Age-Dependent Three-Dimensional Evaluation of the Spheno-Occipital Synchondrosis Using Computed Tomography

AUTHORS

Arezoo Jahanbin 1 , Shirin Dokht Shirazi 2 , Elaheh Kamyabnezhad 1 , * , Neda Eslami 1 , Seyed Hosein Hoseini Zarch 3

1 Department of Orthodontics, School of Dentistry, Mashhad University of Medical Sciences, Mashhad, Iran

2 School of Dentistry, Mashhad University of Medical Sciences, Mashhad, Iran

3 Department of Radiology, School of Dentistry, Mashhad University of Medical Sciences, Mashhad, Iran

How to Cite: Jahanbin A, Shirazi S D, Kamyabnezhad E, Eslami N, Hoseini Zarch S H. Age-Dependent Three-Dimensional Evaluation of the Spheno-Occipital Synchondrosis Using Computed Tomography, Iran J Ortho. 2020 15(1): e115608. doi: 10.5812/ijo.115608.

ARTICLE INFORMATION

Iranian Journal of Orthodontics: 15 (1); e115608
Published Online: May 24, 2021
Article Type: Research Article
Received: April 23, 2021
Revised: May 18, 2021
Accepted: May 18, 2021
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Abstract

Background: The spheno‐occipital synchondrosis (SOS) is an important growth center which plays an important role in cranial base development and can define the final relation of SOS with the upper and lower jaws. The morphology and fusion degree of SOS varies in different ages among different populations.

Objectives: Thus, the aim of this study was to evaluate the age and sex dependence of ossification of the spheno-occipital synchondrosis in the Iranian population using CBCT.

Methods: This cross-sectional retrospective study was performed on 517 CBCT images of 6- to 18-year-old patients in Mashhad, Iran. Patients with obvious pathology or fractures were excluded from the study. The SOS ossification was classified into four stages from 0 to 3. Two independent observers scored the images. The ossification stage of the SOS was classified according to the age and sex of the patients. Kruskal-Wallis and Kendall’s tau-b used for statistical analysis.

Results: In this study, 517 samples of 260 females (50.3%) and 257 males (49.7%) with a mean age of 12.03 ± 3.74 years were examined. A significant difference did not exist between males and females regarding their stage of SOS ossification, although males were younger at the SOS transitional stages of 0 to 1, and 1 to 2 compared to females. Also, the SOS starts the ossification process at the age of 11 in females and 10.8 in males.

Conclusions: The present study showed in the mean age of 16.81 ± 1.12 years, most subjects were in developmental stage 3. Due to the fact that in developmental stage 3 SOS closes, there were no passive maxillary growth after this time. In none of the SOS stages, females and males differed significantly in mean age (P > 0.05). The age of the onset of SOS closure in females was 11 years and in males it was about 10.8 years.

1. Background

Spheno-occipital synchondrosis (SOS) is a cartilage growth center between the occipital bone and the sphenoid. This important growth center is comprised of hyaline cartilage, which will be ossified during puberty, and is abundantly found at the base of the skull during growth. Knowing the chronological age of SOS ossification might result in various decisions in forensic, anthropological and medical practices (1-12).

Craniofacial growth studies show that SOS plays an important role in cranial base development, which defines the final relation of it with the upper and lower jaws (13, 14). Tahiri et al proved a significant correlation between premature closure of the SOS and hypoplasia of the mid-face (15). The study of SOS growth and development and its role in craniofacial growth is an interesting area of research in this field. Moreover, studies have focused on using the spheno-occipital synchondrosis development for age estimation (1).

Regarding sex-dependent differences in human development, like other growth markers, it is thought that cranial base sutures close earlier in females than in males. Hence, the closing time of the SOS is considered as a reliable indicator for estimating biological age (1, 10-12). The spheno-occipital synchondrosis ossifies the latest in comparison with other cranial base synchondroses, which makes it a point of interest for growth investigations (1, 2, 8, 9).

2. Objectives

The aim of this study was to evaluate the ossification stages of the spheno-occipital synchondrosis using computed tomography in both sexes in order to use in age estimation in addition to evaluate the maxillary growth.

3. Methods

This retrospective cross-sectional study was performed from October 2019 to October 2020 in the orthodontic department of Mashhad Dental School. The code of ethics was IR.MUMS.DENTISTRY.REC.1398.047., the data were collected from the radiology center archives via non-random sampling. At first, the CBCTs were collected from 517 patients (260 females, 257 males) aged 6 to 18 years (mean age = 12.03 ± 3.74), who were referred for different reasons such as sinusitis or head and face trauma, and who had visible SOS. Patients with pathological problems or obvious fractures were excluded from the study. Plancema Romexis Viewer software (version 5.2.0, Finland, Helsinki) was used to examine the CBCT images. In this software, sex, age, and the developmental stage of SOS had been recorded.

