Analysis of global spine sagittal parameters in cervical spondylotic patients and asymptomatic subjects

Background: Degenerative changes associated with cervical spondylotic can result in a change of normal sagittal alignment, and this may be the initial change of kyphosis and sagittal imbalance. Few studies have analyzed the correlations between the cervical spine lordosis and global spine balance in patients with cervical spondylotic. This study is applied to investigate the characteristics and relationships of cervical and global sagittal parameters in normal adults and cervical spondylotic patients. Methods: We reviewed 46 asymptomatic control subjects (normal group, NG) and 48 cervical spondylotic patients (cervical spondylotic group, CSG), who had both cervical MRI and global radiographs obtained together, between January 2016 and September 2018. Data includes C1-2 angle, C2–7 lordosis (CL), T1 slope (T1S), thoracic inlet angle (TIA), C2–7 sagittal vertical axis (CSVA), sagittal vertical axis(SVA), thoracic-kyphosis(TK), thoracic-lumbar lordosis(TL), lumbar lordosis (LL), pelvic incidence (PI), pelvic tilt (PT) and sacral slope (SS). The values were presented as the mean ± standard deviation. Student t-test and Pearson’s correlation coefﬁcient were used for statistical analysis. Probability values less than 0.05 were considered statistically signiﬁcant. Results:

to abnormal cervical spine biomechanics and loss of normal sagittal alignment. Abnormalities of the cervical sagittal alignment, in return, could contribute to spinal cord dysfunction [1].On the other hand, neck pain and functional disability could be caused by loss of cervical lordosis [2].
Lee found a significant sequential relationship between C2-7 angle and T1 slope in asymptomatic volunteers without the history of symptoms related to the whole spine [3]. In Kim's study, nearly onefourth of the asymptomatic participants (26.3%) have kyphotic cervical posture and no statistically significant correlations were found among cervical kyphosis and the global spine parameters (TK, LL, SS, PT, and PI) [4]. One study showed that C2-7 angle was the only predictor of CSVA in patients with cervical spondylotic myelopathy. Age combined with CSVA could predict the severity of myelopathy [1]. In one analysis of cervical and global spine alignment in Chinese cervical spondylotic patients and asymptomatic subjects, the authors found that the percentages of cervical lordosis were 28.3 % and 36.4 % in asymptomatic and spondylotic group and cervical angles were significantly related to the thoracic kyphosis [5]. One study reviewed the characteristics of cervical sagittal parameters in 50 healthy cervical spine adults and 50 patients with cervical disc degeneration. They found that T1S was involved in the occurrence and development of cervical disc degeneration, and TIA could be considered as a constant morphological parameter in both the normal population and cervical disc degeneration patients [6]. Yoon Ha reported that changes in the balance of the thoracolumbar spine caused reciprocal changes in cervical spine alignment. Cervical spine alignment may depend on changes in regional anatomic curvatures (thoracic or lumbar) and sagittal alignment [7].
The interaction between thoracic, lumbar spine and pelvis has been well documented in publications during the past decade [8,9]. However, there is little research on the comparison of full-spine sagittal parameters between patients with cervical spondylosis and healthy adults. Moreover, the correlation between the parameters is not clear.
Therefore, we prospectively observed the radiological characteristics of the cervical spine in 46 normal people and 48 cervical spondylotic patients, then analyzed the relationship between cervical and global spine alignment parameters.
Materials And Methods 4 A retrospective analysis was performed of data from 46 normal control subjects whose cervical spine are healthy (normal group, NG) and 48 patients with cervical spondylosis (cervical spondylosis group, CSG), who visited the outpatient department or physical examination center of our hospital between January 2016 and September 2018. Each individual had both a full-length spine lateral X-ray radiographs and cervical MRI scans( Fig. 1 and Fig . 2).
Inclusion criteria of NG Enrolled asymptomatic volunteers whose ages are between 20 and 40 years and no history of diagnosis or treatment related to any part of the spine. No evidence of cervical spondylosis with clinical manifestations, physical examination, and MRI scan. Data including C1-C2 angle ,C2-7 lordosis (CL), T1 slope (T1S), thoracic inlet angle (TIA), C2-7 sagittal vertical axis (CSVA), TL, TK, LL, PI, PT, SS and SVA on radiographs were collected and analyzed.

