Abstract
Study Design
Retrospective cohort study.
Objectives
The aim was to examine cervical spinal cord compression (SCC) in adult scoliosis and clarify the prevalence of and risk factors for cervical SCC.
Methods
This study included 270 adult scoliosis patients and 1211 healthy volunteers. Cervical SCC was evaluated on cervical magnetic resonance imaging (MRI). The rates of SCC for those with adult scoliosis and the healthy volunteers were compared. Logistic regression analysis was conducted to examine the factors associated with cervical SCC on MRI.
Results
In cases with adult scoliosis, preoperative major scoliosis curve was 56.0° ± 18.8°, and cervical SCC was detected in 25 patients (9.3%). Among the healthy volunteers, 64 cases with cervical SCC were detected. Only in cases with adult scoliosis, logistic regression analysis revealed higher age (OR 1.09, 95% CI 1.04–1.14, P < .001), narrow canal diameter (OR 2.27, 95% CI 1.35–3.85, P = .002), and inferior sagittal balance (OR 2.45, 95% CI 1.02–5.89, P = .04) as significant risk factors. In the logistic regression analysis in all subjects (including adult scoliosis and healthy volunteers), higher age (OR 1.08, 95% CI 1.06–1.10, P < .001) and narrow canal diameter (OR 1.62, 95% CI 1.37–1.92, P < .001) were also found to be significant risk factors, but the presence of scoliosis was not a significant factor.
Conclusions
Adult scoliosis itself was not significantly associated with cervical SCC. Inferior sagittal balance in addition to scoliosis constituted a significant risk factor for cervical SCC.
Keywords: adult spinal deformity, scoliosis, cervical spinal cord compression, magnetic resonance imaging, sagittal balance, cervical, alignment, age
Introduction
Adult spinal deformity (ASD) has increasingly become a global health concern due to the overall increased life expectancy observed in society. Adult spinal deformity consists of various pathologies, including adult idiopathic scoliosis (AdIS), adult degenerative scoliosis (ADS), kyphosis, posttraumatic spinal deformity, and iatrogenic deformity.1,2 ASD mainly affects the thoracic and thoracolumbar spine; however, cervical degenerative change can also progress, and cervical spinal stenosis can potentially coexist along with thoracolumbar deformities. Previous studies have reported that advanced cervical degenerative changes are seen on X-ray in ASD, and the prevalence of concurrent cervical spinal cord compression (SCC) is also high.3-5 Shimizu et al 3 investigated cervical magnetic resonance image (MRI) of patients with ASD and reported that the prevalence of concurrent SCC was relatively high at 33.8%. 3
These high rates of cervical SCC, however, included various pathologies in ASD, although the differences in the cervical SCC rates among the various pathologies in ASD were unclear. In particular, the effect of the existence of scoliosis on the cervical spine is uncertain. Adult idiopathic scoliosis is associated with the pathology of adolescent idiopathic scoliosis (AIS), and abnormalities in cervical alignment are manifested by alterations in the sagittal contour of the thoracolumbar spine especially in cases with AIS. Cervical and kyphotic alignments are recognized in 40%–89% cases.6-9 Such cervical alignment alterations can affect health-related quality of life in addition to the severity of scoliosis and can be accompanied by cervical SCC with age-related changes.
However, only a few studies have investigated how the thoracic or thoracolumbar scoliosis can affect cervical degeneration, and the clinical course of changes in the cervical spine in AIS in adulthood is still unclear. Furthermore, no studies have compared the cervical SCC in cases with adult scoliosis and healthy volunteers. Thus, the current study aimed to investigate cervical SCC in cases with adult scoliosis and clarify (1) whether the frequency of cervical SCC is higher than in healthy subjects, and (2) what the risk factors for cervical SCC may be. Our hypothesis was the adult scoliosis was a risk factor for cervical SCC as well as other deformities in ASD.
