Brace Treatment in Adolescent Idiopathic Scoliosis Patients with Curve Between 40° and 45°: Effectiveness and Related Factors

Brace Treatment in Adolescent Idiopathic Scoliosis Patients with Curve Between 40° and 45°: Effectiveness and Related Factors

Original Article Brace Treatment in Adolescent Idiopathic Scoliosis Patients with Curve Between 40 and 45 : Effectiveness and Related Factors Leile...

653KB Sizes 0 Downloads 45 Views

Original Article

Brace Treatment in Adolescent Idiopathic Scoliosis Patients with Curve Between 40 and 45 : Effectiveness and Related Factors Leilei Xu1, Xianfeng Yang2, Yuwen Wang1, Zhichong Wu1, Chao Xia1, Yong Qiu1, Zezhang Zhu1

OBJECTIVE: To investigate effectiveness of brace treatment in patients with adolescent idiopathic scoliosis with curve between 40 and 45 and to determine predictive factors associated with bracing outcome.

-

METHODS: Bracing was used to treat 90 patients with curve >40 degrees. Factors including Risser sign, age, sex, curve pattern, curve magnitude, and initial curve correction were compared between patients with curve improvement and patients with curve progression. Logistic regression analysis was used to determine the independent predictors of curve progression.

-

RESULTS: Curve was improved in 34 (37.8%) patients and stabilized in 12 (13.3%) patients. Remarkable curve progression >50 degrees was observed in 44 (48.9%) patients. Intergroup comparison showed significant differences between the 2 groups in terms of age (12.3  1.4 years vs. 13.2  1.6 years, P [ 0.01), initial curve correction (2.2%  5.4% vs. 19.7%  12.2%, P < 0.001), and curve pattern (P [ 0.03). Logistic regression analysis showed that initial curve correction of <10% (odds ratio [ 12.82, P < 0.001) and Risser grade of 0 (odds ratio [ 1.46, P [ 0.04) were significant indicators of curve progression.

-

CONCLUSIONS: Bracing may produce a favorable outcome in certain patients with curve between 40 and 45 . It should be cautiously used in this situation, as there was a higher probability of bracing failure. It is important to differentiate patients at high risk of curve progression at an early stage to avoid overtreatment.

-

Key words Brace treatment - Effectiveness - Factors - Idiopathic scoliosis - Large curve -

Abbreviations and Acronyms AIS: Adolescent idiopathic scoliosis BMI: Body mass index ICR: Initial curve correction T-curve: Thoracic curve

WORLD NEUROSURGERY -: e1-e6, - 2019

INTRODUCTION

A

dolescent idiopathic scoliosis (AIS) is a common spinal deformity that occurs during puberty.1 As evidenced by earlier research of natural history of AIS, patients with AIS may experience curve progression during the growth period.2,3 A few risk factors have been identified to be associated with curve progression, such as young chronologic age, skeletal immaturity, and curve pattern.4-7 In view of this progressive nature, it is essential to treat patients with AIS with conservative interventions at the time of initial diagnosis, especially for patients with remaining growth potential. Bracing has widely been applied in the conservative treatment of AIS.8-11 The literature has supported the use of bracing to control curve progression in patients with AIS and thus decrease the likelihood of surgery.8-11 The Bracing in Adolescent Idiopathic Scoliosis Trial (BrAIST) showed that 28% of the patients with brace treatment had curve progression to the extent requiring surgical intervention, whereas this rate was 52% in patients with observation only.12 Another large multicenter randomized controlled trial showed that the success rate was 75% among patients with brace treatment compared with a success rate of 42% among patients randomly assigned to observation, which suggested the superiority of bracing to observation.13 In previous studies, brace treatment was prescribed to patients when the curve magnitude was between 20 and 40 .14,15 When confronted with curve >40 , many spinal surgeons may recommend correction surgery. At the present time, with the development of new surgical techniques and implants, it is possible to postpone surgery even when the curve has >40 , so as to gain more time for full growth of the spine. As reported more recently, the indication for surgery has been proposed as a curve of >50 .3,12,13 However, patients with an initial curve of >40 not uncommonly receive brace treatment at diagnosis. Recently,

From the Departments of 1Spine Surgery and 2Radiology, the Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, China To whom correspondence should be addressed: Zezhang Zhu, M.D. [E-mail: [email protected]] Leilei Xu and Xianfeng Yang are coefirst authors. Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.008 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.

www.journals.elsevier.com/world-neurosurgery

e1

ORIGINAL ARTICLE LEILEI XU ET AL.

