxial hyperlordosis in patients with AAD.5,6 In addition, overcorrection of the C1/2 subluxation angle will induce a decreased subaxial angle or even a compensatory kyphotic C2-7 angle. In contrast, undercorrection of the C1/2 subluxation angle may lead to insufficient improvement of C2-C7 lordosis.7 The aforementioned studies displayed the relationship of the occipitoaxial segments and subaxial spine alignment, as well as the treatment target for AAD. However, to the best of our knowledge, few studies have reported the correlation of cervical realignment and improvement in patient-reported outcomes (PROs) after reduction and kyphosis correction in chronic AAD. This study aimed to investigate the effect of a reduction and kyphotic correction of chronic AAD on realignment of cervical spine as well as to clarify the potential independent factors correlated with the improvement of PROs. Endowed with clinical experiences, we hypothesized that the C1-2 Cobb angle correction may significantly correlate with the improvements in PROs. METHODS Setting and Study Population This prospective study was performed from November 2013 to June 2015. Thirty-seven patients who underwent a reduction and kyphosis correction of AAD were routinely evaluated with cervical images. PRO questionnaires (neck disability index [NDI], the short form 12 physical component summary [SF-12 PCS], and Japanese Orthopaedic Association [JOA] score) and physical examinations were recorded by clinical fellows before surgery and follow-up. NDI is a neck-pain-specific PRO tool,8 which was used to reflect how neck pain affects the patients’ behaviors in daily life. SF-12 PCS has been developed to provide a shorter yet valid alternative to SF-36 PCS, which was used to access patients’ general health, physical functioning, role-physical, and bodily pain.9 The JOA score is a generalized index for the assessment of objective cervical spinal cord functional status, such as ambulation, sensation, and muscular tension. Incomplete preoperative and follow-up data were excluded from the results. The investigative protocol and informed consent were approved by our hospital's Institutional Review Board. All subjects provided their informed consent, which was obtained from eligible patients, and the study was designed to conform to the Declaration of Helsinki. The inclusion criteria were patients with AAD who were older than 18 yr and who underwent reduction and kyphosis correction, C1/2 instrumentation, and arthrodesis. The exclusion criteria were AAD patients with basilar invagination, Klippel-Feil syndrome, fused occiput-C1, previous cervical surgery, tumor, and infection, as well as severe comorbidity and peripheral pathological pain. Surgical Treatment All surgeries were performed by 2 experienced surgeons (K.C., H.Y.) from our spine center. After general anesthesia, the patient was prone positioned with 10 kg Gardner-Well tongs traction to horizontally reduce AAD intraoperatively. The posterior midline incision extended from the inion to spinous process of C3. The lateral walls of C2 and posterior atlantal tubercle were exposed subperiosteally. Subperiosteal dissection continued laterally along the inferior border of C1 lamina. The hook end of Penfield was used to palpate and recognize the superior and medial walls of C2 pars, which may be referred to as the safe insertion of the C2 pedicle screw. The convergence of the medial wall of the C1 lateral mass and inferior border of the C1 posterior arch was recognized, which could be referred to as the safe insertion of the C1 pedicle screw. The pedicle screw position was confirmed by intraoperative fluorography after insertion. The rod was set into the tail of the C2 pedicle screw before a sleeve was used to hold the tail of the C2 screw. Pushing down C2 could result in C1-2 reduction, which completed the indirect decompression. All cases in this cohort were not conducted with direct decompression. The reduction result was routinely confirmed by lateral fluorography before the suture. Granular iliac cancellous bone was harvested to graft at C1-C2 interlaminally after decortication of the lamina. In one irreducible AAD case, extra transoral-releasing atlantodontoid joint was necessary to combine with the posterior approach. Finally, 16 patients underwent C1-C2 arthrodesis with a screw-rod system, and the remaining 5 patients, were fixed with screw-plate instrumentations. Postoperative Care and Follow-up After surgery, Cefazolin was administered for 24 h, and patients wore a hard cervical collar for 3 mo. The mean follow-up was not less than 24 mo. Radiographs and