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Incidence and Risk Factors of Cervical Kyphosis in Patients with Adolescent Idiopathic Scoliosis
Original Article
Incidence and Risk Factors of Cervical Kyphosis in Patients with Adolescent Idiopathic Scoliosis Yong Tang, Xingping Xu, Feng Zhu, Changwei Chen, Fusheng Wang, Min Lu, Xing Huang
BACKGROUND: Cervical kyphosis (CK) has been reported in patients with adolescent idiopathic scoliosis (AIS). The report about the incidence of CK between patients with AIS and normal populations was little. Patients included in previous studies often required scoliosis surgery (Cobb angle ‡40 ), which does not represent all patients with AIS. The aims of this study were to compare incidence of CK between patients with AIS (Cobb angle >10 ) and an age-matched normal population and to identify risk factors related to CK, especially coronal parameters that have rarely been studied in current literature.
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METHODS: Patients with AIS (n [ 112) and asymptomatic subjects from the general population (control group; n [ 40) were retrospectively analyzed. Radiographic parameters of coronal and sagittal plane were measured on full-length spine x-rays. Patients with AIS were divided into 2 groups based on cervical lordosis angle: cervical lordosis and CK.
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RESULTS: CK was observed in 14 of 40 (35%) subjects in the control group and 68 of 112 (60.7%) patients with AIS. Several parameters were related to CK, including major curve, proximal thoracic, and main thoracic Cobb angle; proximal thoracic kyphosis angle; main thoracic kyphosis angle; T1 slope; sagittal vertical axis; vertical distance between C7 plumb line and center sacral vertical line; apical vertebral translation; T1 coronal tilt; and lumbar
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Key words Adolescent idiopathic scoliosis - Apical vertebral translation - Cervical kyphosis - Incidence - Lumbar pelvic relationship - Risk factor - T1 coronal tilt -
Abbreviations and Acronyms AIS: Adolescent idiopathic scoliosis AVT: Apical vertebral translation C7PL-CSVL: Vertical distance between C7 plumb line and center sacral vertical line CK: Cervical kyphosis CL: Cervical lordosis LPR: Lumbar pelvic relationship MC: Major curve
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pelvic relationship. Logistic regression identified main thoracic Cobb angle, main thoracic kyphosis angle, sagittal vertical axis, lumbar pelvic relationship, and apical vertebral translation as independent risk factors of CK. CONCLUSIONS: Incidence of CK increases in patients with AIS relative to normal subjects. Coronal parameters of the spine could influence cervical sagittal alignment.
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INTRODUCTION
A
dolescent idiopathic scoliosis (AIS), a three-dimensional deformity of the spine that includes a coronal curve, vertebral rotation, and flattening of the sagittal profile, affects appropriately 2%e3% adolescents.1-3 Curve correction in the coronal and sagittal plane is critical to the long-term success of scoliosis surgery. During the last decade, spinal sagittal alignment has played an important role in the evaluation of spinal deformity preoperatively and postoperatively. Cervical sagittal alignment, as a part of global sagittal alignment, may have a correlation with health-related quality of life.4-6 Cervical kyphosis (CK), which is considered pathologic, may be associated with the development of cervical myelopathy and neck pain.4,7 CK has been reported in patients with AIS in previous studies.3,4,7,8 Hilibrand et al.9 found a significant correlation between the loss of thoracic kyphosis and the development of CK. Canavese et al.10 reported a similar finding in their study.
MT: Main thoracic MTKA: Main thoracic kyphosis angle PT: Proximal thoracic PTKA: Proximal thoracic kyphosis angle SVA: Sagittal vertical axis Department of Orthopedics, Yinzhou People’s Hospital of Ningbo City, Ningbo, Zhejiang, China To whom correspondence should be addressed: Yong Tang, M.D. [E-mail: [email protected]] Yong Tang and Xingping Xu are coefirst authors. Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.264 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Restoration of thoracic kyphosis after surgical intervention and its association with lumbar lordosis have been studied by several authors.11-13 Yu et al.14 found that CK was correlated with global sagittal alignment, and the morphologic characteristics of the sagittal alignments were associated with the Lenke lumbar modifier. Hiyama et al.15 reported that CK correlated significantly with T1 slope, C7 plumb line, and thoracic kyphosis preoperatively and postoperatively. Ito et al.8 showed that the apex of thoracic kyphosis and C7 sagittal vertical axis was related to CK. Most previous studies included patients with AIS requiring scoliosis surgery with Cobb angle 40 , which does not represent all patients with AIS. Furthermore, there have been no comparisons of the incidence of CK between patients with AIS and normal populations. Previous studies often focused on the sagittal parameters to identify the risk factors of CK. Because AIS is a threedimensional spinal deformity, coronal parameters may have an effect on spinal sagittal alignment. Therefore, taking these circumstances into account, our study aimed to (1) compare the incidence of CK between patients with AIS (Cobb angle >10 ) and age-matched normal populations and (2) identify risk factors related to CK, especially coronal parameters that have rarely been studied in the current literature.
MATERIALS AND METHODS This study was approved by the institutional review board. A total of 112 patients with AIS (AIS group) in our hospital from March 2009 to May 2018 were retrospectively reviewed. The control group comprised 83 age-matched normal subjects, who were followed for the same period as the patients with AIS. A definitive diagnosis of AIS was made in all patients. Patients with congenital, neuromuscular, or syndromic scoliosis or other secondary scoliosis were excluded. Study variables included C2-C7 angle, major curve (MC) Cobb angle, sex, age, Risser sign, Lenke type, proximal thoracic curve (PT) Cobb angle, main thoracic curve (MT) Cobb angle, thoracolumbar/lumbar curve Cobb angle, proximal thoracic kyphosis angle (PTKA) (T2-T5), main thoracic kyphosis angle (MTKA) (T5-T12), lumbar lordosis angle (L1-S1), sagittal vertical axis (SVA), vertical distance between C7 plumb line and center sacral vertical line (C7PL-CSVL), apical vertebral translation (AVT), T1 slope,16 T1 coronal tilt,17 sacral slope, and lumbar pelvic relationship (LPR).18 All radiographic parameters were measured on preoperative x-rays. Negative values indicated lordosis, and positive values indicated kyphosis. All patients with AIS were divided into 2 groups based on C2-C7 angle: cervical lordosis (CL) (C2-C7 angle <0 ) and CK (C2-C7 angle >0 ). Statistical Analysis IBM SPSS Version 20.0 software (IBM Corporation, Armonk, New York, USA) was used in all statistical analyses. Results were presented as mean SD. The data were checked for normality and equal variances. Student t test or Wilcoxon rank-sum test was used to compare group differences for quantitative variables. Pearson c2 test or Fisher exact test was used to compare categorical variables. Logistic regression was performed to identify independent risk factors of CK. Statistical significance was set at P < 0.05.