Methods
With respect to cases with adult scoliosis, prospectively collected data from a single center from August 2003 to March 2018 were retrospectively reviewed. Data were analyzed after obtaining approval from the Ethics Committee (approved number: 2019-0094). This study included adult scoliosis patients who were scheduled to undergo spinal corrective surgery for ASD. The enrollment criteria included age (≥20 years), magnitude of scoliosis (Cobb angle >40°), vertebral rotation (grade ≥1, Nash and Moe classification 10 ), and obtained preoperative cervical MRI. Patients with kyphosis without scoliosis, syndromic scoliosis, a history of previous spinal surgery, ankylosing spondylitis, mental disorders with medications, rheumatoid arthritis, other neurological diseases, or malignancies were excluded. In addition, patients from whom informed consent had not been received regarding the use of cervical MRI were also excluded. Finally, 270 consecutive patients (male/female, 27:243) with a mean age of 35.7 ± 18.0 years were included in the study. 178 cases (65.9%) had a history of suspected scoliosis at school checkups and/or brace treatment during adolescence.
As for healthy volunteers, a total of 1230 subjects were prospectively examined by cervical spine MRI and X-rays between February 2006 and February 2008.11,12 The subjects were relatively healthy volunteers without neurological symptoms. We recruited the subjects using newspaper advertisements and posters in facilities. The exclusion criteria included a history of brain or spinal surgery, spinal deformity, or comorbid neurologic disease. There were approximately 100 volunteers representing both sexes and each decade of life from the third to the eighth decade. There were 606 male subjects: 101 in their 20s, 104 in their 30s, 100 in their 40s, 99 in their 50s, 101 in their 60s, and 101 in their 70s. There were 605 female subjects: 100 in their 20s, 99 in their 30s, 100 in their 40s, 103 in their 50s, 103 in their 60s, and 100 in their 70s.
Radiographic Assessments
The cervical bony canal diameter was measured by anteroposterior diameter at the mid C5 vertebral body level in both adult scoliosis and healthy volunteers.
The healthy volunteers were recruited to evaluate cervical MRI and X-rays, and so the following parameters using standing whole spine sagittal images were examined only in cases with adult scoliosis: magnitude of scoliosis in the main curve, thoracic kyphosis (TK), lumbar lordosis (LL), pelvic tilt (PT), C7 sagittal vertical axis (SVA), C2–7 lordotic angle, and global spinal balance. The severity of the global spinal balance was evaluated based on the following criteria 13 :
Sagittal Balance Classification
Grade 1 = C7 SVA is in and behind the S1 endplate;
Grade 2 = C7 SVA is between the midpoint of the femoral head and the anterior edge of the S1 endplate;
Grade 3 = C7 SVA is in front of the midpoint of the femoral head.
Evaluation of SCC
The cervical SCC index 14 was used to evaluate the presence of cervical SCC. This index is the sum of the anterior and posterior compression points (0–3 points) at each disc level, and a grade >2 indicates the presence of cord compression (Figure 1).
Figure 1.
A representative case of a young adult with myelopathy: a comparative study between patients with cervical spondylotic spinal cord compression. 47-year-old female with scoliosis (Cobb angle: 80°). Although there were no myelopathic signs, her cervical MRI showed a spinal cord compression of Grade 3 at C5-6 (A). Her coronal and sagittal balance grades were 1 and 3, respectively, (B and C).
Anterior compression score
0 = No compression
1 = Disc bulging or ossification of the posterior longitudinal ligament with adequate cerebrospinal fluid (CSF) space
2 = No CSF space without cord compression
3 = Obvious cord compression
Posterior compression score
0 = No compression
1 = Enlargement of the ligamentum flavum with adequate CSF space
2 = No CSF space without cord compression
3 = Obvious cord compression
Compression score
Grade 0 = 0
Grade 1 = 1–2
Grade 2 = 3–4
Grade 3 = 5–6
Statistical Analysis
Each variable was reported as the mean ± standard deviation. T-test and one-way analysis of variance were used for group comparison. Logistic regression analysis was performed to investigate the factors associated with cervical SCC on MRI. Factors with P < .20 in the univariate analysis were included in the multivariate analysis. P < .05 was considered to be indicative of statistical significance in the multivariate analysis. All analyses were performed in SPSS software (version 27; SPSS Statistics, IBM Corp., Armonk, NY, USA).