BRACING EFFECTIVENESS IN LARGE CURVES

several studies have shown that brace treatment may be applicable to patients with curve >40 .11,16,17 However, with studies limited by small sample sizes and short follow-up periods, factors related to the effectiveness of bracing in curve >40 remain obscure. The purpose of our study was to investigate the effectiveness of brace treatment in patients with AIS with curve >40 and to further determine the factors predictive of bracing outcome in these patients.

Table 1. Demographic Data of Patients Variables

Initial Visit

Final Follow-Up

Age, years

12.6  1.3

16.3  1.8

Menarche age, years Curve magnitude,



Arm span, cm 2

Body mass index, kg/m

MATERIALS AND METHODS Subjects The study received approval of the local institutional review board. A total of 3283 patients with AIS prescribed brace treatment from January 2005 to May 2016 were reviewed. Inclusion criteria were as follows: 1) an initial curve between 40 and 45 ; 2) skeletal immaturity with a Risser stage of 0e3; 3) no treatment before the diagnosis; 4) a minimum of 1 year of follow-up after completion of brace treatment; 5) bracing compliance >90%. Finally, 90 patients were included in the current study. The baseline characteristics of the patients, including sex, age at menarche, and status of triradiate cartilage, were collected from the medical records. Body mass index (BMI) was calculated by dividing the weight with square of the height. The guardians of all the patients signed the informed consent for the clinical data to be used for research purposes. Strategy of Brace Treatment The patients were instructed to wear a Boston brace for 22 hours per day after the initial visit. Patients were regularly evaluated every 3e5 months until the endpoint of bracing, which was set as follows: 1) reaching skeletal maturity with the curve well controlled or 2) curve progression >50 and surgical intervention recommended. At each visit, guardians of the patients were asked about the actual time spent wearing the brace. The proportion of actual wearing time to the instructed time was calculated to determine compliance. X-ray films of the whole spine were obtained for radiographic evaluations, including curve magnitude, curve pattern, and Risser stage. Curve pattern was recorded as main thoracic curve (T-curve), double major curve, and major lumbar curve. Specifically, the latter 2 curve types were summarized as noneT-curve for the convenience of analysis.18 Initial curve correction (ICR) was calculated according to the following formula as reported previously:

1.3  0.8

4.5  1.6

42.5  2.1

42.1  8.7

153  9.9

156.9  7.5

17.1  2.1

17.9  1.8

BMI, and ICR were compared between patients with curve improvement and patients with curve progression using the Student t test. Patients were then further dichotomized according to sex (male or female), curve pattern (T-curve or noneT-curve), Risser grade (0 or 1), and ICR (<10% or 10%). The rate of curve progression was compared between these subgroups using the c2 test. Logistic regression analysis was used to determine the independent predictor of curve progression. A P value < 0.05 was considered statistically significant. RESULTS Baseline Characteristics of Patients The study enrolled 14 male and 76 female patients with an average age 12.6  1.3 years old. Demographic data of the patients are summarized in Table 1. Of patients, 74.4% (67 of 90) had gone beyond their peak height velocity at their first visit to our scoliosis clinic. The average menarche age was 1.3  0.8 years. There were 46 patients with Risser grade 0, 13 with Risser grade 1, 17 with Risser grade 2, and 14 with Risser grade 3. Of patients, 52 had main T-curve, 11 had double major curve, and 27 had single lumbar curve. The mean initial curve magnitude was 42.5  2.1 . At the first visit after bracing, the average curve magnitude was decreased to 37.2  2.1 , with a mean ICR of 8.8%. At the completion of brace treatment, the mean curve magnitude was 42.1  8.7 . The mean duration of bracing was 2.4  1.3 years, with average follow-up duration of 1.3  0.4 years. Incidence of Curve Progression and Related Factors At the final follow-up, the curve were improved in 34 (37.8%) patients and stabilized in 12 (13.3%) patients (Figure 1). In 44

