Cervical spondylotic myelopathy (CSM), an often progressive, degenerative disease, is the leading cause of acquired spinal cord dysfunction worldwide.1,2 The degenerative changes associated with CSM can also result in loss of normal segmental and regional sagittal alignment, including kyphosis and sagittal imbalance.3 These changes may be from primary cervical disease or related to changes in subjacent spinal regions, including thoracic kyphosis and loss of lumbar lordosis.3–5 Compensatory cervical hyperlordosis with resulting dorsal ligamentous buckling and cord impingement may result from global sagittal imbalance.3–5 In addition, segmental kyphosis may contribute to spinal cord dysfunction through multiple mechanisms, including direct compression, repeated flexion/extension injury, and vascular compromise.
Standard strategies for treatment of CSM have focused on direct spinal canal decompression and often stabilization from an anterior or posterior approach.1,6,7 Myelopathy improvements seen after decompression can be quite variable and have been partly associated with patient age, severity, and duration of preoperative myelopathy, chronicity of symptoms prior to surgical intervention, and cord signal changes seen on magnetic resonance imaging (MRI).1,3,8–11
Work in animal models has demonstrated that cord tension may impact cord function via perfusion and that cervical kyphosis may induce gliosis and neuronal apoptosis.3,12,13 Shimizu et al12 developed an animal model of progressive cervical kyphosis and demonstrated a significant correlation between the kyphotic angle and the development of spinal cord compression, demyelination, vascular compromise, and neuronal cell loss. The study of human cadaveric models of cervical and thoracic kyphosis has demonstrated significant increase in spinal cord intramedullary pressure with progressive deformity.14–16 Reports have also detailed the use of posterior vertebral column subtraction osteotomy techniques as a means of reducing cord tension resulting from recurrent tethered cord syndrome.17,18
To date, the correlations between cervical alignment, sagittal balance, and myelopathy have not been well characterized. Furthermore, it is not well understood whether alignment correction in the cervical spine, in addition to adequate decompression in certain circumstances, may further improve myelopathy scores and disability via decreased cord tension.19–21 The exact extent and manner in which the spinal cord morphological characteristics would respond to changes in vertebral column realignment are unknown.
As a means of evaluating this in detail, our objectives in the present study included development of new methods to determine in vivo cervical spinal cord length, surface area, and volume in relation to vertebral column alignment. This technique was then applied and correlated to preoperative alignment, myelopathy, and disability scores in a group of patients with cervical myelopathy undergoing surgical treatment. On the basis of development of these novel techniques, future work will correlate alignment changes to cord morphology changes and myelopathy outcomes with the global objective of improving the outcomes for patients with CSM treated surgically by better understanding the potential impact of cervical deformity/alignment on myelopathy.
MATERIALS AND METHODS
This study was a post hoc analysis of prospectively collected data from the AOSpine North America CSM Study, which included 302 patients surgically treated for CSM from 12 sites across North America.1,22 For the original prospective study, consecutive patients were offered enrollment between December 2005 and September 2007; only a small number declined to participate. All contributing centers were members of SpineNet, an AOSpine North America consortium dedicated to research of spinal disorders. Key database inclusion criteria were as follows: age 18 years or older, symptomatic CSM (with clinical signs of myelopathy), MRI or computed tomography–myelography demonstrating cervical spinal cord compression, no prior surgical treatment of CSM, and no symptomatic lumbar stenosis. A standardized list of comorbidities was assessed for each patient enrolled, including the presence of diabetes (see Supplementary Digital Content Table 1, available at http://links.lww.com/BRS/A833). Subjects for this study were selected only if they had preoperative MRI in DICOM format that showed the spinal levels from C2 to T1 and preoperative upright sagittal cervical spine radiography in the neutral position. Institutional review board approval was obtained at University of Virginia.