Results
Cases with Adult Scoliosis
The preoperative major scoliosis curve was 56.0° ± 18.8°. The average PI-LL, PT, TK, C2–7 cervical lordosis angle, and C7 SVA were 6.4° ± 20.8°, 17.2° ± 11.2°, 19.41° ± 16.7°, −1.9° ± 16.0°, and 10.7 ± 44.3 mm, respectively. Sagittal balance grades 1, 2, and 3 were in 194 (71.9%), 42 (15.6%), and 34 (12.6%) cases, respectively. Coronal balance grades 1, 2, and 3 were in 213 (78.9%), 44 (16.3%), and 13 (4.8%) cases, respectively. Total balance grades 1, 2, and 3 were in 162 (60.0%), 99 (36.7%), and 9 (3.3%) cases, respectively.
Cervical SCC was found in 25 cases (9.3%), and the number of cases with cervical SCC significantly increased with age (P < .001), with 0, 1 (2.9%), 2 (14.3%), 6 (31.6%), 9 (27.3%), and 7 (38.9%) cases observed in the 20-, 30-, 40-, 50-, 60-, and 70-year age groups, respectively (Table 1). Furthermore, the number of cases with increased signal intensity also increased with age, with 0, 1 (2.9%), 1 (7.1%), 2 (10.5%), 4 (12.1%), and 2 (11.1%) cases observed in the 20-, 30-, 40-, 50-, 60-, and 70-year age groups, respectively (Table 1).
Table 1.
Comparison of radiographical parameters among age decades in cases with adult scoliosis.
| 20s | 30s | 40s | 50s | 60s | 70s | P | |
|---|---|---|---|---|---|---|---|
| Number of cases | 146 | 34 | 13 | 19 | 33 | 18 | |
| Canal diameter at C5 | 12.2 ± 1.2 | 12.2 ± 1.1 | 12.1 ± 0.6 | 12.3 ± 1.5 | 12.2 ± 1.4 | 12.1 ± 1.1 | .99 |
| Degree of scoliosis | 56.3 ± 18.4 | 65.8 ± 21.1 | 54.8 ± 13.3 | 62.4 ± 19.8 | 49.5 ±15.9 | 40.7 ± 10.4 | <.001* |
| LL | 49.8 ± 14.8 | 46.5 ± 15.7 | 38.1 ± 20.1 | 20.8 ± 14.7 | 20.5 ± 18.1 | 16.2 ± 15.4 | <.001* |
| PI-LL | −2.5 ± 15.7 | .3 ± 14.0 | 10.9 ± 16.5 | 27.8 ± 16.8 | 27.8 ± 19.0 | 29.7 ± 17.2 | <.001* |
| PT | 11.8 ± 6.6 | 12.4 ± 6.2 | 21.4 ± 7.9 | 28.5 ± 9.1 | 30.5 ± 11.4 | 31.5 ± 10.7 | <.001* |
| TK | 19.2 ± 16.4 | 20.8 ± 16.3 | 19.8 ± 12.3 | 16.1 ± 15.8 | 18.2 ± 19.4 | 19.6 ± 20.9 | .96 |
| C2-7 lordosis angle | −8.3 ± 11.9 | -2.4 ± 15.9 | 2.4 ± 17.4 | 8.1 ± 12.9 | 12.4 ± 16.7 | 13.0 ±16.2 | <.001* |
| Sagittal balance grade | 1.1 ± 0.4 | 1.2 ± 0.6 | 1.4 ± 0.6 | 2.1 ± 0.7 | 2.1 ± 0.8 | 2.4 ± 0.8 | <.001* |
| Spinal cord compression | 0 | 1 (2.9%) | 2 (15.4%) | 6 (31.6%) | 9 (27.3%) | 7 (38.9%) | <.001* |
| Increased signal intensity | 0 | 1 (2.9%) | 1 (7.1%) | 2 (10.5%) | 4 (12.1%) | 2 (11.1%) | .003* |
Abbreviations: LL, lumbar lordosis; PI, pelvic incidence; PT, pelvic tilt; TK, thoracic kyphosis.