ICR ¼ ð½Cobb angle before brace wearing  ½Cobb angle 3 months after brace wearingÞ =Cobb angle before brace wearing  100%

At the final follow-up, curve progression was identified if the curve magnitude was increased >5 , and curve improvement was identified if the curve magnitude decreased >5 . The curve was considered stable if the change of curve magnitude was within 5 . Statistical Analysis IBM SPSS Version 19.0 software was used for statistical analysis. Factors including initial age, sex, curve pattern, curve magnitude,

e2

www.SCIENCEDIRECT.com

(48.9%) patients, remarkable curve progression >50 was observed. By the end of the last follow-up, 51 (56.7%) patients received correction surgery. The variables sex, menarche age, initial age, BMI, ICR, initial curve magnitude, and curve pattern were compared between the curve progression group and curve improvement group. As shown in Table 2, significant differences between the 2 groups were found in terms of age (12.3  1.4 years vs. 13.2  1.6 years, P ¼ 0.01), menarche age (1.1  0.5

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.008

ORIGINAL ARTICLE LEILEI XU ET AL.

BRACING EFFECTIVENESS IN LARGE CURVES

Figure 1. Successful brace treatment of a patient with curve >40 degrees. (A and B) Adolescent idiopathic scoliosis with a major thoracic curve of 45 was diagnosed in a 13-year-old girl. The initial Risser score was grade 2. (C and D) A Boston brace was used 22 hours per day to control the curve. At 5 months after bracing, the curve magnitude decreased to 32 . The initial

years vs. 1.5  0.9 years, P ¼ 0.01), ICR (2.2%  5.4% vs. 19.7%  12.2%, P < 0.001), and curve pattern (P ¼ 0.03). There was no remarkable difference between the 2 groups for the variables initial curve magnitude, sex, and BMI.

Table 2. Intergroup Comparison Between Patients with Curve Improvement and with Curve Progression Variables

Curve Progression (n [ 44)

Curve Improvement (n [ 34)

P

Age, years

12.3  1.4

13.2  1.6

0.01

Menarche age, years

1.1  0.5

1.5  0.9

0.01

Curve magnitude,



Initial visit

42.1  2.8

43.1  3.0

0.17

First visit after bracing

39.3  4.1

32.1  4.3

0.01

Final follow-up

51.2  2.6

33.5  2.3

<0.001

Body mass index, kg/m2

16.9  2.2

17.1  1.9

0.76

ICR, %

2.2  5.4

19.7  12.2

<0.001

Curve type

0.03

T-curve, n ¼ 42

29

13

NoneT-curve, n ¼ 36

15

21

correction rate was 28.9%. (E and F) At 10 months after bracing, the curve magnitude was 34 . Both coronal and sagittal profiles were well maintained. (G and H) At the final follow-up (2 years 6 months after bracing), the Cobb angle was 26 .

Table 3 summarized the incidence of curve progression in patients with different Risser grade or ICR. Regarding the distribution of ICR, 35.6% of patients were <0%, 18.9% patients were between 0% and 10%, 22.2% patients were between 10% and 20%, 14.4% patients were between 20% and 30%, and 8.9% patients were >30%. Patients with lower Risser grade or less ICR were found to have a significantly higher incidence of curve progression (P ¼ 0.04 for Risser grade; P ¼ 0.001 for ICR). As shown in Figure 2, patients with Risser grade of 0 and ICR of 10% had the highest incidence of curve progression (70.9%).

Table 3. Incidence of Curve Progression in Patients in Risser Grade and Initial Correction Rate Subgroups Curve Progression Risser grade

0.04

0, n ¼ 51

31 (60.8%)

1, n ¼ 13

6 (46.1%)

2, n ¼ 16

5 (31.3%)

3, n ¼ 10

2 (20.0%)

ICR

0.001

0%, n ¼ 32

23 (71.8%)

0%e10%, n ¼ 17

10 (58.8%)

10%e20%, n ¼ 20

8 (40.0%)

Male, n ¼ 10

6

4

20%e30%, n ¼ 1

2 (15.4%)

Female, n ¼ 68

38

30

>30%, n ¼ 8

1 (12.5%)

Sex

0.92

ICR, initial correction rate; T-curve, thoracic curve.