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RESULTS Study Cohort Data This study included 112 patients with AIS and 83 normal subjects. Data for all subjects are shown in Table 1. There was no significant difference regarding age, sex, height, weight, body mass index, and Risser sign between the AIS group and control group. Mean Cobb angle of the AIS group was 43.34 23.21 (range, 11 e98 ). Mean C2-C7 angle of the AIS group was significantly higher than the C2-C7 angle in the control group (6.5 17.2 vs. 2.4 14.2 ). The incidence of CK in the control group was 35%, which was lower than the incidence (60.7%) in the AIS group. Compared with normal subjects, the relative risk of patients with AIS having CK was 1.680 (95% confidence interval, 1.217e2.319), which is statistically significant (P < 0.05). Yu et al.14 reported a classification of cervical sagittal alignment into 4 groups of cervical-thoracic alignment. The distribution of different cervical alignments in patients with AIS according to the classification of Yu et al.14 is shown in Table 2. Risk Factors Related to CK in Patients with AIS Related parameters between patients with CK and patients without CK are shown in Table 3. Some parameters, including MC Cobb angle, PT Cobb angle, MT Cobb angle, PTKA, MTKA, AVT, T1 slope, T1 coronal tilt, SVA, C7PL-CSVL, and LPR, showed significant differences between patients with CK and patients with CL. The remaining parameters had no relationship to CK in patients with AIS. Patients with CK had higher MC Cobb angle, PT Cobb angle, and MT Cobb angle (Table 3). As the Cobb angle increased, the incidence of CK increased from 45% to 72.7%. Compared with the 51.0% incidence of CK in patients with Cobb angle 40 , patients with Cobb angle >40 had a significantly higher incidence (68.7%) of CK (Table 4). CK had a negative correlation with PTKA and MTKA. Patients with CK had lower PTKA and MTKA compared with patients with CL. In patients
Table 1. Data of Participants AIS Group Number
Control Group
P
112
83
16.45 2.45
16.59 2.71
NS
90:22
60:23
NS
Height
156.73 11.34
156.21 12.31
NS
Weight
42.34 9.12
41.91 8.23
NS
BMI
17.24 1.89
17.17 2.03
NS
Age, years Sex, F:M
Risser sign
2.9 0.8
2.9 0.9
NS
Cobb angle
43.34 23.21
5.98 2.63
<0.05
C2-C7 angle
6.5 17.2
2.7 14.8
<0.05
CK
68 (60.7%)
30 (36.1%)
<0.05
AIS, adolescent idiopathic scoliosis; NS, not significant; F, female; M, male; BMI, body mass index; CK, cervical kyphosis.
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Table 2. Distribution of Different Cervical Alignments According to Classification of Yu et al14
Table 4. Cervical Kyphosis Distribution According to Cobb Angle Cobb Angle ( )
Cervical Sagittal Alignment Group
Kyphosis
Straight
Sigmoid
Lordosis
Total
8
18
7
19
52
CNK
Number
CK
23
3
1
0
26
C2-C7 angle,
CMTK
21
3
0
0
24
CK
CLTK
4
5
0
0
9
Total
56
29
8
19
112
11e25
25e40
40e55
>55
20
31
39
22
P
1.6 12.2 2.3 13.2 9.8 15.4 13.9 16.3 <0.05 17 (54.8%) 26 (66.7%) 16 (72.7%) <0.05
9 (45%)
26/51 (51.0%)
42/61 (68.9%)
<0.05
CK, cervical kyphosis.
CNK, cervical nonkyphosis; CK, cervical kyphosis; CMTK, cervical middle thoracic kyphosis; CLTK, cervical lower thoracic kyphosis.
with MTKA of <10 , 10 e40 , and >40 , the incidence of CK was 74.4%, 59.6%, and 38.1% (Table 5). T1-related parameters, such as T1 slope and T1 coronal tilt, showed a relationship with CK. T1 slope in patients with CK was smaller than in patients with CL (8.21 3.41 vs. 29.11 10.25 ). Table 3. Related Parameters Between Patients with Cervical Lordosis and Cervical Kyphosis CK
CL
68
44
Age, years
16.21 2.38
16.82 2.54
NS
Risser sign
2.8 0.8
3.0 0.9
NS
53:15
37:7
NS
47.41 16.72
37.05 14.32
<0.05
25.23 8.92
17.21 7.43
<0.05
DISCUSSION
42.32 14.54
33.23 12.32
<0.05
34.32 11.23
32.34 11.89
NS
3.53 7.23
14.78 9.43
<0.05
19.23 11.43
33.13 19.43
<0.05
57.34 13.32
56.27 16.91
NS
25.35 12.21
17.42 9.37
<0.05
8.21 3.41
29.11 10.25
<0.05
The important role of the sagittal alignment of the spine has been recognized in normal and diseased states. CK seems to be more prevalent in patients with AIS relative to normal adolescents.15 Scoliosis could influence the sagittal profile, including the cervical sagittal alignment. Cervical sagittal alignment was reported to be closely associated with health-related quality of life in patients with AIS.5 Many previous studies have focused on the relationship between cervical sagittal alignment and global or
Number
Sex, F:M
MC Cobb angle, PT Cobb angle,
MT Cobb angle, TL/L Cobb angle, PTKA,
MTKA, LLA,
AVT, mm T1 slope,
P
In contrast, patients with CK had larger T1 coronal tilt than patients with CL (22.03 11.23 vs. 14.91 9.29 ). Greater AVT was found in patients with CK compared with patients with CL (25.35 12.21 mm vs. 17.42 9.37 mm). LPR in patients with CK was larger than in patients with CL (19.6 8.9 vs. 10.3 7.4 ). Significant differences with regard to spinal balance, including SVA and C7PL-CSVL, were observed between patients with CK and CL. SVA had a significant negative correlation with CK, and a positive correlation was found between CK and C7PL-CSVL. Logistic regression showed that MT Cobb angle, MTKA, SVA, LPR, and AVT were independent risk factors of CK in patients with AIS (odds ratio ¼ 1.093, 1.121, 1.071, 1.081, and, 1.085; P < 0.05). In addition, there was a statistically significant difference in the incidence of CK among different Lenke types (P < 0.05) (Table 6). More CK was seen in patients with double thoracic curves and triple curves. All Lenke types had an increase in C2-C7 angle relative to normal populations.
22.03 11.23
14.91 9.29
<0.05
38.52 7.21
37.26 6.98
NS
SVA, mm
11.3 9.4
28.5 23.9
<0.05
C7PL-CSVL, mm
21.4 15.3
9.5 9.8
<0.05
19.6 8.9
10.3 7.4
<0.05
T1 CA, SS,
LPR,
CK, cervical kyphosis; CL, cervical lordosis; NS, not significant; F, female; M, male; MC, major curve; PT, proximal thoracic; MT, main thoracic; TL/L, thoracolumbar/lumbar; PTKA, proximal thoracic kyphosis angle; MTKA, main thoracic kyphosis angle; LLA, lumbar lordosis angle; AVT, apical vertebral translation; CA, coronal angle; SS, sacral slope; SVA, sagittal vertical axis; C7PL-CSVL, vertical distance between C7 plumb line and center sacral vertical line; LPR, lumbar pelvic relationship.