As the age increased, LL (P < .001) decreased, whereas PI-LL (P < .001) and PT (P < .001) significantly increased (Table 1). In addition, the C2–7 lordosis angle also significantly increased (P < .001) with aging. Sagittal balance grade was found to worsen with aging (Table 1).
Healthy Volunteers
The individual data on cervical canal diameter on X-ray and cervical SCC on MRI were summarized in our previous studies.11,12 Cervical SCC was confirmed in 64 (5.3%) subjects on MRI, as shown in our previous study.11,12 SCCs were located at C3-4, C4-5, C5-6, and C6-7 in 11, 19, 39, and 26 subjects, respectively.11,12 Regarding cervical canal diameter, in total, 35 subjects (2.9%) were found to have narrow cervical canals (<13 mm).11,12
Risk Factors for Cervical SCC in Cases with Adult Scoliosis
Comparing cases with and without cervical SCC, it was observed that age was significantly higher (33.1 ± 16.5 and 61.2 ± 11.8 years old, P < .001) in cases with cervical SCC, and PI-LL (4.7° ± 20.0° and 23.8° ± 20.6°, P < .001), PT (16.0° ± 10.5° and 28.8° ± 11.4°, P < .001), and C2–7 lordosis angle (−3.0° ± 15.9° and 8.6° ± 13.7°, P = .001) were significantly greater in cases with cervical SCC (Table 2). Bony canal diameter at C5 (12.2 ± 1.2 and 11.5 ± .9 mm, P = .004) was significantly smaller in cases with cervical SCC (Table 2). Furthermore, sagittal (1.3 ± .6 and 2.2 ± .8, P < .001) balance grade was significantly worse in cases with SCC (Table 2).
Table 2.
Comparison between cases with and without spinal cord compression in cases with adult scoliosis.
| SCC (−) | SCC (+) | P | |
|---|---|---|---|
| Number of cases | 245 | 25 | |
| Age | 33.1 ± 16.5 | 61.2 ± 11.8 | <.001* |
| Canal diameter at C5 | 12.2 ± 1.2 | 11.5 ± 0.9 | .004* |
| Main Cobb angle | 56.8 ± 18.6 | 48.3 ± 19.5 | .03* |
| LL | 42.7 ± 19.5 | 23.0 ± 18.6 | <.001* |
| PI-LL | 4.7 ± 20.0 | 23.8 ± 20.6 | <.001* |
| PT | 16.0 ± 10.5 | 28.8 ± 11.4 | <.001* |
| TK | 19.0 ± 16.4 | 20.1 ± 19.9 | .75 |
| C2-7 lordosis angle | −3.0 ± 15.9 | 8.6 ± 13.7 | .001* |
| Sagittal balance grade | 1.3 ± 0.6 | 2.2 ± 0.8 | <.001* |
Abbreviations: SCC, spinal cord compression; LL, lumbar lordosis; PI, pelvic incidence; PT, pelvic tilt; TK, thoracic kyphosis. *Values are P < .05.
Logistic regression analysis showed that advanced age [odds ratio (OR), 1.09; 95% confidence interval [CI], 1.04–1.14; P < .001], narrow canal diameter (OR, 2.27; 95% CI, 1.35–3.85; P = .002), and worse sagittal balance grade (OR, 2.45; 95% CI, 1.02–5.89; P = .04) were significant risk factors for cervical SCC (Table 3).
Table 3.