Health-Related Quality-of-Life Measures
All data from the original prospective study were collected using standardized forms and questionnaires. Demographic parameters included age and sex. Health-related quality-of-life (HRQOL) scores were assessed using a variety of instruments, including the modified Japanese Orthopedic Association (mJOA) scale23 and the Neck Disability Index (NDI).24
Radiographical parameters were measured using the SpineView software (Laboratory of Biomechanics, ENSAM, Paris, France; Figure 1). Calibration for linear measurements was directly calculated from the information contained within the DICOM tags that accompanied images from each contributing institution. Digitalization of each vertebral endplate on coronal and sagittal radiographs, as well as the posterior walls of the vertebral bodies from T1 to C2 and the 2 external auditory canals on sagittal radiographs, permitted calculation of the following radiographical parameters.3,4
- Sagittal parameters:
- Sagittal vertical axis (SVA): horizontal offset between a chosen plumbline and the posterosuperior corner of C7. Measured using plumblines from the barycenter of C1 (C1–C7 SVA), the barycenter of C2 (C2–C7 SVA), and the center of gravity of the head, taken as the midpoint of the line between the 2 external auditory canals (center of gravity–C7 SVA)
- C2 tilt: the angle between the posterior aspect of C2 (dens) and the vertical; (−) for posterior inclination and (+) for anterior inclination
- C2 slope: angle between the inferior endplate of C2 and a horizontal reference line
- C7 slope: angle between the superior endplate of C7 and a horizontal reference line
- T1 slope: angle between the superior endplate of T1 and a horizontal reference line
- C2–C7 Cobb angle: sagittal cervical curvature from C2 to C7, using the Cobb method; (+) for lordosis and (−) for kyphosis
- C2–C7 Harrison angle: sagittal cervical curvature from C2 to C7, using Harrison method,3; (+) for lordosis and (−) for kyphosis
- T1 slope minus C2–C7 Cobb angle
- T1 slope minus C2–C7 Harrison angle
- Posterior length: summation of the lengths of the posterior aspects of the vertebral bodies and disk heights from the inferior endplate of C7 to the inferior endplate of C2
- Anterior length: summation of the lengths of the anterior aspects of vertebral bodies and disk heights from the inferior endplate of C7 to the inferior endplate of C2
- Anterior length/posterior length: anterior length divided by posterior length
- Coronal parameters:
- C2–C7 coronal Cobb angle: coronal curvature from C2 to C7, using the Cobb method
- C2–C7 plumbline: horizontal offset between a plumbline dropped from the barycenter of the C2 vertebral body and the center of the inferior endplate of C7, with (+) and (−) values reflecting offset to the right and left, respectively.
Preoperative magnetic resonance images were loaded into a custom version of Surgimap Spine (Nemaris Inc., New York, NY). Calibration for linear measurements was directly calculated from the information contained within the DICOM tags that accompanied images from each contributing institution. The external border of the spinal cord was outlined from C2 to T1, based on T2-weighted images, with reference to other available corresponding axial image sequences to help mitigate the potential augmentation effects of MRI that can lead to overestimation of compression. Although the number of contours (i.e., measurements) used to define the spinal cord for each patient was dependent on the MRI slice thickness and interval, analysis for each subject included at a minimum 1 contour per intervertebral disc and 2 contours per vertebral level. The coordinate of each digitalized point of each contour was then exported to a dedicated Matlab (MathWorks Inc., Natick, MA) function, and the following calculations were performed for each patient:
- Three-dimensional (3D) reconstruction of the spinal cord:
- On the basis of the information contained in the DICOM files (i.e., DICOM tags), 4 × 4 transformation matrices were calculated to transpose the 2-dimensional original contours (Figure 2A) into 3D contours (Figure 2B) (i.e., from the image coordinate system to the patient coordinate system).
- A 3D spline passing through the barycenter of each 3D contour was created to define the local orientation of the spinal cord (Figure 2C).
- Each 3D contour was then projected onto a plane originating at its barycenter and perpendicular to the 3D spline.
- Finally, the external envelope of the spinal cord was defined by a set of 100 vertical splines passing through the edge of each 3D contour (Figure 2D).
- Spinal cord measurements:
- For each 3D contour slice, the following parameters were calculated: cross-sectional area, anteroposterior distance, and lateral distance.
- Using an integration method, the volume of the spinal cord and the surface area of the external envelope were calculated from the C2–C3 disc to the C7–T1 disc.