CT scans were taken to assess bone fusion according to the bridging bone formation between C1 and C2 lamina. Radiological Measurements All parameters were measured on cervical radiographs with upright position before surgery and at follow-up. Every figure was recorded by an average value after 2 times' quantifications to decrease measuring errors, which was assessed by 2 of the researchers who did not join the surgeries for reducing subjective potential bias (J.Z., Y.C.), as well as recording PROs. The parameters of cervical alignment10-12 including Cobb angles of C0-1, C1-2, C0-2, and C2-7, the C1-7 sagittal vertical axis (SVA), C2-7 SVA, the center of gravity to C7 SVA (CG-C7 SVA), the thoracic inlet angle (TIA), neck tilt (NT), cervical tilt, cranial tilt, and the T1 slope (T1S) were measured (Figures 1 and 2). FIGURE 1. View largeDownload slide Preoperative and postoperative lateral radiographies of an atlantoaxial anterior dislocation (AAD) case. A, The AAD case with atlantoaxial kyphosis (the C1-2 Cobb angle is subtended between line b and line c) and compensative subaxial cervical hyperlordosis (the C2-7 Cobb angle is subtended between line c and line d). B, After reduction and fusion at C1-2, the subaxial cervical spine switched to lordosis (angle subtended between line c and line d) from hyperlordosis, and the occipitoatlantal Cobb angle improved to postoperative kyphosis (the C0-1 Cobb angle is subtended between line a and line b). C, The C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) were negative values. D, After surgery, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were translated to normal values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Cervicothoracic parameters were significantly improved after surgery. FIGURE 1. View largeDownload slide Preoperative and postoperative lateral radiographies of an atlantoaxial anterior dislocation (AAD) case. A, The AAD case with atlantoaxial kyphosis (the C1-2 Cobb angle is subtended between line b and line c) and compensative subaxial cervical hyperlordosis (the C2-7 Cobb angle is subtended between line c and line d). B, After reduction and fusion at C1-2, the subaxial cervical spine switched to lordosis (angle subtended between line c and line d) from hyperlordosis, and the occipitoatlantal Cobb angle improved to postoperative kyphosis (the C0-1 Cobb angle is subtended between line a and line b). C, The C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) were negative values. D, After surgery, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were translated to normal values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Cervicothoracic parameters were significantly improved after surgery. FIGURE 2. View largeDownload slide Improvements in the positive C2-7 SVA, CG-C7 SVA, and C1-7 SVA. A, Preoperative compensative subaxial cervical hyperlordosis (angle subtended between line c and line d). B, The C2-7 Cobb angle (angle subtended between line c and line d) was improved postoperatively. C, Preoperative C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) are positive values. D, After reduction and kyphosis correction, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were improved and translated to neutral values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Postoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. FIGURE 2. View largeDownload slide Improvements in the positive C2-7 SVA, CG-C7 SVA, and C1-7 SVA. A, Preoperative compensative subaxial cervical hyperlordosis (angle subtended between line c and line d). B, The C2-7 Cobb angle (angle subtended between line c and line d) was improved postoperatively. C, Preoperative C2-7 SVA (green line), CG-C7 SVA (yellow line), and C1-7 SVA (red line) are positive values. D, After reduction and kyphosis correction, C1-7 SVA, CG-C7 SVA, and C2-7 SVA were improved and translated to neutral values. E, Preoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. F, Postoperative cervicothoracic parameters, including TIA, NT, T1S, cervical tilt, and cranial tilt. Statistical Analysis SPSS Version 19.0 statistical software (IBM, Armonk, New York) was used to analyze all data, which were presented as the mean and standard deviation (SD). Patients with incomplete data were excluded in this study, and a P value less than 0.05 was considered significant. Preoperative and follow-up NDI, SF-12 PCS, and JOA score were compared by a paired t test. Associations between cervical realignment and the improvement of PROs were identified by the Pearson correlation. Multiple stepwise regression was used to distinguish the independent