Introduction. Skeletal maturity assessment in Idiopathic Scoliosis (IS) is used for the evaluation of
deformation progression risk, as well as selecting a method of treatment. The Sanders Maturity Scale (SMS)
is based on the ossification of phalanges, metacarpal bones and radius rated on AP radiograms of the left
Aim. This retrospective study aimed to compare SMS to other skeletal maturity assessment methods used
in daily practice.
Materials and methods. We included 39 female patients with IS (50 series of radiograms) with a mean age
of 13.4, ranging from 10.3 to 17.3. Each series of radiograms was evaluated by three observers with different
experience. Skeletal maturity was assessed using the Sanders Maturity Scale (SMS), Risser sign, Greulich
and Pyle (GP) atlas, as well as the closure of the triradiate cartilage.
Results. The majority of patients, 17 out of 50 (34 %) were classified as type 3 (adolescent rapid – early).
Intra-observer and inter-observer reliability for the SMS was very good (Krippendorff’s alpha >0.95).
The GP and Risser method showed good reliability, whereas the triradiate cartilage closure assessment
showed lower reliability. The Risser 0 grade corresponded with as many as four Sanders stages, 16 out of
20 (80 %) were rated Sanders 3. All radiograms with open triradiate cartilage (7/50, 14 %) were rated Sanders
2 or 3; they all received a Risser 0 grading.
Conclusions. The SMS proved to have a very good intra-observer and inter-observer reliability, it is easy to
be used by physicians and does not require an atlas. The SMS enhances the assessment of skeletal maturity
of IS patients by providing additional stages in the early phase of growth (Risser 0).
Wstęp. Ocena wieku kostnego pacjentów leczonych z powodu skoliozy idiopatycznej (SI) służy określeniu
ryzyka progresji deformacji oraz decyzji o wyborze sposobu leczenia. Metoda Sandersa opiera się na ocenie
kostnienia paliczków i kości promieniowej na radiogramach AP ręki lewej.
Cel. Celem pracy było porównanie metody Sandersa oraz innych stosowanych w codziennej praktyce
metod oceny wieku kostnego.
Materiał i metody. Do badania włączonych zostało 39 pacjentek (50 serii radiogramów) z rozpoznaniem SI,
w wieku 13,4 lat (od 10,3 do 17,3). Każda seria radiogramów została oceniona przez trzech obserwatorów
o różnym doświadczeniu. Dojrzałość kostna została oceniona przy użyciu skali Sandersa, testu Rissera,
atlasu Greulicha i Pyle (GP) oraz obecność chrząstki Y.
Wyniki. Najwięcej pacjentek, 17 z 50 (34%) zostało ocenionych jako stopień 3 w skali Sandersa (adolescent
rapid – early). Skala Sandersa cechowała się bardzo dobrą zgodnością wewnątrz oraz między obserwatorami
(Krippendroff’s alpha>0,95). Test Rissera i metoda GP cechowały się dobrą zgodnością, a ocena chrząstki Y
słabą. Pacjentkom ze stopniem Risser 0 odpowiadały aż 4 różne stopnie w skali Sandersa, 16 z 20 (80%)
pacjentek została oceniona jako Sanders 3. Pacjentki z otwartą chrząstką Y (7/50, 14 %) były oceniane jako
Sanders 2 i Sanders 3; wszystkie zostały ocenione jako Risser 0.
Wnioski. Metoda Sandersa cechuje się bardzo dobrą zgodnością i powtarzalnością, jest łatwa w stosowaniu
i nie wymaga używania atlasu. Początkowym etapom szybkiego wzrastania (Risser 0) odpowiadają
aż 4 stadia Sandersa, co zwiększa precyzję oceny wieku kostnego u pacjentek ze skoliozą idiopatyczną.
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 . 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 . 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 . 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.
The aim of the study was to compare the SMS to other, used in daily practice, skeletal maturity assessment methods.
Materials and methods
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).
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 . 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.
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).
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 . 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 . However, Swany et al. noticed the method might cause some difficulties delineating SMS stages 2 through 4 that are essential when assessing adolescent growth . These difficulties have not been depicted in our material.
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.
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