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Table 5. Cervical Kyphosis Distribution According to Thoracic Kyphosis Thoracic Kyphosis ( ) <10 Number C2-C7 angle,
10e40
>40
P
39
52
21
19.23 11.34
2.9 9.65
12.76 11.91
<0.05
29 (74.4%)
31 (59.6%)
8 (38.1%)
<0.05
CK CK, cervical kyphosis.
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CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Table 6. Cervical Kyphosis Distribution According to Lenke Type Lenke Type
Number
C2-C7
CK
1
35
8.23 8.92
23 (65.7%)
2
19
11.32 7.34
15 (78.9%)
3
13
4.32 4.29
6 (46.2%)
4
12
10.87 7.13
9 (75%)
5
24
2.89 7.19
11 (45.8%)
6
9
4.52 5.23
4 (44.4%)
<0.05
<0.05
P CK, cervical kyphosis.
regional sagittal profile.3,16,19 In our opinion, as AIS is a three-dimensional spinal deformity, not only sagittal alignment but also coronal parameters could exert effects on cervical sagittal alignment. The correlation between sagittal alignment and cervical sagittal alignment used to identify the risk factors of abnormal cervical sagittal alignment is incomplete. Thus, this study addresses this limitation to gain an understanding of the impact of coronal parameters on the cervical spine. Our study showed that the incidence of CK increased in patients with AIS compared with normal subjects, which was inconsistent with the result reported by Hiyama et al.15 In their study, the incidence of CK was 59.5% in the AIS group, which was larger than the incidence (41.7%) in the control group. Both findings confirmed the effect of AIS on kyphosis of the cervical spine. Moreover, the incidence of CK in patients with AIS was reported to be 40%e86%.8,14,15,20 The incidence of CK in patients with AIS in our study was comparable to these studies. The thoracic hypokyphosis (both proximal and main thoracic hypokyphosis) was associated with the increase of CK and the decrease of CL in this study. Hilibrand et al.9 noted that there was a significant correlation between the loss of thoracic kyphosis and the development of CK in 38 patients with AIS.9 Akbar et al.3 reported that patients with hypokyphotic AIS often had a kyphotic cervical spine. Wang and Liu21 found that in the CK group, T5-T12 Cobb angle was significantly lower than in the CL group. In the study by Hiyama et al.,15 CK was found to be related to thoracic hypokyphosis in the AIS group, but not in the normal group. In line with the previous studies,7,15 our study demonstrated that no significant difference in lumbar lordosis was observed between CK and CL groups. For coronal parameters, MC, PT, and MT Cobb angle; AVT; and LPR showed a significant difference between patients with CL and CK. The size of the major curve reflects the severity of spinal deformity to some extent. To our knowledge, studies focusing on the relationship between coronal curve size and CK are scarce. In the study by Hu and Lieberman,20 the patients who had a coronal thoracic curve of 20 had higher CK incidence. Smith et al.22 reported that adult patients with thoracic scoliosis had higher CK incidence. In this study, no association between CK and lumbar curve size was found. These results indicate that CK may be mainly affected by the coronal curve of the thoracic spine.
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LPR is the angle between the line at the inferior endplate of the lower end vertebra in a lumbar curve and the iliac crest line, which reflects in part the relationship between spine and pelvis. Our finding indicated that patients with CK had significantly larger LPR. In other studies, some pelvic parameters were found to be associated with CK.23,24 These findings suggested that pelvic parameters may affect the alignment of the cervical spine and even the entire spine. This study indicated that AVT was associated with CK. Jiang et al.17 found that the increase of cervical tilt significantly positively correlated with the increase of AVT of thoracic curve, which suggested a correlation between cervical coronal alignment and AVT. La Maida et al.25 reported that in scoliosis surgery, the apical vertebral derotation and translation technique seemed to give less sagittal imbalance with a better cervical sagittal profile, which implied that decreased AVT may contribute to less cervical sagittal imbalance. Our results directly demonstrated the correlation between AVT and CK. AVT may be an important predictor of cervical spine pathology. Spinal balance is related to the spinal alignment. In this study, our results indicated that sagittal and coronal balance could influence the profile of cervical spine. In patients with CK, SVA was significantly smaller compared with patients with CL. Hiyama et al.15 observed a positive correlation between CL and SVA. Yagi et al.26 and Knott et al.27 reported similar results in their studies. Smith et al.22 found that higher SVA grades were associated with lower CK prevalence (0 ¼ 40%, þ ¼ 23%, þþ ¼ 11%), but greater cervical positive sagittal malalignment prevalence (0 ¼ 24%, þ ¼ 24%, þþ ¼ 48%). Relevant parameters of T1 vertebra have been reported as predictors of the status of the spine.16,23,24,28 Knott et al.27 reported that T1 slope was significantly correlated with SVA and could predict the sagittal balance of the spine. Pesenti et al.16 found that T1 slope and sagittal tilt are good indicators of postoperative changes for regional (CL and thoracic kyphosis) and global parameters. Our findings were inconsistent with these studies. In this study, patients with CK had significantly larger T1 slope than patients with CL. Moreover, increased T1 coronal tilt was positively correlated with CK. Taken together, sagittal and coronal parameters of T1 could influence the sagittal alignment of the cervical spine. There was a significant difference in the incidence of CK among different Lenke types. Lenke types 1, 2, and 4 had a higher incidence of CK compared with other Lenke types. A common denominator of Lenke types 1, 2, and 4 may be that they have thoracic hypokyphosis. Thoracic hypokyphosis may contribute to the development of CK. Furthermore, these 3 curve types have the major portion of the curve in the thoracic spine, leading to an upper spine three-dimensional deformity. There are some limitations to this study. First, this was a retrospective study, which may have resulted in some inherent biases. Second, we did not collect data regarding patients’ symptoms, and it is not clear if there is a relationship between CK and clinical symptoms. Third, owing to the limited sample size, analysis may have been underpowered in multiple subgroup analysis. Last, we focused only on the cervical sagittal alignment in patients before surgery in this study. We believe that the evaluation could have been more
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
complete if postsurgery characteristics, such as cervical alignment, thoracic and lumbar curves, and pelvic parameters, were considered. CONCLUSIONS Several novel factors (LPR, AVT, and T1 coronal tilt) are correlated with CK in patients with AIS, demonstrating the
kyphosis after operative treatment of adolescent idiopathic scoliosis: a multicenter comparison of three surgical approaches. Spine (Phila Pa 1976). 2008;33:2630-2636.