WORLD NEUROSURGERY -: e1-e6, - 2019

P

ICR, initial correction rate.

www.journals.elsevier.com/world-neurosurgery

e3

ORIGINAL ARTICLE LEILEI XU ET AL.

BRACING EFFECTIVENESS IN LARGE CURVES

Figure 2. Incidence of curve progression in patients with different Risser grade or initial curve correction (ICR). The incidence of curve progression was significantly higher in patients with low Risser grade or less ICR. A combination of Risser grade of 0 and ICR of

Logistic Regression Analysis Four factors, Risser grade, initial age, ICR, and curve pattern, were enrolled in the logistic regression analysis. As shown in Table 4, ICR of <10% (odds ratio ¼ 12.82, P < 0.001) and Risser grade of 0 (odds ratio ¼ 1.46, P ¼ 0.04) were found to be significant indicators of curve progression. Regarding initial age and curve pattern, no significant association with the bracing outcome was found. With ICR and Risser grade included in the regression model, the sensitivity and the specificity for curve progression were 80.4% and 71.4%, respectively. The value of Cox-Snell R2 was 0.309, suggesting that the model can explain approximately 30.9% of the overall variance. DISCUSSION Numerous studies have been performed to evaluate the efficacy of bracing in patients with AIS. It has been well documented that Table 4. Logistic Regression Model Variables

Regression Coefficient

P

OR

95% CI

Age

0.30

0.21

1.41

0.35e5.21

Risser sign

0.35

0.04

1.46

0.89e2.15

ICR

2.54

<0.001

12.82

3.57e35.5

Curve type

0.42

0.17

2.13

0.64e8.02

OR, odds ratio; CI, confidence interval; ICR, initial correction rate.

e4

www.SCIENCEDIRECT.com

10% was indicative of the highest incidence of curve progression (70.9%). By contrast, a combination of Risser grade 1 and ICR >10% was indicative of the lowest incidence of curve progression (9.5%). ICR, initial curve correction.

bracing can effectively alter the natural history of the curve and prevent the need for surgical interventions.10,14,19,20 For patients with curve magnitude >40 , however, there was less evidence supporting the use of brace treatment in this cohort. In this study, we investigated the ability to correct curves >40 through brace treatment in 90 patients. Of these patients, 34 (37.8%) were successfully treated with the curve improved >5 . Similar to the current study, 2 earlier studies have also investigated the efficacy of brace treatment in curves >40 .16,17 Negrini et al.17 reported 20 of 28 (71.4%) patients had remarkable curve improvement. Aulisa et al.16 summarized bracing outcome in 104 patients and observed that 78% of these patients could obtain curve correction. Based on these findings, we confirmed that some patients with curves >40 may benefit from brace treatment. For such patients, it may be an option to control the curve through bracing, especially for patients who strongly wish to avoid surgical interventions. It is noteworthy that 44 (48.9%) patients in our study had remarkable curve progression >50 . By contrast, for patients with an initial curve between 20 and 40 , the incidence of curve progression at the completion of bracing was reported to be 18.0%e 30.3%.12,13,18,21 Katz et al.21 investigated the efficacy of bracing in 100 patients with AIS and reported that the incidence of bracing failure was 18%. Thompson et al.18 reviewed 168 patients with high compliance to brace treatment. They observed that the rate of progression to 50 was 30.3% in main T-curves and 5.3% in main lumbar curves. Apparently, when treating curves >40 at the initial visit, there could be an obvious decline in the bracing effectiveness. Therefore, it is important to differentiate patients at high risk of curve progression to avoid overtreatment.

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.008

ORIGINAL ARTICLE LEILEI XU ET AL.

