Introduction

Idiopathic scoliosis (IS) is a three-dimensional distortion of the vertebral column with more than a 10° Cobb angle in the radiological examination. It is a disease with unknown etiology. The decision as to treatment (surgical vs non-surgical) is based on deformation magnitude and progression risk prognosis. Such prognosis can be established on the basis of skeletal maturity and remaining growth potential. Overtreatment or undertreatment can be an issue in IS management [1]. The incorrect assessment of the progression risk may result in a delay in treatment and increase spine deformity.
A discrepancy between chronological and biological age is quite a common phenomenon in pediatric orthopedics. Bone age is most commonly used as an equivalent of biological age. There is a large variability of the pediatric population that makes the assessment of biological age one of the key points in defining the biological status of the patient. Several radiological methods have been described to assess bone age [2-6]. Most of them refer to the presence of the primary or secondary ossification centers within the bones of the axial or limb skeleton. Some of them require additional radiograms, therefore they increase radiological exposure [7,4,5]. The Risser sign allows to assess iliac apophysis and is used in daily orthopedic practice. However, it has a drawback of missing the early phases of growth acceleration in adolescent patients [8]. Any way that enhances the accuracy of the assessment of progression risk could be useful in preventing IS undertreatment or overtreatment.
The Sanders Maturity Scale (SMS) relies on the ossification of phalanges, metacarpal bones, and radius, as shown in table 1. It was proposed by the author as a method that facilitates the stratification of progression risk in IS [9]. The method described by Sanders and co-authors is becoming more widely used worldwide, however it is still not prevalent. Moreover, the original method by Sanders et al., was developed on the USA population, while there is no data concerning the use of the SMS on the Caucasian Central European population.

Aim

The aim of the study was to compare the SMS to other, used in daily practice, skeletal maturity assessment methods.
Materials and methods

Materials
In this retrospective study the radiograms and medical data of female adolescent patients with idiopathic scoliosis treated at our department between 2018 and 2022 were reviewed. All consecutive girls who had a standing scoliosis radiogram and a left-hand radiogram, both taken during the same hospital stay, were included. Patients whose triradiate cartilage or iliac apophysis could not be seen on the radiograms were excluded. All patients were referred to the department for operative treatment of spine deformity. If the patient was hospitalized twice or more, and the gap between the two stays was longer than 6 months, each stay was counted as a new case. We reviewed the medical data of 40 patients (54 series of radiograms). Finally, we included 39 female patients (50 series of radiograms) who met inclusion criteria, with a mean age of 13.4, ranging from 10.3 to 17.3 (SD = 1.58).

Methods
Each case was evaluated for skeletal maturity by three observers. The observers had different experience with skeletal maturity assessment: the first observer had no experience (a medical student), the second observer was familiar with the methods (a resident), and the third observer was experienced with different methods of skeletal maturity assessment (an orthopedic surgeon). The first author evaluated each case twice, at a 6-week interval to evaluate for intra-observer reliability.
Skeletal maturity was assessed using the Sanders Maturity Scale (SMS), the Risser sign, the Greulich and Pyle (GP) Radiographic Atlas of Skeletal Development of the Hand and Wrist, as well as the closure of the triradiate cartilage. The triradiate cartilage and Risser sign were evaluated on AP pelvis radiograms, visible on scoliosis radiograms. The triradiate cartilage was rated as: open or closed, or closing (medial cortical closed, lateral open). Iliac apophysis ossification (the Risser sign) was classified from 0 to 5, as presented in its original form [10]. Skeletal maturity assessment according to SMS or GP were assessed on an AP non-dominant hand radiogram. For the SMS, the radiograms were classified as one through to the eighth stage of maturation (Fig 1). The GP method allows to match the patient’s hand radiogram with a standard age specific hand radiogram presented in the GP atlas.
The SMS, the GP, the Risser sign, and the triradiate cartilage closure were tested for intra-observer and inter-observer reliability. Intra-observer and inter-observer reliability were analyzed with Krippendorf’s alpha. Statistical analysis was performed with the use of STATISTICA.
Results