REFERENCES 1. Lang C, Zou Q, Sui W, Deng Y, Huang Z, Yang J. Coronal deformity angular ratio may serve as a valuable parameter to predict in-brace correction in patients with adolescent idiopathic scoliosis [epub ahead of print]. Spine J. 2018. https://doi.org/ 10.1016/j.spinee.2018.12.002. 2. Lang C, Sui W, Di M, et al. Factors that influence in-brace correction in patients with adolescent idiopathic scoliosis. World Neurosurg. 2019;123: e597-e603. 3. Akbar M, Almansour H, Lafage R, et al. Sagittal alignment of the cervical spine in the setting of adolescent idiopathic scoliosis. J Neurosurg Spine. 2018;29:506-514. 4. Zhu C, Yang X, Zhou B, et al. Cervical kyphosis in patients with Lenke type 1 adolescent idiopathic scoliosis: the prediction of thoracic inlet angle. BMC Musculoskelet Disord. 2017;18:220. 5. Youn MS, Shin JK, Goh TS, Kang SS, Jeon WK, Lee JS. Relationship between cervical sagittal alignment and health-related quality of life in adolescent idiopathic scoliosis. Eur Spine J. 2016; 25:3114-3119. 6. Protopsaltis TS, Scheer JK, Terran JS, et al. How the neck affects the back: changes in regional cervical sagittal alignment correlate to HRQOL improvement in adult thoracolumbar deformity patients at 2-year follow-up. J Neurosurg Spine. 2015; 23:153-158. 7. Norheim EP, Carreon LY, Sucato DJ, Lenke LG, Glassman SD. Cervical spine compensation in adolescent idiopathic scoliosis. Spine Deform. 2015; 3:327-331. 8. Ito K, Imagama S, Ito Z, et al. Analysis of cervical kyphosis and spinal balance in young idiopathic scoliosis patients classified by the apex of thoracic kyphosis. Eur Spine J. 2016;25:3220-3225. 9. Hilibrand AS, Tannenbaum DA, Graziano GP, Loder RT, Hensinger RN. The sagittal alignment of the cervical spine in adolescent idiopathic scoliosis. J Pediatr Orthop. 1995;15:627-632. 10. Canavese F, Turcot K, De Rosa V, de Coulon G, Kaelin A. Cervical spine sagittal alignment variations following posterior spinal fusion and instrumentation for adolescent idiopathic scoliosis. Eur Spine J. 2011;20:1141-1148. 11. Sucato DJ, Agrawal S, O’Brien MF, Lowe TG, Richards SB, Lenke L. Restoration of thoracic
impact of coronal plane parameters on CK. MT Cobb angle, MTKA, SVA, LPR, and AVT are identified as independent risk factors of CK through the logistic regression model. The incidence of CK is higher in patients with AIS than normal subjects. Coronal parameters of the spine have an effect on cervical sagittal alignment.
12. Lowenstein JE, Matsumoto H, Vitale MG, et al. Coronal and sagittal plane correction in adolescent idiopathic scoliosis: a comparison between all pedicle screw versus hybrid thoracic hook lumbar screw constructs. Spine (Phila Pa 1976). 2007;32:448-452. 13. Stokes IA. Three-dimensional terminology of spinal deformity. A report presented to the Scoliosis Research Society by the Scoliosis Research Society Working Group on 3-D terminology of spinal deformity. Spine (Phila Pa 1976). 1994;19:236-248. 14. Yu M, Silvestre C, Mouton T, Rachkidi R, Zeng L, Roussouly P. Analysis of the cervical spine sagittal alignment in young idiopathic scoliosis: a morphological classification of 120 cases. Eur Spine J. 2013;22:2372-2381. 15. Hiyama A, Sakai D, Watanabe M, Katoh H, Sato M, Mochida J. Sagittal alignment of the cervical spine in adolescent idiopathic scoliosis: a comparative study of 42 adolescents with idiopathic scoliosis and 24 normal adolescents. Eur Spine J. 2016;25:3226-3233. 16. Pesenti S, Blondel B, Peltier E, Choufani E, Bollini G, Jouve JL. Interest of T1 parameters for sagittal alignment evaluation of adolescent idiopathic scoliosis patients. Eur Spine J. 2016;25: 424-429. 17. Jiang J, Qian BP, Qiu Y, Wang B, Yu Y, Zhu ZZ. Full fusion of proximal thoracic curve helps to prevent postoperative cervical tilt in Lenke type 2 adolescent idiopathic scoliosis patients with rightelevated shoulder. BMC Musculoskelet Disord. 2017; 18:362. 18. Katz DE, Durrani AA. Factors that influence outcome in bracing large curves in patients with adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2001;26:2354-2361. 19. Matsubayashi Y, Chikuda H, Oshima Y, et al. C7 sagittal vertical axis is the determinant of the C5C7 angle in cervical sagittal alignment. Spine J. 2017;17:622-626. 20. Hu X, Lieberman IH. Prevalence and factors affecting cervical deformity in adolescent idiopathic scoliosis patients: a single-center retrospective radiological study. Int J Spine Surg. 2018; 12:22-25.
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21. Wang L, Liu X. Cervical sagittal alignment in adolescent idiopathic scoliosis patients (Lenke type 1-6). J Orthop Sci. 2017;22:254-259. 22. Smith JS, Lafage V, Schwab FJ, et al. Prevalence and type of cervical deformity among 470 adults with thoracolumbar deformity. Spine (Phila Pa 1976). 2014;39:E1001-E1009. 23. Protopsaltis TS, Lafage R, Smith JS, et al. The lumbar pelvic angle, the lumbar component of the T1 pelvic angle, correlates with HRQOL, PI-LL mismatch, and it predicts global alignment. Spine (Phila Pa 1976). 2018;43:681-687. 24. Protopsaltis T, Terran J, Soroceanu A, et al. T1 slope minus cervical lordosis (TS-CL), the cervical answer to PI-LL, defines cervical sagittal deformity in patients undergoing thoracolumbar osteotomy. Int J Spine Surg. 2018;12:362-370. 25. La Maida GA, Peroni DR, Ferraro M, Della Valle A, Vitali C, Misaggi B. Apical vertebral derotation and translation (AVDT) for adolescent idiopathic scoliosis using screws and sublaminar bands: a safer concept for deformity correction. Eur Spine J. 2018;27:157-164. 26. Yagi M, Iizuka S, Hasegawa A, et al. Sagittal cervical alignment in adolescent idiopathic scoliosis. Spine Deform. 2014;2:122-130. 27. Knott PT, Mardjetko SM, Techy F. The use of the T1 sagittal angle in predicting overall sagittal balance of the spine. Spine J. 2010;10:994-998. 28. Tamai K, Romanu J, Grisdela P Jr, et al. Small C7T1 lordotic angle and muscle degeneration at C7 level were independent radiological characteristics of patients with cervical imbalance: a propensity score-matched analysis. Spine J. 2018;18:1505-1512.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 27 December 2018; accepted 26 March 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.264 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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Incidence and Risk Factors of Cervical Kyphosis in Patients with Adolescent Idiopathic Scoliosis Yong Tang, Xingping Xu, Feng Zhu, Changwei Chen, Fusheng Wang, Min Lu, Xing Huang
BACKGROUND: Cervical kyphosis (CK) has been reported in patients with adolescent idiopathic scoliosis (AIS). The report about the incidence of CK between patients with AIS and normal populations was little. Patients included in previous studies often required scoliosis surgery (Cobb angle ‡40 ), which does not represent all patients with AIS. The aims of this study were to compare incidence of CK between patients with AIS (Cobb angle >10 ) and an age-matched normal population and to identify risk factors related to CK, especially coronal parameters that have rarely been studied in current literature.