parameters, which may affect the PROs. RESULTS Of the 37 surgical cases, 16 (43%) were excluded due to loss to follow-up or had incomplete data, and the remaining 21 (57%) patients with an average disease course of 39.4 ± 7.8 mo were analyzed in this study. The mean age of the 12 male and 9 female patients was 48.1 ± 6.3 yr. This cohort consisted of 16 chronic traumatic AADs and 4 congenital and 1 rheumatoid AAD. One case was irreducible AAD, and the remaining 20 cases were reducible (Table 1). TABLE 1. Demographic Characteristics Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  BMI, body mass index. aValues of age, BMI, and duration of disease were presented as mean ± standard deviation. View Large TABLE 1. Demographic Characteristics Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  Characteristic  Values  Gender     Female  9   Male  12  aAge (years)  48.1 ± 6.3  aBMI (kg/cm2)  23.3 ± 2.9  aDuration of disease (months)  39.4 ± 7.8  Etiology     Traumatic  16   Congenital  4   Rheumatoid  1  Surgery approach     Posterior only  20   Anteroposterior combined  1  BMI, body mass index. aValues of age, BMI, and duration of disease were presented as mean ± standard deviation. View Large Surgical Results and Cervical Sagittal Realignment The parameters from the cervical and cervicothoracic sagittal alignments showed significant improvements after surgery and all patients achieved osseous fusion. The mean operation time was 120 min (range, 90-180 min), mean intraoperative blood loss was 260 ml (range, 100-620 ml) and mean hospital stay after surgery was 5 d (range, 3-8 d). All incisions primarily healed, and there were no instrument failures, loss of reduction and correction after surgery. The preoperative C1-2 Cobb angle significantly improved after surgery (−4.0° ± 16.2° vs −13.5° ± 8.1°; mean difference [MD] = −9.5°, 95% confidence interval [CI], −10.9° to 3.2° vs −16.9° to −10.0°, P = .005), as did the C2-7 Cobb angle, TIA, cervical tilt and T1S. The parameters of sagittal realignment are summarized in Table 2. TABLE 2. Pre- and Follow-up Comparisons of Radiographic Parameters Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  CI, confidence interval; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large TABLE 2. Pre- and Follow-up Comparisons of Radiographic Parameters Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  C0-1 Cobb angle (°)  0.9 ± 9.1 (−3.1-5.0)  2.7 ± 7.1 (−0.4-5.6)  .325  C1-2 Cobb angle (°)  −4.0 ± 16.2 (−10.9-3.2)  −13.5 ± 8.1 (−16.9 to −10.0)  .005b  C0-2 Cobb angle (°)  −3.1 ± 12.2 (−8.3-2.4)  −10.8 ± 6.6 (−13.3 to −7.9)  .058  C2-7 Cobb angle (°)  −29.2 ± 11.2 (−33.8 to −24.3)  −18.0 ± 12.0 (−23.1 to −12.7)  <.001b  C1-7 SVA (mm)  23.2 ± 22.1 (13.5-32.7)  20.8 ± 16.6 (13.2-28.0)  .568  C2-7 SVA (mm)  3.4 ± 21.0 (−5.9-12.5)  9.0 ± 14.3 (2.6-15.3)  .178  CG-C7 SVA (mm)  15.9 ± 22.6 (6.1-25.8)  13.2 ± 18.7 (4.3-22.1)  .553  TIA (°)  73.1 ± 13.3 (67.2-79.4)  67.1 ± 11.6 (61.8-71.9)  .042a  NT (°)  43.9 ± 11.3 (39.1-49.1)  43.1 ± 9.1 (39.0-47.3)  .712  Cervical tilt (°)  30.4 ± 8.5 (26.7-34.6)  23.1 ± 10.3 (18.4-26.9)  .007a  Cranial tilt (°)  −1.2 ± 11.1 (−6.3-3.8)  0.9 ± 8.2 (−2.7-4.5)  .341  T1S (°)  29.1 ± 8.8 (25.6-33.1)  24.0 ± 7.0 (21.2-26.7)  .011a  CI, confidence interval; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large Patient-Reported Outcomes NDI, JOA, and SF-12 PCS scores showed that PROs were improved at follow-up. The SF-12 PCS score improved from preoperatively to last follow-up (31.3 ± 5.1 vs 45.9 ± 1.9; MD = 14.6, 95% CI, 29.3-33.6 vs 45.1-47.1, P < .001). The NDI score decreased from 42.5 ± 4.8 before surgery to 8.2 ± 2.9 at the most recent follow-up (MD = −34.3, 95% CI, 41.3-44.8 vs 6.9-9.5, P < .001), as did the JOA score. The preoperative and last follow-up PROs are summarized in Table 3. TABLE 3. Preoperative and Follow-up Comparisons of Patient-Reported Outcomes Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  CI, confidence interval; JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large TABLE 3. Preoperative and Follow-up Comparisons of Patient-Reported Outcomes Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  Variable  Preoperation (95% CI)  Last follow-up (95% CI)  P value  JOA score  8.1 ± 2.5 (7.2-9.3)  14.2 ± 2.1 (13.4-15.0)  <.001a  NDI  42.5 ± 4.8 (41.3-44.8)  8.2 ± 2.9 (6.9-9.5)  <.001a  SF-12 PCS  31.3 ± 5.1 (29.3-33.6)  45.9 ± 1.9 (45.1-47.1)  <.001a  CI, confidence interval; JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). Data presented as mean ± standard deviation. View Large Associations of Cervical Realignment With an Improvement of PROs Several