The Results of the Skeletal Maturity Assessment
The number and percentage of cases for each Risser stage were as follows: Risser 0-20 cases (40%), Risser 1-5 cases (10%), Risser 2-4 cases (8%), Risser 3-7 cases (14%), Risser 4-11 cases (22%), Risser 5-3 cases (6%). On most of the radiograms (43/50, 84%), the triradiate cartilage was rated as closed, the rest of cases was rated as open. The hand radiograms were rated according to the SMS as follows: Sanders 1-0 cases, Sanders 2-2 cases (4%), Sanders 3-17 cases (34%), Sanders 4-3 cases (6%), Sanders 5-3 cases (6%), Sanders 6-9 cases (18%), Sanders 7-12 cases (24%), Sanders 8-4 cases (8%). Risser vs SMS staging is presented in table 1 and 2. 19 out of 22 (86,36%) Sanders 2, 3, or 4 cases were rated as Risser 0, whereas 16 out of 20 (80%) Risser 0 cases were rated as Sander 3.
Patients with an open triradiate were aged 11.7 +- 1.1. All radiograms with an open triradiate cartilage were rated as Sanders 2 or 3 (2 cases of Sanders 2, and 5 cases of Sanders 3); they all received Risser 0 grading (7 cases). Patients with a closed triradiate were aged 13.6 +- 1.5. Radiograms with a closed triradiate cartilage were rated as Sanders 3 through Sanders 8 in SMS, and Risser 0 through 5 (Fig. 1 and 2).
Figure 3 shows periods according to GP bone age at which each stage of the SMS and Risser sign occurs.
Intra-observer and inter-observer reliability
A very good intra-observer reliability for the SMS (alpha = 0.97), the Risser sign (alpha = 0.96) and GP (alpha = 0.95) was found, while for the triradiate closure a lower intra-observer reliability (alpha=0.79) was noted. Inter-observer reliability for SMS showed very good agreement (alpha = 0.96), as well as for the Risser sign (0.91) and the GP method (0.95); while the inter-observer reliability test for triradiate closure evaluation showed a low level of agreement (alpha = 0.55).

The correlation between methods of skeletal maturity assessment.
The Spearman correlation for the SMS vs the Risser sign showed a very strong correlation (rho = 0.878, p < 0.001) (Fig. 4), as well as the SMS vs the GP method (rho = 0.959, p < 0.001). The correlation between the SMS vs triradiate closure evaluation showed a moderate correlation (rho = 0.496, p < 0.001).

Discussion

The SMS method was recently introduced in our department, thus we aimed to compare the assessment provided by observers with different levels of experience, to determine the difficulty of each method. Krippendorf’s alpha was chosen to determine intra-observer and inter-observer reliability. It allows to analyze ordinal data provided by more than 2 observers. Krippendorf’s alpha equal 1 signifies the strongest agreement, and 0 signifies the strongest disagreement. Krippendorf’s alpha above 0.80 are considered good, and above 0.95 as very good, while between 0.67 and 0.80 are acceptable only when tentative conclusions are acceptable [11,12]. Each skeletal maturity assessment method, beside the triradiate closure evaluation, showed good or very good intra-observer and inter-observer reliability. Previous papers reported on a high reliability as well as strong correlation between the SMS and other methods including the Risser system [3,7,13,14].
Our study showed that a great number of patients was at an early stage of maturation. The most predominant SMS stage was Sanders 3 (17 cases, 34 %), and the most predominant Risser grade was Risser 0 (20 cases, 40%). The drawbacks of Risser sign grading was depicted in our results (Tab. 1,2 and Fig. 3). The Risser sign evaluation was not accurate enough to show the stage of skeletal maturation of patients in early adolescence. On the other hand, the SMS allows to categorize them with additional stages. Triradiate cartilage closure assessment provides another marker at that early phase of maturation, but in comparison with the SMS it turned out not to have good intra-observer and inter-observer reliability.
The question is whether it is justified to expose the patient to additional radiation. The hand radiograph provides the effective dose of radiation between 0.0001-0.1 mSV, which can be considered a safe dose, corresponding to less than 20 minutes of natural background radiation [15]. Another argument for the use of the hand radiograph is to increase the accuracy of skeletal age assessment. Relying only on one method in assessing bone age might be insufficient and lead to a delay in operative treatment. Especially for Risser 0 patients there exists a wide range of uncertainty regarding the progression risk of spinal deformity. In our study Risser 0 corresponded with as many as four Sanders stages. By applying the SMS method, Risser 0 patients could be classified into subcategories which may enhance maturity stratification. The SMS together with the Cobb angle have a potential to become a predictive value for the curve progression risk in IS [9,16,17]. A significant difference in progression risk of IS patients with Sanders 1, 2, 3 or 4+ stages was shown by Dolan et al. in 2019 [16]. However, Swany et al. noticed the method might cause some difficulties delineating SMS stages 2 through 4 that are essential when assessing adolescent growth [18]. These difficulties have not been depicted in our material.