-
METHODS: Patients with AIS (n [ 112) and asymptomatic subjects from the general population (control group; n [ 40) were retrospectively analyzed. Radiographic parameters of coronal and sagittal plane were measured on full-length spine x-rays. Patients with AIS were divided into 2 groups based on cervical lordosis angle: cervical lordosis and CK.
-
RESULTS: CK was observed in 14 of 40 (35%) subjects in the control group and 68 of 112 (60.7%) patients with AIS. Several parameters were related to CK, including major curve, proximal thoracic, and main thoracic Cobb angle; proximal thoracic kyphosis angle; main thoracic kyphosis angle; T1 slope; sagittal vertical axis; vertical distance between C7 plumb line and center sacral vertical line; apical vertebral translation; T1 coronal tilt; and lumbar
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Key words Adolescent idiopathic scoliosis - Apical vertebral translation - Cervical kyphosis - Incidence - Lumbar pelvic relationship - Risk factor - T1 coronal tilt -
Abbreviations and Acronyms AIS: Adolescent idiopathic scoliosis AVT: Apical vertebral translation C7PL-CSVL: Vertical distance between C7 plumb line and center sacral vertical line CK: Cervical kyphosis CL: Cervical lordosis LPR: Lumbar pelvic relationship MC: Major curve
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pelvic relationship. Logistic regression identified main thoracic Cobb angle, main thoracic kyphosis angle, sagittal vertical axis, lumbar pelvic relationship, and apical vertebral translation as independent risk factors of CK. CONCLUSIONS: Incidence of CK increases in patients with AIS relative to normal subjects. Coronal parameters of the spine could influence cervical sagittal alignment.
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INTRODUCTION
A
dolescent idiopathic scoliosis (AIS), a three-dimensional deformity of the spine that includes a coronal curve, vertebral rotation, and flattening of the sagittal profile, affects appropriately 2%e3% adolescents.1-3 Curve correction in the coronal and sagittal plane is critical to the long-term success of scoliosis surgery. During the last decade, spinal sagittal alignment has played an important role in the evaluation of spinal deformity preoperatively and postoperatively. Cervical sagittal alignment, as a part of global sagittal alignment, may have a correlation with health-related quality of life.4-6 Cervical kyphosis (CK), which is considered pathologic, may be associated with the development of cervical myelopathy and neck pain.4,7 CK has been reported in patients with AIS in previous studies.3,4,7,8 Hilibrand et al.9 found a significant correlation between the loss of thoracic kyphosis and the development of CK. Canavese et al.10 reported a similar finding in their study.
MT: Main thoracic MTKA: Main thoracic kyphosis angle PT: Proximal thoracic PTKA: Proximal thoracic kyphosis angle SVA: Sagittal vertical axis Department of Orthopedics, Yinzhou People’s Hospital of Ningbo City, Ningbo, Zhejiang, China To whom correspondence should be addressed: Yong Tang, M.D. [E-mail: [email protected]] Yong Tang and Xingping Xu are coefirst authors. Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.264 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Restoration of thoracic kyphosis after surgical intervention and its association with lumbar lordosis have been studied by several authors.11-13 Yu et al.14 found that CK was correlated with global sagittal alignment, and the morphologic characteristics of the sagittal alignments were associated with the Lenke lumbar modifier. Hiyama et al.15 reported that CK correlated significantly with T1 slope, C7 plumb line, and thoracic kyphosis preoperatively and postoperatively. Ito et al.8 showed that the apex of thoracic kyphosis and C7 sagittal vertical axis was related to CK. Most previous studies included patients with AIS requiring scoliosis surgery with Cobb angle 40 , which does not represent all patients with AIS. Furthermore, there have been no comparisons of the incidence of CK between patients with AIS and normal populations. Previous studies often focused on the sagittal parameters to identify the risk factors of CK. Because AIS is a threedimensional spinal deformity, coronal parameters may have an effect on spinal sagittal alignment. Therefore, taking these circumstances into account, our study aimed to (1) compare the incidence of CK between patients with AIS (Cobb angle >10 ) and age-matched normal populations and (2) identify risk factors related to CK, especially coronal parameters that have rarely been studied in the current literature.
MATERIALS AND METHODS This study was approved by the institutional review board. A total of 112 patients with AIS (AIS group) in our hospital from March 2009 to May 2018 were retrospectively reviewed. The control group comprised 83 age-matched normal subjects, who were followed for the same period as the patients with AIS. A definitive diagnosis of AIS was made in all patients. Patients with congenital, neuromuscular, or syndromic scoliosis or other secondary scoliosis were excluded. Study variables included C2-C7 angle, major curve (MC) Cobb angle, sex, age, Risser sign, Lenke type, proximal thoracic curve (PT) Cobb angle, main thoracic curve (MT) Cobb angle, thoracolumbar/lumbar curve Cobb angle, proximal thoracic kyphosis angle (PTKA) (T2-T5), main thoracic kyphosis angle (MTKA) (T5-T12), lumbar lordosis angle (L1-S1), sagittal vertical axis (SVA), vertical distance between C7 plumb line and center sacral vertical line (C7PL-CSVL), apical vertebral translation (AVT), T1 slope,16 T1 coronal tilt,17 sacral slope, and lumbar pelvic relationship (LPR).18 All radiographic parameters were measured on preoperative x-rays. Negative values indicated lordosis, and positive values indicated kyphosis. All patients with AIS were divided into 2 groups based on C2-C7 angle: cervical lordosis (CL) (C2-C7 angle <0 ) and CK (C2-C7 angle >0 ). Statistical Analysis IBM SPSS Version 20.0 software (IBM Corporation, Armonk, New York, USA) was used in all statistical analyses. Results were presented as mean SD. The data were checked for normality and equal variances. Student t test or Wilcoxon rank-sum test was used to compare group differences for quantitative variables. Pearson c2 test or Fisher exact test was used to compare categorical variables. Logistic regression was performed to identify independent risk factors of CK. Statistical significance was set at P < 0.05.