BRACING EFFECTIVENESS IN LARGE CURVES

Previous studies have revealed many factors related to the outcome of bracing. Karol et al.22 reviewed a large number of patients at various Risser stages who received brace treatment. They found that patients at Risser stage 0, especially with open triradiate cartilage, may be at highest risk for bracing failure. Thompson et al.18 compared the effectiveness of bracing in patients with different curve types and reported that patients with T-curves are at greater risk of curve progression than patients with lumbar curves. Aulisa et al.16 found that vertebral rotation and growth potential could be used to predict the final bracing outcome. In line with these studies, we observed that patients with low Risser grade, main T-curve, low ICR, and low initial age had significantly higher incidence of curve progression. To further determine the independent factors of curve progression, we performed logistic regression analysis and found that initial Risser grade of 0 and ICR of <10% were significantly associated with curve progression, with odds ratio of 1.45 and 12.82, respectively. Therefore, close observation of patients with Risser grade 0 is warranted to detect potential curve progression in an early stage. Especially for patients with a weak response to bracing as indicated by ICR <10%, high risk of bracing failure should be disclosed to the patients. The current study shed light on the gray zone of brace treatment where surgeons need to break the conventional rules. On the basis of scientific evidence shown by our study and other published data, it is feasible to control curves >40 through brace treatment. However, it remains a great challenge to differentiate patients who are resistant to bracing before the initiation of treatment. Therefore, patients

and their guardians should be informed of the high possibility of bracing failure before the initiation of treatment. The present study has several limitations. First, some patients were excluded from the study for incomplete follow-up, which could potentially bias the statistics of bracing outcome. Second, subjective report of daily braced time was used to determine the compliance in our study. Recently, a heat sensor that objectively measured the exact number of hours of brace wear has been applied to clinical practice.23 In future studies, more patients treated by brace fitted with a heat sensor need to be included to facilitate a more reliable conclusion. Third, determination of the maturity is fundamental for bracing in patients with AIS. Predictors of maturity, such as thumb ossification composite index and digital skeletal age, have been reported in previous studies.24,25 However, owing to the inherent limitation of the retrospective nature of this study, these maturity predictors were not evaluated. In future studies, more predictors of maturity should be assessed to better determine the effectiveness of bracing. CONCLUSIONS Brace treatment may produce a favorable outcome in certain patients with curve between 40 and 45 . It should be cautiously used in this situation, however, as there was a higher probability of bracing failure. An initial Risser grade of 0 and ICR of <10% are strongly predictive of curve progression in this situation. It is important to differentiate patients at high risk of curve progression at an early stage to avoid overtreatment.

Study of the Scoliosis Research Society. J Bone Joint Surg Am. 1995;77:823-827.

REFERENCES

13. Weinstein SL, Dolan LA, Wright JG, Dobbs MB. Effects of bracing in adolescents with idiopathic scoliosis. N Engl J Med. 2013;369:1512-1521.

1. Weinstein SL, Dolan LA. The evidence base for the prognosis and treatment of adolescent idiopathic scoliosis: The 2015 Orthopaedic Research and Education Foundation Clinical Research Award. J Bone Joint Surg Am. 2015;97:1899-1903.

7. Ryan PM, Puttler EG, Stotler WM, Ferguson RL. Role of the triradiate cartilage in predicting curve progression in adolescent idiopathic scoliosis. J Pediatr Orthop. 2007;27:671-676.

2. Agabegi SS, Kazemi N, Sturm PF, Mehlman CT. Natural history of adolescent idiopathic scoliosis in skeletally mature patients: a critical review. J Am Acad Orthop Surg. 2015;23:714-723.

8. Goldberg CJ, Moore DP, Fogarty EE, Dowling FE. Adolescent idiopathic scoliosis: the effect of brace treatment on the incidence of surgery. Spine (Phila Pa 1976). 2001;26:42-47.

3. Danielsson AJ. Natural history of adolescent idiopathic scoliosis: a tool for guidance in decision of surgery of curves above 50 degrees. J Child Orthop. 2013;7:37-41.

9. Xu L, Qin X, Qiu Y, Zhu Z. Initial correction rate can be predictive of the outcome of brace treatment in patients with adolescent idiopathic scoliosis. Clin Spine Surg. 2017;30:E475-E479.

4. Busscher I, Wapstra FH, Veldhuizen AG. Predicting growth and curve progression in the individual patient with adolescent idiopathic scoliosis: design of a prospective longitudinal cohort study. BMC Musculoskelet Disord. 2010;11:93.

10. Yrjonen T, Ylikoski M, Schlenzka D, Poussa M. Results of brace treatment of adolescent idiopathic scoliosis in boys compared with girls: a retrospective study of 102 patients treated with the Boston brace. Eur Spine J. 2007;16:393-397.

5. Hung VW, Qin L, Cheung CS, et al. Osteopenia: a new prognostic factor of curve progression in adolescent idiopathic scoliosis. J Bone Joint Surg Am. 2005;87:2709-2716.