According to Franklin et al study (11) in which sagittal cross-section used for SOS examination in the CBCT images, the SOS was standardized in the axial and coronal sections with Planmeca software so that it was well displayed in the mid-sagittal image of the SOS. To reduce errors in determining the developmental stage, if there was a doubt between two developmental stages, the lower developmental stage was recorded for the patient (Figure 1)(16).

Figure 1. The mid-sagittal cross section of CBCT and SOS different ossification stages.

Since in this study two evaluators scored the variables, it was necessary to examine the internal and external agreements (inter and intra examiner reliability) of the evaluators. For evaluating internal and external agreements, the evaluators re-scored 40 radiographic images one week later and then the scores of the two evaluators were compared. Cohen's kappa coefficient was used to evaluate the degree of internal and external agreements. It was revealed that for intra examiner reliability, the value of agreement was kappa = 0.833 and for the inter examiner reliability, the value of agreement was kappa = 0.777.

According to a study by Franklin et al. (11), the following four steps were defined for spheno-occipital sutures: (0) They are completely open and there is no sign of a connection between the occipital and sphenoid bones and no bone between them exists. (1) Less than half of the seam length is connected and the process of converting endocranial to ectocranial is in progress. (2) More than half the length of the seam is connected and most of the bottom board is not connected. (3) They are perfectly connected and a normal view of the bone is visible. There is a possibility of scarring from the joint.

3.1. Bayesian Transition Analysis

The Bayesian transition analysis is a suitable method for modeling a sequential variable in which the order of the steps is determined by a skeletal trait and its morphological changes are constantly changing (17). This analysis is based on a cumulative probability model in which age can be considered as an independent variable and estimated for a person transitioning from one age to another (18-21). By estimating the regression slope for age and tracking each transition of the regression model, a cumulative probability was obtained for each subgroup. The mean and standard deviation were then calculated by adjusting the previous uniformity, which assigns the same probability to each age group and combines this information with parameter estimation. The calculated parameters are the mean and standard deviation of the lognormal distributions for each transition path (22). Standard error of means (SEM) was determined considering 1000 longitudinal samples n (n = number of observations in each group) and by replacing the male and female groups separately and using the bootstrap sampling method, the non-parametric vector of Monte Carlo was calculated. The Bayesian transfer model was implemented for each female and male subgroup and the parameters as well as the SEM of each group and the transfer were calculated. Subsequently, for each transfer, two independent t-tests were performed to evaluate the statistical difference using the estimated mean and SEM.

Kendall's tau-b was used to evaluate the degree of correlation between sex and the variables of this study. The Kruskal-Wallis test was used to examine the correlation of age in different stages of SOS. Bayesian cumulative application model was applied using the Arm package, which was implemented in the software R 3.6.3. The significance level was considered 5% in all statistical tests.

4. Results

The current study was performed on 517 subjects that consisted of 260 females (50.3%) and 257 males (49.7%) with the mean age of 12.03 ± 3.74 years and age range of 6 to 18 years. The subjects were evaluated in terms of SOS developmental stage and its relationship with age and sex. The results are as follows:

Table 1 shows the number and percentage of each SOS stage separately for females and males. As it appears, when comparing females and males, the highest percentage was related to the zero developmental stage with 43.8% for females (114 females) and 40.1% for males (103 males). Amongst females, the lowest percentage was related to developmental stages 1 and 2 with 18.1% (n = 47) and in males, it was related to developmental stage of 1 with 18.3% (n = 47). In general, there was no statistically significant difference between females and males in terms of different developmental stages of SOS (P = 0.325).

Table 1. Frequency Distribution of SOS Developmental Stages in Male and Female a
SOS Developmental StageTotal
0123
Sex
Female114 (43.8)47 (18.1)47 (18.1)52 (20.0)260 (100)
Male103 (40.1)47 (18.2)48 (18.7)59 (23.0)257 (100)
Total217 (42.0)94 (18.2)95 (18.3)111 (21.5)517 (100)
Kendall’s tau-b test resultΤk = 0.040, P = 0.325

aValues are expressed as No. (%).