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RESULTS Study Cohort Data This study included 112 patients with AIS and 83 normal subjects. Data for all subjects are shown in Table 1. There was no significant difference regarding age, sex, height, weight, body mass index, and Risser sign between the AIS group and control group. Mean Cobb angle of the AIS group was 43.34 23.21 (range, 11 e98 ). Mean C2-C7 angle of the AIS group was significantly higher than the C2-C7 angle in the control group (6.5 17.2 vs. 2.4 14.2 ). The incidence of CK in the control group was 35%, which was lower than the incidence (60.7%) in the AIS group. Compared with normal subjects, the relative risk of patients with AIS having CK was 1.680 (95% confidence interval, 1.217e2.319), which is statistically significant (P < 0.05). Yu et al.14 reported a classification of cervical sagittal alignment into 4 groups of cervical-thoracic alignment. The distribution of different cervical alignments in patients with AIS according to the classification of Yu et al.14 is shown in Table 2. Risk Factors Related to CK in Patients with AIS Related parameters between patients with CK and patients without CK are shown in Table 3. Some parameters, including MC Cobb angle, PT Cobb angle, MT Cobb angle, PTKA, MTKA, AVT, T1 slope, T1 coronal tilt, SVA, C7PL-CSVL, and LPR, showed significant differences between patients with CK and patients with CL. The remaining parameters had no relationship to CK in patients with AIS. Patients with CK had higher MC Cobb angle, PT Cobb angle, and MT Cobb angle (Table 3). As the Cobb angle increased, the incidence of CK increased from 45% to 72.7%. Compared with the 51.0% incidence of CK in patients with Cobb angle 40 , patients with Cobb angle >40 had a significantly higher incidence (68.7%) of CK (Table 4). CK had a negative correlation with PTKA and MTKA. Patients with CK had lower PTKA and MTKA compared with patients with CL. In patients
Table 1. Data of Participants AIS Group Number
Control Group
P
112
83
16.45 2.45
16.59 2.71
NS
90:22
60:23
NS
Height
156.73 11.34
156.21 12.31
NS
Weight
42.34 9.12
41.91 8.23
NS
BMI
17.24 1.89
17.17 2.03
NS
Age, years Sex, F:M
Risser sign
2.9 0.8
2.9 0.9
NS
Cobb angle
43.34 23.21
5.98 2.63
<0.05
C2-C7 angle
6.5 17.2
2.7 14.8
<0.05
CK
68 (60.7%)
30 (36.1%)
<0.05
AIS, adolescent idiopathic scoliosis; NS, not significant; F, female; M, male; BMI, body mass index; CK, cervical kyphosis.
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Table 2. Distribution of Different Cervical Alignments According to Classification of Yu et al14
Table 4. Cervical Kyphosis Distribution According to Cobb Angle Cobb Angle ( )
Cervical Sagittal Alignment Group
Kyphosis
Straight
Sigmoid
Lordosis
Total
8
18
7
19
52
CNK
Number
CK
23
3
1
0
26
C2-C7 angle,
CMTK
21
3
0
0
24
CK
CLTK
4
5
0
0
9
Total
56
29
8
19
112
11e25
25e40
40e55
>55
20
31
39
22
P
1.6 12.2 2.3 13.2 9.8 15.4 13.9 16.3 <0.05 17 (54.8%) 26 (66.7%) 16 (72.7%) <0.05
9 (45%)
26/51 (51.0%)
42/61 (68.9%)
<0.05
CK, cervical kyphosis.
CNK, cervical nonkyphosis; CK, cervical kyphosis; CMTK, cervical middle thoracic kyphosis; CLTK, cervical lower thoracic kyphosis.
with MTKA of <10 , 10 e40 , and >40 , the incidence of CK was 74.4%, 59.6%, and 38.1% (Table 5). T1-related parameters, such as T1 slope and T1 coronal tilt, showed a relationship with CK. T1 slope in patients with CK was smaller than in patients with CL (8.21 3.41 vs. 29.11 10.25 ). Table 3. Related Parameters Between Patients with Cervical Lordosis and Cervical Kyphosis CK
CL
68
44
Age, years
16.21 2.38
16.82 2.54
NS
Risser sign
2.8 0.8
3.0 0.9
NS
53:15
37:7
NS
47.41 16.72
37.05 14.32
<0.05
25.23 8.92
17.21 7.43
<0.05
DISCUSSION
42.32 14.54
33.23 12.32
<0.05
34.32 11.23
32.34 11.89
NS
3.53 7.23
14.78 9.43
<0.05
19.23 11.43
33.13 19.43
<0.05
57.34 13.32
56.27 16.91
NS
25.35 12.21
17.42 9.37
<0.05
8.21 3.41
29.11 10.25
<0.05
The important role of the sagittal alignment of the spine has been recognized in normal and diseased states. CK seems to be more prevalent in patients with AIS relative to normal adolescents.15 Scoliosis could influence the sagittal profile, including the cervical sagittal alignment. Cervical sagittal alignment was reported to be closely associated with health-related quality of life in patients with AIS.5 Many previous studies have focused on the relationship between cervical sagittal alignment and global or
Number
Sex, F:M
MC Cobb angle, PT Cobb angle,
MT Cobb angle, TL/L Cobb angle, PTKA,
MTKA, LLA,
AVT, mm T1 slope,
P
In contrast, patients with CK had larger T1 coronal tilt than patients with CL (22.03 11.23 vs. 14.91 9.29 ). Greater AVT was found in patients with CK compared with patients with CL (25.35 12.21 mm vs. 17.42 9.37 mm). LPR in patients with CK was larger than in patients with CL (19.6 8.9 vs. 10.3 7.4 ). Significant differences with regard to spinal balance, including SVA and C7PL-CSVL, were observed between patients with CK and CL. SVA had a significant negative correlation with CK, and a positive correlation was found between CK and C7PL-CSVL. Logistic regression showed that MT Cobb angle, MTKA, SVA, LPR, and AVT were independent risk factors of CK in patients with AIS (odds ratio ¼ 1.093, 1.121, 1.071, 1.081, and, 1.085; P < 0.05). In addition, there was a statistically significant difference in the incidence of CK among different Lenke types (P < 0.05) (Table 6). More CK was seen in patients with double thoracic curves and triple curves. All Lenke types had an increase in C2-C7 angle relative to normal populations.
22.03 11.23
14.91 9.29
<0.05
38.52 7.21
37.26 6.98
NS
SVA, mm
11.3 9.4
28.5 23.9
<0.05
C7PL-CSVL, mm
21.4 15.3
9.5 9.8
<0.05
19.6 8.9
10.3 7.4
<0.05
T1 CA, SS,
LPR,
CK, cervical kyphosis; CL, cervical lordosis; NS, not significant; F, female; M, male; MC, major curve; PT, proximal thoracic; MT, main thoracic; TL/L, thoracolumbar/lumbar; PTKA, proximal thoracic kyphosis angle; MTKA, main thoracic kyphosis angle; LLA, lumbar lordosis angle; AVT, apical vertebral translation; CA, coronal angle; SS, sacral slope; SVA, sagittal vertical axis; C7PL-CSVL, vertical distance between C7 plumb line and center sacral vertical line; LPR, lumbar pelvic relationship.