- In an effort to take into account variability in size between patients, MRI measurements were then normalized by dividing the length of the upper endplate of C7.
Descriptive statistics were calculated for demographic characteristics, HRQOL scores, and radiographical and MRI parameters. Pearson correlations were calculated between the HRQOL instruments and between the HRQOL scores and sagittal radiographical measurements and MRI parameters. Correlations within radiographical parameters and within MRI parameters were also calculated, as were correlations between these 2 sets of measurements. Finally, patients were stratified on the basis of whether their C2–C7 Cobb angle demonstrated kyphosis or lordosis. Differences between the 2 groups in MRI parameters were assessed, and correlations between HRQOL scores and MRI parameters within each group were calculated. Results were considered significant at P < 0.05.
A total of 56 subjects from the CSM database met the inclusion criteria for this study (Table 1). The average age of the included patients was 55.4 years, and 60.7% of the sample was male (n = 34). The mean duration of symptoms prior to surgical intervention was 27.7 months.
The mJOA scale ranges from 0 (worst) to 18 (best); no subject reported a preoperative score lower than 5, and only 3 patients reported a score of 18. The NDI scale ranges from 0 (best) to 100 (worst); 2 subjects reported a preoperative score of 0, and no subjects reported a score of 100. The average preoperative HRQOL instrument scores for the 56 subjects in this study were 13.2 (SD = 2.9) for the mJOA score and 40.9 (SD = 20.6) for the NDI (Table 1). The NDI correlated significantly with mJOA (r = −0.386, P < 0.01). Neither the mJOA score nor the NDI correlated significantly with the duration of symptoms or any comorbidities in the data set, including the presence of diabetes.
Preoperative radiographical measurements in the sagittal and coronal planes are summarized in Tables 2 and 3. The mean C2–C7 SVA for the entire group was 32 mm, and the mean C2–C7 cervical lordosis was 6.5° when measured by the Cobb method and 13.2° when measured by the Harrison method. Kyphotic alignment of the cervical spine was observed in 30% of the patients.
The mJOA score was found to correlate negatively with C2–C7 SVA (r = −0.282, P = 0.035) and C1–C7 SVA (r = −0.286, P = 0.033), as well as with C2 tilt (r = −0.272, P = 0.043) and C2 slope (r = −0.281, P = 0.036). The mJOA score also correlated weakly with T1 slope minus C2–C7 Cobb angle (r = −0.234, P = 0.083). The mJOA score was not found to correlate significantly with center of gravity–C7 SVA, C2–C7 Cobb angle, or the posterior or anterior length of the spinal column. A summary of correlations between mJOA scores and sagittal radiographical parameters is provided in Table 4. The NDI was found to correlate negatively with the anterior length of the spinal column (r = −0.274, P = 0.022), but it was not found to correlate significantly with any other radiographical parameters (Supplementary Digital Content Table 2, available at http://links.lww.com/BRS/A833).
Within the radiographical parameters, C2–C7 SVA correlated with T1 slope minus C2–C7 Cobb angle (r = 0.568, P < 0.001), as well as with the anterior (r = 0.231, P = 0.043) and posterior (r = 0.251, P = 0.031) lengths of the cervical spine (see Supplementary Digital Content Table 3, available at http://links.lww.com/BRS/A833). In addition, the anterior length of the cervical spine correlated with C2–C7 Cobb angle (r = 0.316, P = 0.009) and the posterior length of the cervical spine (r = 0.932, P < 0.001). The ratio between the anterior and posterior lengths of the cervical spine demonstrated correlation with the following:
- C2 tilt (r = −0.322, P < 0.05)
- C2, C7, and T1 slopes (r = −0.544, 0.577, and 0.628; all Ps < 0.001)
- C2–C7 Cobb angle (r = 0.968, P < 0.001) and C2–C7 Harrison angle (r = 0.852, P < 0.001)
- T1 slope minus C2–C7 Cobb angle (r = −0.535, P < 0.001).
Preoperative MRI measurements (Table 5) revealed that more variability existed among patients for spinal cord volume than for spinal cord length, as measured by the coefficient of variation (SD/mean). This finding was also demonstrated for the normalized spinal cord measurements (Table 6).