Logistic regression analysis for spinal cord compression in cases with adult scoliosis.
| OR | 95% CI | P | |
|---|---|---|---|
| Age | 1.09 | 1.04–1.14 | <.001* |
| Narrow cervical canal diameter at C5 | 2.27 | 1.35–3.85 | .002* |
| Main Cobb angle | .99 | .96–1.03 | .80 |
| PI-LL | .97 | .92–1.02 | .19 |
| PT | 1.03 | .95–1.12 | .51 |
| C2-7 lordosis angle | .99 | .95–1.03 | .47 |
| Sagittal balance grade | 2.45 | 1.02–5.89 | .04* |
Abbreviations: OR, odds ratio; CI, confidence interval; LL, lumbar lordosis; PI, pelvic incidence; PT, pelvic tilt. *Values are P < .05.
Risk Factors for Cervical SCC for Both Cases with Adult Scoliosis and Healthy Volunteers
In total, cervical SCC was observed in 89 subjects. Subjects with SCC were significantly older (45.9 ± 17.6 and 64.5 ± 11.2 years old, P < .001) and had significantly smaller canal diameters (15.2 ± 2.0 and 13.7 ± 1.9 mm, P < .001) and higher rates of scoliosis (17.6% and 28.1%, P = .013) (Table 4). Logistic regression analysis showed that advanced age [odds ratio (OR), 1.08; 95% confidence interval (CI), 1.06–1.10; P < .001] and narrow canal diameter (OR, 1.62; 95% CI, 1.37–1.92; P < .001) were significant risk factors for cervical SCC, but the presence of scoliosis was not significant (OR, .99; 95% CI, .47–2.10; P = .98) (Table 5).
Table 4.
Comparison between cases with and without spinal cord compression in both cases with adult scoliosis and healthy volunteers.
| SCC (−) | SCC (+) | P | |
|---|---|---|---|
| Number of cases | 1393 | 89 | |
| Age | 45.9 ± 17.6 | 64.5 ± 11.2 | <.001* |
| Sex (male/female) | 592/801 | 42/47 | .39 |
| Canal diameter at C5 (mm) | 15.2 ± 2.0 | 13.7 ± 1.9 | <.001* |
| Presence of scoliosis | 245 (17.6%) | 25 (28.1%) | .013* |
Abbreviation: SCC, spinal cord compression.
Table 5.
Logistic regression analysis for spinal cord compression in both cases with adult scoliosis and healthy volunteers.
| OR | 95% CI | P | |
|---|---|---|---|
| Age | 1.08 | 1.06–1.10 | <.001* |
| Narrow cervical canal diameter at C5 | 1.62 | 1.37–1.92 | <.001* |
| Presence of scoliosis | .99 | .47–2.10 | .98 |
Abbreviations: OR, odds ratio; CI, confidence interval.
Discussion
This study evaluated cervical MRI of patients with adult scoliosis. The rate of cervical SCC increased with age, and the total rate of cervical SCC was 9.3%. Sagittal balance deterioration was a significant risk factor in addition to the cervical narrow bony canal and advanced age. However, when comparing patients with adult scoliosis with those in the healthy control group, the presence of scoliosis itself was not found to be associated with cervical SCC, although we hypothesized adult scoliosis was a risk factor for cervical concurrent SCC. Based on the above, it is possible that poor sagittal balance in scoliosis may be associated with cervical SCC, and poor sagittal alignment has a greater relationship with cervical SCC than coronal deformity in ASD. The current study was not longitudinal, and so the development of cervical SCC over time in cases with AIS could not be investigated, but the three-dimensional deformity of the thoracic and thoracolumbar spine in AIS might only slightly affect the concurrent cervical spine SCC in adults.
Straightened or kyphotic cervical alignment is well recognized in cases with AIS,6-9 and not only the thoracolumbar spine but also the cervical spine is affected in AIS. Although scoliosis progressed even after adulthood in AIS,15,16 the current study found that the sagittal alignment also altered, and the risk of cervical SCC increased. There was, however, no data on whether the cervical SCC is higher in patients with adult scoliosis than in the healthy participants, nor data concerning the age from which the occurrence of cervical SCC increases. In the current comparison of cervical SCC in cases with adult scoliosis and healthy subjects, the frequency of cervical SCC was significantly higher in cases with adult scoliosis (Table 4). However, the scoliosis was not a significant risk factor in the logistic regression analysis, and so the scoliosis itself was not considered to be a confounding factor for cervical SCC (Table 5).