parameters were associated with improvements in SF-12 PCS, NDI, and JOA scores. Specifically, we found that an improvement in the JOA score was associated with changes in the C1-2 Cobb angle, C0-2 Cobb angle, and C2-7 Cobb angle (r = −0.600, r = −0.433, and r = 0.512, respectively), improvement in NDI was associated with the changes in the C1-2 Cobb angle, C0-2 Cobb angle, C2-7 Cobb angle, C2-7 SVA, and cranial tilt (r = 0.676, r = 0.598, r = −0.612, r = −0.487, and r = −0.445, respectively). Amelioration of SF-12 PCS was relevant to the changes in the C1-2 Cobb angle, C0-2 Cobb angle, and C2-7 Cobb angle (r = −0.592, r = −0.526, and r = 0.469, respectively; Table 4). TABLE 4. Associations Between Changes of Cervical Sagittal Realignment and Improvements of Patient-Reported Outcomes Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01); The values in table were correlation coefficients with 1-tailed test. View Large TABLE 4. Associations Between Changes of Cervical Sagittal Realignment and Improvements of Patient-Reported Outcomes Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  Variable  Δ JOA score  Δ NDI  Δ SF-12 PCS  Δ C0-1 Cobb angle (°)  0.345  −0.201  0.243  Δ C1-2 Cobb angle (°)  −0.600b  0.676b  −0.592b  Δ C0-2 Cobb angle (°)  −0.433a  0.598b  −0.526a  Δ C2-7 Cobb angle (°)  0.512b  −0.612b  0.469a  Δ C1-7 SVA (mm)  0.22  −0.374  0.273  Δ C2-7 SVA (mm)  0.312  −0.487a  0.375  Δ CG-C7 SVA (mm)  −0.212  −0.184  0.263  Δ TIA (°)  0.169  −0.232  −0.162  Δ NT (°)  0.241  −0.189  0.301  Δ Cervical tilt (°)  −0.318  0.383  −0.412  Δ Cranial tilt (°)  0.31  −0.445a  0.368  Δ T1S (°)  −0.186  −0.207  −0.266  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary; SVA, sagittal vertical axis; TIA, thoracic inlet angle; NT, neck tilt; T1S, T1 slope. aStatistical significance (P < .05); bStatistical significance (P < .01); The values in table were correlation coefficients with 1-tailed test. View Large Multiple Stepwise Regression Analysis After controlling for the potential confounding variables, we found an improvement in C1-2 Cobb angle as an independent factor correlated with an amelioration of the JOA score (R2 = 0.360, P = .004, Figure 3A), NDI (R2 = 0.457, P = .001, Figure 3B), and SF-12 PCS (R2 = 0.351, P = .005, Figure 3C; Table 5). FIGURE 3. View largeDownload slide Correlated coefficients of the improvement in the JOA, NDI, and SF-12 PCS scores with the restoring of the C1-2 Cobb angle. A, ΔJOA was negatively correlated with the ΔC1-2 Cobb angle (P = .004). B, ΔNDI was positively correlated with the C1-2 Cobb angle (P = .001). C, T1S (P = .005) was negatively correlated with the C1-2 Cobb angle. FIGURE 3. View largeDownload slide Correlated coefficients of the improvement in the JOA, NDI, and SF-12 PCS scores with the restoring of the C1-2 Cobb angle. A, ΔJOA was negatively correlated with the ΔC1-2 Cobb angle (P = .004). B, ΔNDI was positively correlated with the C1-2 Cobb angle (P = .001). C, T1S (P = .005) was negatively correlated with the C1-2 Cobb angle. TABLE 5. The Results of Stepwise Multiple Linear Regression Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). View Large TABLE 5. The Results of Stepwise Multiple Linear Regression Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  Variable  Coefficient  R²  t  P value  ΔJOA score           ΔC1-2  −0.121  0.360  −3.267  .004a   Constant  4.750    7.476  <.001  ΔNDI           ΔC1-2  0.129  0.457  3.998  .001a   Constant  −33.006    −59.565  <.001  ΔSF-12 PCS           ΔC1-2  −0.189  0.351  −3.205  .005a   Constant  12.483    12.344  <.001  JOA, Japanese Orthopaedic Association; NDI, neck disability index; SF-12 PCS, the short form 12 physical component summary. aStatistical significance (P < .01). View Large DISCUSSION Chronic AAD is frequently associated with kyphosis and result in a compensatory hyperlordosis in the subaxial cervical spine. Statistically significant preoperative negative associations were observed between the upper (C1-2) and lower (C2-7) cervical spinal sagittal angles (r = −0.852) in this cohort, which was consistent with Wang's report,6 which described the range of Occiput-C2 angles as −35.2° to 44.8°. The C2-C7 angles were −17.4° to 77.8° in a series of 298 patients with AAD and atlas occipitalization. Other studies also discovered the negative association between the upper and lower cervical Cobb angles in normal volunteers.13,14 This reciprocal compensatory change between the upper and lower cervical spine was proposed to act as an indispensable role for maintaining horizontal gaze. Concomitant Subaxial Realignment After AAD-Related Kyphosis Correction