Within the MRI measurements, cord volume correlated with cord length (r = 0.472, P < 0.001) and cord average cross-sectional area (r = 0.957, P < 0.001) (see Supplementary Digital Content Table 4, available at http://links.lww.com/BRS/A833). Between MRI and radiographical measurements, the only significant correlations involved the anterior and posterior cervical spine lengths as measured on radiopgraphs: with MRI cord length (anterior: r = 0.663, P < 0.001; posterior: r = 0.751, P < 0.001), cord volume (anterior: r = 0.458, P < 0.001; posterior: r = 0.425, P < 0.01), and mean cord cross-sectional area (anterior: r = 0.289, P < 0.05; posterior: r = 0.228, P < 0.05). As illustrated in Figure 3, patients with similar radiographical parameters and mJOA scores can have very different MRI parameters.
On the basis of the full set of data, no correlations were found between MRI measurements of spinal cord length, volume, mean cross-sectional area, or surface area and HRQOL scores (see Supplementary Digital Content Table 5, available at http://links.lww.com/BRS/A833). Patients were subsequently grouped on the basis of whether they demonstrated a lordotic (n = 39, mean C2–C7 Cobb angle = 13°) or kyphotic (n = 17, mean C2–C7 Cobb angle = −8°) cervical curvature (Table 7). There was no significant difference in terms of NDI scores between patients with lordotic (mean NDI = 39.8 ± 17) and kyphotic (mean NDI = 43.2 ± 27.3) cervical spine alignment (P = 0.642). As shown in Table 8, for patients with lordotic cervical spine, the mJOA score correlated positively with the normalized spinal cord volume (r = 0.366, P = 0.022), normalized spinal cord external area (r = 0.399, P < 0.05), normalized mean cross-sectional spinal cord area (r = 0.345, P = 0.031), and normalized mean lateral distance (r = 0.402, P = 0.011). In contrast, for patients with kyphotic cervical spine, the mJOA score correlated negatively with the normalized spinal cord volume (r = −0.496, P = 0.043), normalized mean cross-sectional spinal cord area (r = −0.535, P = 0.027), and normalized mean lateral distance (r = −0.497, P = 0.043). Representative case examples of lordotic and kyphotic cervical alignment and associated MRI measurements and mJOA scores are shown in Figure 4.
To our knowledge, this is the first study to correlate cervical sagittal balance (C2–C7 SVA) to myelopathy severity. It is interesting to note that although cervical translational alignment (C2–C7 SVA) was correlated to the mJOA score, the cervical C2–C7 Cobb angle (lordosis/kyphosis) was not correlated to the mJOA score. Previous work by Tang et al25 correlated outcomes in patients undergoing posterior cervical fusion to the same C2–C7 SVA parameter, although that study contained only postoperative patients and represented a mixed population of indications including primary cervical deformity. This finding would seem to substantiate the in vitro work by Chavanne et al14 and others,15,16 who found that increased cord intramedullary pressures were correlated to increased cervical SVA. The study of Chavanne et al14 also found increased prevalence of elevated cord pressures beyond 7.5° of kyphosis (38%) and beyond 21° of kyphosis (100%).
Although kyphosis was not correlated to mJOA scores in this study of preoperative patients, we did find a moderate negative correlation in kyphotic patients of normalized cord volume and normalized cord cross-sectional area to mJOA scores. It is very interesting to note that the opposite (positive correlations) was found for lordotic patients. The reason for this difference is unclear, but both correlation values were moderately strong. This unexpected finding raises many possible explanations that may serve as starting points for future investigations. The difference suggests a relationship of normalized cord volume to myelopathy that differs on the basis of alignment. In addition, the nature of compressing material (hard vs. soft) and the variability of vascular response to any compression could also have a significant role in the development of neurological sequelae.
Again, considering the previous work of Chavanne et al,14 it seems reasonable to postulate that given some elasticity and cord redundancy, morphological changes in the cord due to kyphosis-induced tension would occur only after certain threshold alignment values at which cord redundancy may be exceeded and cord elasticity is maximized. Concomitant compression due to osteophytes and other spondylotic changes may also impact these threshold values in individual patients.