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Table 5. Cervical Kyphosis Distribution According to Thoracic Kyphosis Thoracic Kyphosis ( ) <10 Number C2-C7 angle,
10e40
>40
P
39
52
21
19.23 11.34
2.9 9.65
12.76 11.91
<0.05
29 (74.4%)
31 (59.6%)
8 (38.1%)
<0.05
CK CK, cervical kyphosis.
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
Table 6. Cervical Kyphosis Distribution According to Lenke Type Lenke Type
Number
C2-C7
CK
1
35
8.23 8.92
23 (65.7%)
2
19
11.32 7.34
15 (78.9%)
3
13
4.32 4.29
6 (46.2%)
4
12
10.87 7.13
9 (75%)
5
24
2.89 7.19
11 (45.8%)
6
9
4.52 5.23
4 (44.4%)
<0.05
<0.05
P CK, cervical kyphosis.
regional sagittal profile.3,16,19 In our opinion, as AIS is a three-dimensional spinal deformity, not only sagittal alignment but also coronal parameters could exert effects on cervical sagittal alignment. The correlation between sagittal alignment and cervical sagittal alignment used to identify the risk factors of abnormal cervical sagittal alignment is incomplete. Thus, this study addresses this limitation to gain an understanding of the impact of coronal parameters on the cervical spine. Our study showed that the incidence of CK increased in patients with AIS compared with normal subjects, which was inconsistent with the result reported by Hiyama et al.15 In their study, the incidence of CK was 59.5% in the AIS group, which was larger than the incidence (41.7%) in the control group. Both findings confirmed the effect of AIS on kyphosis of the cervical spine. Moreover, the incidence of CK in patients with AIS was reported to be 40%e86%.8,14,15,20 The incidence of CK in patients with AIS in our study was comparable to these studies. The thoracic hypokyphosis (both proximal and main thoracic hypokyphosis) was associated with the increase of CK and the decrease of CL in this study. Hilibrand et al.9 noted that there was a significant correlation between the loss of thoracic kyphosis and the development of CK in 38 patients with AIS.9 Akbar et al.3 reported that patients with hypokyphotic AIS often had a kyphotic cervical spine. Wang and Liu21 found that in the CK group, T5-T12 Cobb angle was significantly lower than in the CL group. In the study by Hiyama et al.,15 CK was found to be related to thoracic hypokyphosis in the AIS group, but not in the normal group. In line with the previous studies,7,15 our study demonstrated that no significant difference in lumbar lordosis was observed between CK and CL groups. For coronal parameters, MC, PT, and MT Cobb angle; AVT; and LPR showed a significant difference between patients with CL and CK. The size of the major curve reflects the severity of spinal deformity to some extent. To our knowledge, studies focusing on the relationship between coronal curve size and CK are scarce. In the study by Hu and Lieberman,20 the patients who had a coronal thoracic curve of 20 had higher CK incidence. Smith et al.22 reported that adult patients with thoracic scoliosis had higher CK incidence. In this study, no association between CK and lumbar curve size was found. These results indicate that CK may be mainly affected by the coronal curve of the thoracic spine.
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LPR is the angle between the line at the inferior endplate of the lower end vertebra in a lumbar curve and the iliac crest line, which reflects in part the relationship between spine and pelvis. Our finding indicated that patients with CK had significantly larger LPR. In other studies, some pelvic parameters were found to be associated with CK.23,24 These findings suggested that pelvic parameters may affect the alignment of the cervical spine and even the entire spine. This study indicated that AVT was associated with CK. Jiang et al.17 found that the increase of cervical tilt significantly positively correlated with the increase of AVT of thoracic curve, which suggested a correlation between cervical coronal alignment and AVT. La Maida et al.25 reported that in scoliosis surgery, the apical vertebral derotation and translation technique seemed to give less sagittal imbalance with a better cervical sagittal profile, which implied that decreased AVT may contribute to less cervical sagittal imbalance. Our results directly demonstrated the correlation between AVT and CK. AVT may be an important predictor of cervical spine pathology. Spinal balance is related to the spinal alignment. In this study, our results indicated that sagittal and coronal balance could influence the profile of cervical spine. In patients with CK, SVA was significantly smaller compared with patients with CL. Hiyama et al.15 observed a positive correlation between CL and SVA. Yagi et al.26 and Knott et al.27 reported similar results in their studies. Smith et al.22 found that higher SVA grades were associated with lower CK prevalence (0 ¼ 40%, þ ¼ 23%, þþ ¼ 11%), but greater cervical positive sagittal malalignment prevalence (0 ¼ 24%, þ ¼ 24%, þþ ¼ 48%). Relevant parameters of T1 vertebra have been reported as predictors of the status of the spine.16,23,24,28 Knott et al.27 reported that T1 slope was significantly correlated with SVA and could predict the sagittal balance of the spine. Pesenti et al.16 found that T1 slope and sagittal tilt are good indicators of postoperative changes for regional (CL and thoracic kyphosis) and global parameters. Our findings were inconsistent with these studies. In this study, patients with CK had significantly larger T1 slope than patients with CL. Moreover, increased T1 coronal tilt was positively correlated with CK. Taken together, sagittal and coronal parameters of T1 could influence the sagittal alignment of the cervical spine. There was a significant difference in the incidence of CK among different Lenke types. Lenke types 1, 2, and 4 had a higher incidence of CK compared with other Lenke types. A common denominator of Lenke types 1, 2, and 4 may be that they have thoracic hypokyphosis. Thoracic hypokyphosis may contribute to the development of CK. Furthermore, these 3 curve types have the major portion of the curve in the thoracic spine, leading to an upper spine three-dimensional deformity. There are some limitations to this study. First, this was a retrospective study, which may have resulted in some inherent biases. Second, we did not collect data regarding patients’ symptoms, and it is not clear if there is a relationship between CK and clinical symptoms. Third, owing to the limited sample size, analysis may have been underpowered in multiple subgroup analysis. Last, we focused only on the cervical sagittal alignment in patients before surgery in this study. We believe that the evaluation could have been more
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ORIGINAL ARTICLE YONG TANG ET AL.
CERVICAL KYPHOSIS IN PATIENTS WITH AIS
complete if postsurgery characteristics, such as cervical alignment, thoracic and lumbar curves, and pelvic parameters, were considered. CONCLUSIONS Several novel factors (LPR, AVT, and T1 coronal tilt) are correlated with CK in patients with AIS, demonstrating the
kyphosis after operative treatment of adolescent idiopathic scoliosis: a multicenter comparison of three surgical approaches. Spine (Phila Pa 1976). 2008;33:2630-2636.