Conclusions

The Sanders Maturity Scale is a useful method in assessing bone age among children with scoliosis. It is easy to be used by physicians and does not require an atlas. The method is characterized by a very good intra-observer and inter-observer reliability. Its main advantage is a wider range of stages comparing to the Risser method that is commonly used. Currently, most clinical and radiographic markers do not help pediatric orthopedic surgeons to clearly distinguish maturity levels prior to Risser 1, which is essential to qualify a patient for operative or brace treatment. The Sanders Maturity Scale enhances the assessment of skeletal maturity in IS patients by providing additional stages in the early phase of growth.

References

1. Kotwicki T, Chowanska J, Kinel E et al.: Optimal management of idiopathic scoliosis in adolescence. Adolesc. Health. Med. Ther. 2013.
2. Canavese F, Charles YP, Dimeglio A: Skeletal age assessment from elbow radiographs. Review of the literature. Chir. Organi. Mov. 2008.
3. Nicholson AD, Sanders JO, Liu RW et al.: The relationship of calcaneal apophyseal ossification and sanders hand scores to the timing of peak height velocity in adolescents. Bone Jt. J. 2015.
4. O’Connor JE, Coyle J, Spence LD et al.: Epiphyseal maturity indicators at the knee and their relationship to chronological age: Results of an Irish population study. Clin. Anat. 2013.
5. O’Connor JE, Bogue C, Spence LD, et al.: A method to establish the relationship between chronological age and stage of union from radiographic assessment of epiphyseal fusion at the knee: an Irish population study. J Anat. 2008.
6. Li DT, Cui JJ, Devries S et al.: Humeral Head Ossification Predicts Peak Height Velocity Timing and Percentage of Growth Remaining in Children. J. Pediatr. Orthop. 2018.
7. Neal KM, Shirley ED, Kiebzak GM: Maturity Indicators and Adolescent Idiopathic Scoliosis. Spine (Phila Pa 1976) 2018.
8. Dimeglio A, Canavese F: Progression or not progression? How to deal with adolescent idiopathic scoliosis during puberty. J. Child Orthop. 2013.
9. Sanders JO, Khoury JG, Kishan S et al.: Predicting scoliosis progression from skeletal maturity: a simplified classification during adolescence. J. Bone Joint Surg. Am. 2008.
10. Kotwicki T: Improved accuracy in Risser sign grading with lateral spinal radiography. Eur. Spine J. 2008.
11. Stephanie G: “Krippendorff’s Alpha Reliability Estimate: Simple Definition” https://www.statisticshowto.com/krippendorffs-alpha/.
12. Hayes A, Krippendorff K: Answering the Call for a Standard Reliability Measure for Coding Data, Communication Methods and Measures. 2007 1:1, 77-89.
13. Vira S, Husain Q, Jalai C, Paul J et al.: The Interobserver and Intraobserver Reliability of the Sanders Classification Versus the Risser Stage. J. Pediatr. Orthop. 2017.
14. Li DT, Linderman GC, Cui JJ et al.: The Proximal Humeral Ossification System Improves Assessment of Maturity in Patients with Scoliosis. J. Bone Joint Surg. Am. 2019.
15. Mughal AM, Hassan N, Ahmed A: Bone Age Assessment Methods: A Critical Review. Pakistan J. Med. Sci. 2014.
16. Dolan L et al.: Bracing in Adolescent Idiopathic Scoliosis Trial (BrAIST): Development and Validation of a Prognostic Model in Untreated Adolescent Idiopathic Scoliosis Using the Simplified Skeletal Maturity System. Spine Deform. 2019.
17. Johnson MA, Flynn JM, Anari JB et al. Risk of Scoliosis Progression in Nonoperatively Treated Adolescent Idiopathic Scoliosis Based on Skeletal Maturity. J. Pediatr. Orthop. 2021.
18. Swany LM, Larson AN, Milbrandt TA et al.: Inter- and intra-rater reliability and accuracy of Sanders Skeletal Maturity Staging System when used by surgeons performing vertebral body tethering. Spine Deform. 2021.