Alternatively, it is possible that these differences may result from an as-of-yet unrecognized artifact of imaging or analysis. For example, in kyphosis, the spinal cord is pushed anteriorly in the spinal canal, leading to anterior cord compression. This compression could result in the opening of the anteromedian fissure that could artificially increase the apparent cross-sectional volume.
By establishing these relationships in the preoperative condition, without the variable of surgical intervention and outcome, we can better understand the isolated effect of alignment and cord morphology on myelopathy. It seems that cervical sagittal balance (C2–C7 SVA) and normalized cord volume and area will be the key parameters to investigate in evaluating the effect of alignment changes in the surgical treatment of myelopathy. Furthermore, it seems that these morphological parameters may have different correlations in myelopathic patients with concomitant cervical deformity. Investigation of the correlations between changes in these parameters and mJOA scores may help demonstrate how alignment changes impact the structure and function of the cervical spinal cord in vivo.
Although this study does not demonstrate a correlation between preoperative kyphosis and myelopathy severity, previous reports have suggested potential impact of cervical kyphosis on myelopathy symptoms and outcomes with surgery.7,19–21,26,27 Nakanishi et al27 and Kawaguchi et al26 describe case reports of patients with cervical kyphosis and myelopathy resulting from primary dropped head syndrome with extreme kyphotic angles that after surgical correction show substantial improvement in myelopathy. Watanabe et al7 reported a series of 12 young patients (ranging from 12 to 22 yr of age) with cervical flexion myelopathy that improved after surgical correction. It is possible that the apparent link between kyphosis and myelopathy symptoms in these reports, which contrasts with the findings in the present study, may reflect differing underlying pathologies, because the present study focused specifically on adults with CSM and compressive cord pathology.
Two previous reports have also noted a lack of correlation between cervical kyphosis and severity of myelopathy among patients with CSM. Uchida et al20 assessed 43 patients with CSM and found no significant correlation between the preoperative kyphotic angle and the preoperative JOA score. They attributed this lack of correlation to the many potential confounding factors for each patient, including age, duration of symptoms, irreversible changes in the spinal cord, and static and dynamic canal stenosis including segmental instability that could impact myelopathy severity.20,28 In a large series of patients with CSM treated with laminoplasty (n = 103), Kawakami et al19 found no difference in mean JOA scores at follow-up among patients with lordotic, straight, or kyphotic spine.
Although spinal cord dimensions did not correlate significantly with mJOA scores, except when patients were stratified on the basis of kyphotic versus lordotic alignment, a recent report from Arvin et al11 does suggest that preoperative spinal cord signal change on MRI correlates with neurological status at baseline and preoperative recovery. Specifically, the authors demonstrated that low T1 signal, focal increased T2 signal, and segmentation of T2 signal changes were MRI indicators of poorer outcomes.
The primary limitation of this study is the retrospective design, although the data on which the study is based are derived from a prospectively collected patient series. This study includes only patients with CSM who were deemed surgical candidates, and the protocol did not include dynamic MRI studies, which could demonstrate compressive pathology that may not be readily apparent on static images. In addition, this study used assessment of cervical sagittal alignment based on standing radiographs, whereas spinal cord measurements were based on supine MRI studies. It is possible that differences in spinal cord morphology between the standing and supine positions could have confounded the analyses in this study; however, the scenario assessed (standing radiographs and supine magnetic resonance images) reflects the clinical assessment of CSM. Although not specifically assessed in this study, it is also possible that segmental instability could contribute to CSM. Because the prospective study on which these data are based did not require upright sagittal imaging of the spine beyond the cervical region, potential variables related to thoracolumbar posture, which have recently been shown to have potential impact on cervical alignment,5 could be assessed. Furthermore, it is important to recognize that this work is an exploratory study and further studies will be necessary to validate these results. Strengths of this study include the novel quantitative techniques used for spinal cord assessment, standardizing imaging analysis performed at a single center, and the use of prospectively collected, multicenter patient data.