REFERENCES 1. Lang C, Zou Q, Sui W, Deng Y, Huang Z, Yang J. Coronal deformity angular ratio may serve as a valuable parameter to predict in-brace correction in patients with adolescent idiopathic scoliosis [epub ahead of print]. Spine J. 2018. https://doi.org/ 10.1016/j.spinee.2018.12.002. 2. Lang C, Sui W, Di M, et al. Factors that influence in-brace correction in patients with adolescent idiopathic scoliosis. World Neurosurg. 2019;123: e597-e603. 3. Akbar M, Almansour H, Lafage R, et al. Sagittal alignment of the cervical spine in the setting of adolescent idiopathic scoliosis. J Neurosurg Spine. 2018;29:506-514. 4. Zhu C, Yang X, Zhou B, et al. Cervical kyphosis in patients with Lenke type 1 adolescent idiopathic scoliosis: the prediction of thoracic inlet angle. BMC Musculoskelet Disord. 2017;18:220. 5. Youn MS, Shin JK, Goh TS, Kang SS, Jeon WK, Lee JS. Relationship between cervical sagittal alignment and health-related quality of life in adolescent idiopathic scoliosis. Eur Spine J. 2016; 25:3114-3119. 6. Protopsaltis TS, Scheer JK, Terran JS, et al. How the neck affects the back: changes in regional cervical sagittal alignment correlate to HRQOL improvement in adult thoracolumbar deformity patients at 2-year follow-up. J Neurosurg Spine. 2015; 23:153-158. 7. Norheim EP, Carreon LY, Sucato DJ, Lenke LG, Glassman SD. Cervical spine compensation in adolescent idiopathic scoliosis. Spine Deform. 2015; 3:327-331. 8. Ito K, Imagama S, Ito Z, et al. Analysis of cervical kyphosis and spinal balance in young idiopathic scoliosis patients classified by the apex of thoracic kyphosis. Eur Spine J. 2016;25:3220-3225. 9. Hilibrand AS, Tannenbaum DA, Graziano GP, Loder RT, Hensinger RN. The sagittal alignment of the cervical spine in adolescent idiopathic scoliosis. J Pediatr Orthop. 1995;15:627-632. 10. Canavese F, Turcot K, De Rosa V, de Coulon G, Kaelin A. Cervical spine sagittal alignment variations following posterior spinal fusion and instrumentation for adolescent idiopathic scoliosis. Eur Spine J. 2011;20:1141-1148. 11. Sucato DJ, Agrawal S, O’Brien MF, Lowe TG, Richards SB, Lenke L. Restoration of thoracic
impact of coronal plane parameters on CK. MT Cobb angle, MTKA, SVA, LPR, and AVT are identified as independent risk factors of CK through the logistic regression model. The incidence of CK is higher in patients with AIS than normal subjects. Coronal parameters of the spine have an effect on cervical sagittal alignment.
12. Lowenstein JE, Matsumoto H, Vitale MG, et al. Coronal and sagittal plane correction in adolescent idiopathic scoliosis: a comparison between all pedicle screw versus hybrid thoracic hook lumbar screw constructs. Spine (Phila Pa 1976). 2007;32:448-452. 13. Stokes IA. Three-dimensional terminology of spinal deformity. A report presented to the Scoliosis Research Society by the Scoliosis Research Society Working Group on 3-D terminology of spinal deformity. Spine (Phila Pa 1976). 1994;19:236-248. 14. Yu M, Silvestre C, Mouton T, Rachkidi R, Zeng L, Roussouly P. Analysis of the cervical spine sagittal alignment in young idiopathic scoliosis: a morphological classification of 120 cases. Eur Spine J. 2013;22:2372-2381. 15. Hiyama A, Sakai D, Watanabe M, Katoh H, Sato M, Mochida J. Sagittal alignment of the cervical spine in adolescent idiopathic scoliosis: a comparative study of 42 adolescents with idiopathic scoliosis and 24 normal adolescents. Eur Spine J. 2016;25:3226-3233. 16. Pesenti S, Blondel B, Peltier E, Choufani E, Bollini G, Jouve JL. Interest of T1 parameters for sagittal alignment evaluation of adolescent idiopathic scoliosis patients. Eur Spine J. 2016;25: 424-429. 17. Jiang J, Qian BP, Qiu Y, Wang B, Yu Y, Zhu ZZ. Full fusion of proximal thoracic curve helps to prevent postoperative cervical tilt in Lenke type 2 adolescent idiopathic scoliosis patients with rightelevated shoulder. BMC Musculoskelet Disord. 2017; 18:362. 18. Katz DE, Durrani AA. Factors that influence outcome in bracing large curves in patients with adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2001;26:2354-2361. 19. Matsubayashi Y, Chikuda H, Oshima Y, et al. C7 sagittal vertical axis is the determinant of the C5C7 angle in cervical sagittal alignment. Spine J. 2017;17:622-626. 20. Hu X, Lieberman IH. Prevalence and factors affecting cervical deformity in adolescent idiopathic scoliosis patients: a single-center retrospective radiological study. Int J Spine Surg. 2018; 12:22-25.
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21. Wang L, Liu X. Cervical sagittal alignment in adolescent idiopathic scoliosis patients (Lenke type 1-6). J Orthop Sci. 2017;22:254-259. 22. Smith JS, Lafage V, Schwab FJ, et al. Prevalence and type of cervical deformity among 470 adults with thoracolumbar deformity. Spine (Phila Pa 1976). 2014;39:E1001-E1009. 23. Protopsaltis TS, Lafage R, Smith JS, et al. The lumbar pelvic angle, the lumbar component of the T1 pelvic angle, correlates with HRQOL, PI-LL mismatch, and it predicts global alignment. Spine (Phila Pa 1976). 2018;43:681-687. 24. Protopsaltis T, Terran J, Soroceanu A, et al. T1 slope minus cervical lordosis (TS-CL), the cervical answer to PI-LL, defines cervical sagittal deformity in patients undergoing thoracolumbar osteotomy. Int J Spine Surg. 2018;12:362-370. 25. La Maida GA, Peroni DR, Ferraro M, Della Valle A, Vitali C, Misaggi B. Apical vertebral derotation and translation (AVDT) for adolescent idiopathic scoliosis using screws and sublaminar bands: a safer concept for deformity correction. Eur Spine J. 2018;27:157-164. 26. Yagi M, Iizuka S, Hasegawa A, et al. Sagittal cervical alignment in adolescent idiopathic scoliosis. Spine Deform. 2014;2:122-130. 27. Knott PT, Mardjetko SM, Techy F. The use of the T1 sagittal angle in predicting overall sagittal balance of the spine. Spine J. 2010;10:994-998. 28. Tamai K, Romanu J, Grisdela P Jr, et al. Small C7T1 lordotic angle and muscle degeneration at C7 level were independent radiological characteristics of patients with cervical imbalance: a propensity score-matched analysis. Spine J. 2018;18:1505-1512.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 27 December 2018; accepted 26 March 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.264 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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