Significant subaxial cervical realignment occurred after reduction and kyphosis correction of atlantoaxial dislocation in this study. However, insufficient or excessive reduction and kyphosis correction of AAD may induce an exaggerated subaxial lordotic or kyphotic malalignment and result in a shifting head posteriorly or anteriorly. Several studies reported these unfavorable reciprocal changes before and after occipitocervical fusion. Matsunaga et al15 demonstrated that the occurrence of these changes was related to the occipitoaxial angle created intraoperatively. Yoshimoto16 reported that excessive reduction in the atlantoaxial joint with a hyperlordotic position could lead to a subaxial kyphotic alignment. Thus, it is important that atlantoaxial joint is fused in correct neutral alignment intraoperatively. However, it was difficult for surgeons to estimate the correct neutral alignment during surgery.17 To achieve intraoperative craniocervical neutral alignment, we used Gardner-Well tong traction to maintain craniocervical straightness. In asymptomatic normal volunteers, atlantoaxial lordosis ranges from 25.6° to 28.9°, lordosis of occipital-axial angle ranges from 14.5° to 16°, and subaxial lordosis ranges from 9° to 16°.13,14 A large percentage of 75% to 80% of cervical standing lordosis was due to the C1-2 joint,18,19 while the mean occiput-C1 kyphotic segment is 2.1° ± 5.0°.18 In our series, C1-2 lordotic angle was improved to 13.5° ± 8.1° from −4.0° ± 16.2° preoperatively, and the C2-7 lordotic angle was sequentially changed from −29.2° ± 11.2° to −18.0° ± 12.0° postoperatively, which was approximately within a normal range. Association of Cervical Realignment With the Improvements in PROs In this study, most of the patients not only had severe myelopathic symptoms with preoperative low JOA scores, but also had physical and neck functional disabilities with low SF-12 PCS scores and high NDI scores. Postoperatively improved JOA, SF-12 PCS, and NDI scores reflected ameliorative myelopathy as well as physical and neck function. Gao20 operated on 44 patients with AAD, demonstrated JOA score significantly improved after surgeries and the postoperative cervicomedullary angle (CMA) significantly increased. Reiter21 found that JOA score was significantly correlated with increased CMA after reduction and symptom improvement and reported that patients with CMA less than 135° were most suitable for posterior atlantoaxial arthrodesis. Since CMA can be used to evaluate the effects of craniovertebral junction (CVJ) surgery on relieving the compression of medulla spinalis, postoperative normal CMA indicates thorough decompression surgeries. Jiang's study22 showed that immediately improved JOA scores were related to increased CMA and vice versa (Pearson's coefficient = 0.46, P < .05) and demonstrated that CVJ volume change rate was more sensitive in evaluating neurological function recovery (Pearson's coefficient = 0.63, P < .05). However, in our study, we found that the improved JOA score was correlated with improved C1-2 lordosis in chronic AAD patients. CMA was increased to normal when the C1-2 angle was reduced from dislocation status, in which the compression of the medulla spinalis was relieved. We preferred to analyze the correlation between the improvement of JOA score and the change in C1-2 Cobb angle postoperatively versus preoperatively, rather than analyze the correlation of the postoperative C1-2 Cobb angle and JOA score, because the majority of patients in this series had similar postoperative upper cervical alignment and JOA scores. Thus, it was difficult to determine a subtle change. This was why our result of a correlation of restoration of the C1-2 Cobb angle and clinical outcomes was different from Passias's report,5 in which the correlation of the JOA score was not significant with the clinical outcomes. To the best of our knowledge, no study has investigated physical and neck function-related score improvement after AAD surgery except neurological functional amelioration. We found that improvement in NDI and SF-12 PCS correlated well with an improvement in C1-2 Cobb angle due to the restoration of upper cervical lordosis. To maintain horizontal gaze in the existing C1-2 anterior dislocation and kyphosis, subaxial cervical segments have to be switched to the hyperlordotic status to support the head, and cervical extensor muscles work more energetically as well, which result in musculoskeletal dysfunction and neck pain.23,24 Neck pain is a common clinical symptom and is relevant to health-related quality of life.25 When kyphotic C1-2 segments