CSM is the leading cause of spinal cord dysfunction worldwide. To date, the correlations between cervical alignment, sagittal balance, and myelopathy have not been well characterized. This study is the first to correlate cervical sagittal balance (C2–C7 SVA) to myelopathy severity. It is interesting to note that that sagittal balance but not kyphosis is tied to myelopathy score. Although the cervical C2–C7 Cobb angle (lordosis/kyphosis) was not correlated to mJOA scores, we did find a moderate negative correlation in kyphotic patients of normalized spinal cord volume and normalized cord cross-sectional area to mJOA scores. Notably, the opposite (positive correlation) was found for lordotic patients, suggesting a relationship of normalized cord volume to myelopathy that differs on the basis of sagittal cervical alignment. Further study is warranted to establish the basis for these opposite correlations. Establishing key threshold alignment values beyond which correction of the deformity would result in improved myelopathy outcomes will be the important focus of future investigation.
Summary Statements. This is the first study to correlate sagittal balance (C2–C7 SVA) to myelopathy severity. We found a moderate negative correlation in kyphotic patients of cord volume and crosssectional area to mJOA scores. The opposite (positive correlation) was found for lordotic patients, suggesting a relationship of cord volume to myelopathy that differs on the basis of sagittal alignment.
- CSM is the leading cause of spinal cord dysfunction worldwide. Correlations between cervical alignment, sagittal balance, and myelopathy have not been well characterized.
- Novel techniques were developed to determine in vivo spinal cord dimensions based on MRI and applied and correlated to preoperative alignment, myelopathy, and disability scores in patients with CSM.
- This study is the first to correlate cervical sagittal balance (C2–C7 SVA) to myelopathy severity based on the mJOA score.
- More variability existed among patients for spinal cord volume than for spinal cord length, as measured by the coefficient of variation (SD/mean). This finding was also demonstrated for normalized spinal cord measurements.
- Patients with cervical kyphosis had a moderate negative correlation of normalized cord volume and normalized cord cross-sectional area to mJOA scores. The opposite (positive correlation) was found for lordotic patients, suggesting a relationship of normalized cord volume to myelopathy that differs on the basis of sagittal alignment.
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1. Fehlings MG, Wilson JR, Kopjar B, et al. Efficacy and safety of surgical decompression in patients with cervical spondylotic myelopathy: results of the AOSpine North America prospective multi-center study. J Bone Joint Surg [Am] In press.
2. Nurick S. The pathogenesis of the spinal cord disorder associated with cervical spondylosis. Brain 1972;95:87–100.
3. Scheer JK, Tang J, Smith JS, et al. Cervical spine alignment: a comprehensive review. J Neurosurg Spine In press.
4. Ames CP, Blondel B, Scheer JK, et al. Cervical Radiographical Alignment: Comprehensive Assessment Techniques and Potential Importance in Cervical Myelopathy. Spine 2013;38:S149–60.
5. Smith JS, Shaffrey CI, Lafage V, et al. Spontaneous improvement of cervical alignment after correction of global sagittal balance following pedicle subtraction osteotomy. J Neurosurg Spine 2012;17:300–7.
6. Cabraja M, Abbushi A, Koeppen D, et al. Comparison between anterior and posterior decompression with instrumentation for cervical spondylotic myelopathy: sagittal alignment and clinical outcome. Neurosurg Focus 2010;28:E15.
7. Watanabe K, Hasegawa K, Hirano T, et al. Anterior spinal decompression and fusion for cervical flexion myelopathy in young patients. J Neurosurg Spine 2005;3:86–91.
8. Liu H, Li Y, Chen Y, et al. Cervical curvature, spinal cord MRI T2 signal, and occupying ratio impact surgical approach selection in patients with ossification of the posterior longitudinal ligament. Eur Spine J 2013;22:1480–8.
9. Yagi M, Ninomiya K, Kihara M, et al. Long-term surgical outcome and risk factors in patients with cervical myelopathy and a change in signal intensity of intramedullary spinal cord on magnetic resonance imaging. J Neurosurg Spine 2010;12:59–65.