11. Zhu Z, Xu L, Jiang L, et al. Is brace treatment appropriate for adolescent idiopathic scoliosis patients refusing surgery with Cobb angle between 40 and 50 degrees. Clin Spine Surg. 2017;30:85-89.

17. Negrini S, Negrini F, Fusco C, Zaina F. Idiopathic scoliosis patients with curves more than 45 Cobb degrees refusing surgery can be effectively treated through bracing with curve improvements. Spine J. 2011;11:369-380.

6. Peterson LE, Nachemson AL. Prediction of progression of the curve in girls who have adolescent idiopathic scoliosis of moderate severity. Logistic regression analysis based on data from The Brace

12. Weinstein SL, Dolan LA, Wright JG, Dobbs MB. Design of the Bracing in Adolescent Idiopathic Scoliosis Trial (BrAIST). Spine (Phila Pa 1976). 2013; 38:1832-1841.

18. Thompson RM, Hubbard EW, Jo CH, Virostek D, Karol LA. Brace success is related to curve type in patients with adolescent idiopathic scoliosis. J Bone Joint Surg Am. 2017;99:923-928.

WORLD NEUROSURGERY -: e1-e6, - 2019

14. Richards BS, Bernstein RM, D’Amato CR, Thompson GH. Standardization of criteria for adolescent idiopathic scoliosis brace studies: SRS Committee on Bracing and Nonoperative Management. Spine (Phila Pa 1976). 2005;30:2068-2075 [discussion: 2076-2077]. 15. Stokes OM, Luk KD. The current status of bracing for patients with adolescent idiopathic scoliosis. Bone Joint J. 2013;95B:1308-1316. 16. Aulisa AG, Guzzanti V, Falciglia F, Giordano M, Galli M, Aulisa L. Brace treatment of idiopathic scoliosis is effective for a curve over 40 degrees, but is the evaluation of Cobb angle the only parameter for the indication of treatment? [e-pub ahead of print] Eur J Phys Rehabil Med https://doi.org/10.23736/S19739087.18.04782-2. Accessed March 7, 2018.

www.journals.elsevier.com/world-neurosurgery

e5

ORIGINAL ARTICLE LEILEI XU ET AL.

19. Upadhyay SS, Nelson IW, Ho EK, Hsu LC, Leong JC. New prognostic factors to predict the final outcome of brace treatment in adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 1995;20: 537-545. 20. Zheng X, Sun X, Qian B, et al. Evolution of the curve patterns during brace treatment for adolescent idiopathic scoliosis. Eur Spine J. 2012;21: 1157-1164. 21. Katz DE, Herring JA, Browne RH, Kelly DM, Birch JG. Brace wear control of curve progression in adolescent idiopathic scoliosis. J Bone Joint Surg Am. 2010;92:1343-1352. 22. Karol LA, Virostek D, Felton K, Jo C, Butler L. The effect of the Risser stage on bracing outcome in

e6

www.SCIENCEDIRECT.com

BRACING EFFECTIVENESS IN LARGE CURVES

adolescent idiopathic scoliosis. J Bone Joint Surg Am. 2016;98:1253-1259. 23. Karol LA, Virostek D, Felton K, Wheeler L. Effect of compliance counseling on brace use and success in patients with adolescent idiopathic scoliosis. J Bone Joint Surg Am. 2016;98:9-14.

Chinese female idiopathic scoliosis. Spine (Phila Pa 1976). 2007;32:1648-1654.

Conflict of interest statement: This work was supported by the National Natural Science Foundation of China (Grant Nos. 81501849 and No. 81201385).

24. Hung ALH, Chau WW, Shi B, et al. Thumb Ossification Composite Index (TOCI) for predicting peripubertal skeletal maturity and peak height velocity in idiopathic scoliosis: a validation study of premenarchal girls with adolescent idiopathic scoliosis followed longitudinally until skeletal maturity. J Bone Joint Surg Am. 2017;99:1438-1446.

Received 21 January 2019; accepted 2 March 2019

25. Wang S, Qiu Y, Ma Z, Xia C, Zhu F, Zhu Z. Histologic, Risser sign, and digital skeletal age evaluation for residual spine growth potential in

1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.008 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.008