Advanced age, narrow bony canal, and male gender have been recognized as risk factors for developing degenerative cervical myelopathy (DCM).12,17-19 In one retrospective cohort study, 17 advanced age was an independent risk factor for DCM compared with cases without DCM (OR = 1.1 per year of age; 95% CI, 1.01–1.14); this risk factor was consistent in the current study. Furthermore, several reports demonstrate that a narrow bony canal is a risk factor for DCM.12,18,19 In a study comparing 100 patients with DCM treated with surgery and 100 healthy participants, the bony canal was significantly smaller in each cervical vertebrae in cases with DCM. 19 Cervical SCC was common in participants with narrow cervical bony canal <12 mm at mid C5 vertebral body level, 12 and this narrow bony canal could be a risk factor for cervical SCC. However, while male gender was associated with the presence of DCM,17,18 AIS and AdIS are more common in females, and so gender was not a risk factor. This might affect the presence of scoliosis itself not being associated with cervical SCC.
Although there have been no previous reports investigating cervical concurrent SCC only in cases with adult scoliosis, a relationship between thoracolumbar sagittal alignment and cervical degeneration including SCC in ASD including various pathologies has also been reported. Fujimori et al 5 reported that greater radiographic degeneration score correlated with loss of cervical lordosis in the setting of compensatory thoracic hypokyphosis induced by degenerative flat back (high PI-LL mismatch). 5 Shimizu et al 3 investigated cervical SCC in 121 patients with ASD and reported advanced age, increased body mass index, and PI-LL mismatch as independent predictive factors for cervical SCC. 3 Yuk et al 20 reported that cervical SCC is more likely to develop in patients with sagittal imbalance. 20 Moreover, Yuk et al 20 investigated the whole spine MRI and sagittal alignment in 100 cases with lumbar pathologies, and observed a very close correlation between C7 SVA and cervical SCC (r = .688, P < .01) as well as C2–7 SVA (r = .563, P < .01), age (r = .397, P < .01), and T1 slope-cervical lordosis (r = .281, P < .01) in Pearson correlation coefficients. 20 Also in the current study, deterioration of sagittal alignment was associated with cervical SCC, and thus it is conceivable that reduced global spinal balance can increase the mechanical load on the cervical spine, resulting in cervical SCC.
Some study limitations exist which should be considered when interpreting our results. First, the current study was just a cross-sectional study. In total, 92 cases (34.1%) did not have any history of scoliosis during adolescence, and these cases have the potential for both AdIS and adult de novo scoliosis. Future prospective longitudinal study is essential to analyze the cause-effect basis for the development of cervical SCC in cases with adolescent scoliosis. Second, although sagittal balance was a significant risk factor for cervical SCC in cases with adult scoliosis, it was not determined whether degenerative spine pathology or inferior sagittal balance itself affected the onset of cervical SCC. Future study is necessary to reanalyze the risk factors of cervical SCC by including the degree of other spinal degenerative changes in addition to factors in the current study. Last, the results were obtained from patients treated at a single center, and all patients were of a single race. To support the results of the current study, an international multicenter large-scale study needs to be conducted.
In conclusion, scoliosis itself was not found to be significantly associated with cervical SCC; rather, it was the deterioration in sagittal balance that was found to be significant in this respect, in addition to narrow cervical bony canal and advanced age.
Acknowledgments
We are grateful to Ms. Sachiko Hiraiwa and Ms. Naoko Kojima at Meijo Hospital for their assistance throughout this study. The authors would like to thank ENAGO (www.enago.jp) for the English language review.
Footnotes
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iDs
Hiroaki Nakashima https://orcid.org/0000-0002-0039-9678
Noriaki Kawakami https://orcid.org/0000-0002-7780-1020
Shiro Imagama https://orcid.org/0000-0002-6951-8575
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