10. Karpova A, Arun R, Davis AM, et al. Predictors of surgical outcome in cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2013;38:392–400.
11. Arvin B, Kalsi-Ryan S, Mercier D, et al. Pre-operative MRI imaging is associated with baseline neurological status and can predict postoperative recovery in patients with cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2013;38:1170–6.
12. Shimizu K, Nakamura M, Nishikawa Y, et al. Spinal kyphosis causes demyelination and neuronal loss in the spinal cord: a new model of kyphotic deformity using juvenile Japanese small game fowls. Spine (Phila Pa 1976) 2005;30:2388–92.
13. Takenouchi T, Setoguchi T, Yone K, et al. Expression of apoptosis signal-regulating kinase 1 in mouse spinal cord under chronic mechanical compression: possible involvement of the stress-activated mitogen-activated protein kinase pathways in spinal cord cell apoptosis. Spine (Phila Pa 1976) 2008;33:1943–50.
14. Chavanne A, Pettigrew DB, Holtz JR, et al. Spinal cord intramedullary pressure in cervical kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976) 2011;36:1619–26.
15. Farley CW, Curt BA, Pettigrew DB, et al. Spinal cord intramedullary pressure in thoracic kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976) 2012;37:E224–30.
16. Winestone JS, Farley CW, Curt BA, et al. Laminectomy, durotomy, and piotomy effects on spinal cord intramedullary pressure in severe cervical and thoracic kyphotic deformity: a cadaveric study. J Neurosurg Spine 2012;16:195–200.
17. Hsieh PC, Ondra SL, Grande AW, et al. Posterior vertebral column subtraction osteotomy: a novel surgical approach for the treatment of multiple recurrences of tethered cord syndrome. J Neurosurg Spine 2009;10:278–86.
18. Hsieh PC, Stapleton CJ, Moldavskiy P, et al. Posterior vertebral column subtraction osteotomy for the treatment of tethered cord syndrome: review of the literature and clinical outcomes of all cases reported to date. Neurosurg Focus 2010;29:E6.
19. Kawakami M, Tamaki T, Ando M, et al. Relationships between sagittal alignment of the cervical spine and morphology of the spinal cord and clinical outcomes in patients with cervical spondylotic myelopathy treated with expansive laminoplasty. J Spinal Disord Tech 2002;15:391–7.
20. Uchida K, Nakajima H, Sato R, et al. Cervical spondylotic myelopathy associated with kyphosis or sagittal sigmoid alignment: outcome after anterior or posterior decompression. J Neurosurg Spine 2009;11:521–8.
21. Zdeblick TA, Bohlman HH. Cervical kyphosis and myelopathy. Treatment by anterior corpectomy and strut-grafting. J Bone Joint Surg Am 1989;71:170–82.
22. Fehlings MG, Smith JS, Kopjar B, et al. Perioperative and delayed complications associated with the surgical treatment of cervical spondylotic myelopathy based on 302 patients from the AOSpine North America Cervical Spondylotic Myelopathy Study. J Neurosurg Spine 2012;16:425–32.
23. Benzel EC, Lancon J, Kesterson L, et al. Cervical laminectomy and dentate ligament section for cervical spondylotic myelopathy. J Spinal Disord 1991;4:286–95.
24. Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity. J Manipulative Physiol Ther 1991;14:409–15.
25. Tang JA, Scheer JK, Smith JS, et al. The impact of standing regional cervical sagittal alignment on outcomes in posterior cervical fusion surgery. Neurosurgery 2012;71:662–9; discussion 669.
26. Kawaguchi A, Miyamoto K, Sakaguchi Y, et al. Dropped head syndrome associated with cervical spondylotic myelopathy. J Spinal Disord Tech 2004;17:531–4.
27. Nakanishi K, Taneda M, Sumii T, et al. Cervical myelopathy caused by dropped head syndrome. Case report and review of the literature. J Neurosurg Spine 2007;6:165–8.
28. Uchida K, Nakajima H, Sato R, et al. Multivariate analysis of the neurological outcome of surgery for cervical compressive myelopathy. J Orthop Sci 2005;10:564–73.