Cervical sagittal parameters (Fig. 3)
C1-C2 angle: an angle between C1 and the C2 lower endplate was measured using the Cobb method.

Discussion
The global spine lateral radiograph is a key image to evaluate global spinal sagittal alignment.
Previous studies have attempted to find out the relationship between the cervical spine sagittal parameters and global spine sagittal parameters, but do not form a unified opinion [1,10,11].
Usually, we use the C2-C7 angle to represent cervical lordosis(CL), but the relationship between cervical degeneration and cervical lordosis has been controversial. Wang observed no significant difference in the C2-7 angle between the normal group and the degenerative cervical spondylolisthesis group [12]. Generally speaking, the presence of a kyphotic cervical alignment may indicate substantial deformity and be linked to poor clinical outcomes. But in an author's report, 29% of patients without cervical complaints have kyphotic cervical alignment. Kyphotic alignment of the cervical spine cannot alone define cervical deformity [10,13]. Kim's report showed that nearly onefourth of asymptomatic people have kyphotic cervical posture [4]. Yoshida's study demonstrated that the pathology of the responsible lesion was related to global sagittal balance but not regional cervical alignment, which might be due to compensation against global malalignment during aging [11]. On the other hand, the C2-7 angle increased with age in the normal population [14,15]. In our study, the cervical lordosis in CSG is higher than NG(11.87 ± 6.99 VS 8.18 ± 9.06 P < 0.05) and the age of the CSG is also higher than NG(57.91 ± 9.58VS 28.00 ± 8.09 P < 0.01). Therefore, we speculate that age combined with cervical lordosis reflects the disease status of cervical spondylosis.
Sang-Hun Lee found that no significant relationship between CL and TK in seventy-seven asymptomatic volunteers without the history of symptoms (p=-0.154) [3]. Also, Our study suggests that CL and TK are not related in the NG(P = 0.119). Bassel found that as thoracic kyphosis increased, the amount of lower cervical lordosis increased in patients with a diverse range of thoracolumbar pathologies [13]. Jeffrey 's study revealed there was a significant association between the thoracic kyphosis and cervical lordosis for females (r = 0:33, P < 0.001), and for males (r = 0:27, P < 0.03) in post-mortem lateral spinal radiographs [15]. In our study, CL has positively correlated with TK(r = 0.335 P < 0.05) in CSG. It may be that cervical spondylosis changes the relationship between CL and TK. Cervical lordosis could increase as a compensatory reaction against sagittal imbalance or hyperthoracic kyphosis in with adult spinal deformity [10].
As a key vertebra, T1 joins the cervical and thoracic vertebra, fixed on both sides of the ribs not altered by position. Therefore, T1S parameter may provide a reference value for determining the correction of the sagittal balance of the cervical spine [16]. Also, T1S was involved in the occurrence and development of cervical disc degeneration [6]. In our study, CL is influenced by T1S(r = 0.382 in NG and r = 0.433 in CSG respectively P < 0.01). T1S exhibited a significant correlation with CL in previous research [3,[16][17][18]. Rong found that T1S positively correlated to CL patients with cervical disc degeneration. Lower T1S decreased the CL to obtain a sagittally balanced cervical spine and led to a relatively straight cervical spine [6]. T1S is the site that mainly bears the stress from the head weight. Long-term exposure to the stress could result in T1 tilting forward. To maintain a horizontal gaze, CL would increase along with the increased T1S in a compensatory manner [3]. In our study, T1S has a positive relation with TK, CSVA ,and SVA in CSG. As T1 slope is the angle between T1 and the global horizontal line, T1 slope becomes greater when thoracic kyphosis becomes greater or positive sagittal imbalance becomes larger [10,13].
In our study, the mean TIA of the NG and CSG were 67.32 ± 7.81 and 68.18 ± 7.45, similar to data in the previous study that the mean TIA of the NG and DG were 70.22 ± 6.8 and 71.5 ± 8.0, respectively.
There were no significant differences in the TIA between the two groups in our study, indicating that TIA was not involved in the development of cervical disc degeneration, which could be considered a constant parameter of approximately 70°. TIA could be considered as a constant morphological parameter in the normal population and cervical disc degeneration patients [6].TIA concerning cervical sagittal balance may be as important as pelvic incidence in lumbar lordosis [3]. There were positive correlations between TIA and T1S (r = 0.475) in Xing's study. [6] In our study, TIA has positively correlated with T1S in the two groups (r = 0.376 and r = 0.416). TIA is a more important parameter than TK and that it influences cervical spine sagittal balance to achieve physiologic posture with horizontal gaze in the spine without sagittal imbalance [3].