were changed to lordosis, the compensatory hyperlordotic C2-7 segments were improved to physiological lordotic status, which may result in normal cervical alignment. With the changes in our series, the postoperative neck pain-related NDI score and physical-related SF-12 PCS improved significantly. Changes Between Preoperative and Postoperative C2-7 SVA In our previous study, C2-7 SVA, which reflects the shifting of head and neck, was tightly correlated with improved NDI after realignment of cervical spinal tuberculotic kyphosis.26 C2-7 SVA is the distance between a plumb line dropped from the centroid of C2 and another vertical line dropped from the posterosuperior corner of C7. The normal value of C2-7 SVA was distributed in a narrow range (16.8 ± 11.2 mm), which was measured from asymptomatic volunteers.18 In current study, we found that the preoperative C2-7 SVA were larger than the normal range in the majority of cases and then decreased closely to normal values after C1-2 reduction and kyphosis correction. However, the improvement of C2-7 SVA was not correlated with JOA score or SF-12 PCS. Tracing this question from its source, we found that some patients had negative preoperative C2-7 SVA, and others had positive preoperative C2-7 SVA (Figures 1 and 2). Thus, the values of C2-7 SVA in some cases were counteracted for each other when analyzing all of the values together. This may also contribute to small values of preoperative and postoperative C2-7 SVA and no significant difference between preoperative and postoperative C2-7 SVA values. Thus, an improvement in C2-7 SVA was not the significant factor associated with PROs in this cohort. Limitations There were some limitations in this study. First, although this was a prospective study, of the recruited 37 patients, 43% patients (16/37) were lost to follow-up, which might potentially confound the study results. In addition, the remaining 21 (57%) cases consisted of a small sample that may not result in powerful statistical results. However, since chronic kyphotic AAD cases are not so common in clinical work, this is the first study to assess sagittal realignment of cervical spine of AAD and its correlation with the improvements in PROs. In addition, correction of the C1-2 Cobb angle was an independent factor to improve PROs. Thus, a multicenter, large sample study is required in future studies. Second, the instruments used in this study had not been strictly controlled, which may generate clinical heterogeneity. Third, 95.2% (20/21) of the procedures were performed using only the posterior approach, while 4.8% (1/21) were conducted by combined approaches with anterior release and posterior reduction. It was difficult to evaluate the confounding factors from different approaches in this study. Furthermore, it was a 2-dimensional analysis based on lateral radiographs, while biases of rotational dislocation had not been considered. CONCLUSION Dislocation-related kyphosis correction surgery not only realigned the atlantoaxial segments but also concomitantly realigned subaxial cervical spine in patients with chronic AAD. Cervical realignment significantly improves PROs. The C1-2 Cobb angle is an independent parameter correlated with the improvement in PROs, which enlightens spine surgeons to pay more attention to correct C1-2 dislocation-related kyphosis in patients with AAD. Disclosures The present study was financially supported by the grants of China Scholarship Council (2017-3109/201708260068), National Natural Science Foundation of China (81460405), 5511 Innovation-driven Program of Jiangxi Province Department of Science and Technology (20165BCB18017), and Key Program of Jaingxi Provincial Department of Science and Technology (20152ACB21024). The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Subin B, Liu JF, Marshall GJ, Huang HY, Ou JH, Xu GZ. Transoral anterior decompression and fusion of chronic irreducible atlantoaxial dislocation with spinal cord compression. Spine . 1995; 20( 11): 1233- 1240. Google Scholar CrossRef Search ADS PubMed  2. 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Google Scholar CrossRef Search ADS PubMed  Acknowledgments We thank the reviewers and editors for their helpful comments on this article, and thank Sun Kyu Choi (who is a biostatistician works at Yonsei University College of Medicine) for his statistical suggestions. Copyright © 2018 by the Congress of Neurological Surgeons

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Operative NeurosurgeryOxford University Press

Published: Mar 20, 2018

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