CSVA is an important parameter for evaluating cervical sagittal balance. According to the previous studies, the CSVA values in asymptomatic normal volunteers are maintained in a tight range within 20 mm [11,19]. In Yuan's report, the mean CSVA value in patients with CSM was 17.2 ± 12.1 mm, within the normal value, indicating that most patients with CSM before surgery presented normal sagittal balance [1]. These are different from our findings. In our report, there is no difference in C2-7 SVA between NG and CSG(21.89 ± 11.44 mm VS 21.81 ± 12.70 mm P > 0.05). In the normal group, the value of CSVA is also higher than that reported in the previous literature. We suspect that a considerable number of people in the asymptomatic group also have a cervical sagittal imbalance, which requires further research in the future. In Rong's report, C2-7 lordosis was correlated with CSVA in the normal group(r=-0.482 P < 0.01) [6]. In Yuan's report, C2-7 lordosis was also correlated with CSVA in patients with cervical spondylotic myelopathy (r=-0.395, p = 0.001) [1]. Kwon also reported that C2-7 lordosis was significantly correlated CSVA in patients with spondylotic myelopathy and/or radiculopathy for ossification of the posterior longitudinal ligament and degenerative disc disorders.
(r=-0.631, P < .001) [20]. These above studies are the same as the results of our study. In our study, C2-7 lordosis was negatively correlated with CSVA in NG and CSG (r=-.062 and r=-0.309, P < 0.05). It means an excessively large CSVA that caused cervical spine decompensation would contribute to an imbalance in the cervical spine [1]. CSVA should be corrected by surgeons to improve the clinical outcomes when treating CSM. The restoration of C2-7 lordosis is critical to achieving a satisfactory CSVA [20].
The development of cervical spondylotic is a dynamic process. Accordingly, it is practical to assess each patient based on the individual conditions of global sagittal balance and regional alignment.
[21]Now more researches reported that cervical lordosis has less related to spinopelvic parameters.
Lee found no direct correlation between pelvic parameters and thoracic or cervical spine alignment [12]. Kim found no statistically significant correlations were found among cervical kyphosis and the global spine parameters [4]. Miao found that the cervical angles were related to thoracic angles, but not with the lumbar angles. They conclude that the cervical alignment is more liable to be influenced by the local parameters as an independent degenerative disease but is seldom influenced by the global spinal degeneration [5]. These results agree with our current research. In our study, CL has no relation with LL, PT, SS PT and SVA. In our opinion, cervical lordosis is mainly affected by cervical and thoracic parameters such as T1S, TIA, and TK, but not by lumbar-pelvic parameters.
There are some limitations in this study. Firstly, due to the small sample size, we are unable to further group according to the level of cervical spondylotic. Secondly, this study lacked scores like JOA and NDI. Our next work is to explore the relationship between JOA and NDI and the sagittal balance of the whole spine.

Conclusion
Cervical spondylosis causes changes in sagittal parameters of the cervical and thoracic spine but does not affect on lumbar and pelvic parameters. TIA could be considered as a constant morphological parameter in the normal population and cervical spondylotic. The study design was approved by the Ethical Committee of Shanghai General Hospital, Shanghai Jiao Tong University . All of the participants provided written informed consent.

Consent for publication
Not applicable.

Availability of data and materials
All data generated or analyzed during this study are included in this published article and its additional files.

Competing interest
We declare that we do not have any competing interests.

Funding
We declare that we do not have any Funding support.

Authors' contributions
Liang Zhu and Xiaojun Ma contributed to interpreting the data and writing the final manuscript. Bao Sun was responsible for the original data collection. Qiang Shen contributed to reviewing the accuracy of the data. Qiang Fu was in charge and contributed to all stages of the present study. All authors read and approved the final manuscript.  Cervical lateral X-ray C1-C2 angle: an angle between C1 and the C2 lower endplate was