Table 2 shows the mean, standard deviation, minimum, maximum, median, and mid-quarters of the age variable for each of the different stages of SOS. The different stages of SOS were significantly different in terms of mean age (P < 0.001). Comparing the SOS stages with each other, all stages had significantly statistical differences.

Table 2. Age Comparison in Different Developmental Stages of SOS
SOS StageNumberMean ± SD (y)Median ± Mid-quarter Amplitude (y)Min-Max (y)Kruskal-Wallis Test Result
02178.64 ± 2.018.0 ± 3.06 – 13X2 = 414.4, P < 0.001
19411.44 ± 1.7012.0 ± 3.07 – 14
29514.77 ± 1.2515.0 ± 1.012 – 18
311116.81 ± 1.1217.0 ± 2.014 – 18

According to Table 3 by age increasing, SOS ossification also moved to higher stages. According to Kendall’s tau-b test result the distribution of SOS stages was not significantly different between girls and boys at any age.

Table 3. Comparison of SOS Stages Between Girls and Boys Separately by Each Year
Age (y)/ Gender0123TotalP-Value
6.0-
Female22 (100)0 (0)0 (0)0 (0)22 (100)
Male18 (100)0 (0)0 (0)0 (0)18 (100)
7.00.432
Female21 (100)0 (0)0 (0)0 (0)21 (100)
Male15 (93.8)1 (6.3)0 (0)0 (0)16 (100)
8.01.00
Female18 (90)2 (10)0 (0)0 (0)20 (100)
Male18 (90)2 (10)0 (0)0 (0)20 (100)
9.00.721
Female15 (78.9)4 (21.1)0 (0)0 (0)19 (100)
Male15 (71.4)6 (28.6)0 (0)0 (0)21 (100)
10.00.738
Female15 (71.4)6 (28.6)0 (0)0 (0)21 (100)
Male12 (63.2)7 (36.8)0 (0)0 (0)19 (100)
11.00.744
Female11 (61.1)7 (38.9)0 (0)0 (0)18 (100)
Male15 (68.2)7 (31.8)0 (0)0 (0)22 (100)
12.00.442
Female10 (47.6)11 (52.4)0 (0)0 (0)21 (100)
Male7 (36.8)11 (57.9)1 (5.3)0 (0)19 (100)
13.00.568
Female2 (10)13 (65)5 (25)0 (0)20 (100)
Male3 (15)9 (45)8 (40)0 (0)20 (100)
14.00.588
Female0 (0)4 (21.1)14 (73.7)1 (5.3)19 (100)
Male0 (0)4 (19)14 (66.7)3 (14.3)21 (100)
15.01.00
Female0 (0)0 (0)15 (75)5 (25)20 (100)
Male0 (0)0 (0)15 (75)5 (25)20 (100)
16.01.00
Female0 (0)0 (0)6 (30)14 (70)20 (100)
Male0 (0)0 (0)7 (35)13 (65)20 (100)
17.00.698
Female0 (0)0 (0)5 (23.8)16 (76.2)21 (100)
Male0 (0)0 (0)3 (15.8)16 (84.2)19 (100)
18.00.196
Female0 (0)0 (0)2 (11.1)16 (88.9)18 (100)
Male0 (0)0 (0)0 (0)22 (100)22 (100)

4.1. Bayesian Transition Analysis

The most probable age at which SOS transmission and maturation occurs was estimated as the age for transition from one developmental stage to another. Standard deviation was also considered as the scattering parameter for each transfer.

According to Table 4 and Figure 2, the mean age SOS transmission from 0 to 1 and from 1 to 2 was higher in females than males, but the differences were not statistically significant (P > 0.05).

Table 4. Bayesian Estimation of Transition Age and Transition Analysis for SOS Stages
Transition StageMale, n = 257Female, n = 260TP-Value
Estimate ± SEMSDEstimate ± SEMSD
SOS0.850.80
0 - 110.80 ± 0.2511.02 ± 0.24-0.630.525
1 - 213.14 ± 0.1613.41 ± 0.15-1.320.218
2 - 315.68 ± 0.1915.92 ± 0.19-0.890.371

Abbreviation: SEM, Standard Error Mean.

Figure 2. Density Chart of the Probability of Age in Females and Males for SOS

5. Discussion

In this cross-sectional study, 517 subjects consisting of 260 females (50.3%) and 257 males (49.7%) with a mean age of 12.3 ± 3.74 years were examined for SOS developmental stages.

The highest frequency was related to the zero developmental stage with 217 subjects (42%). According to statistical tests, there was no significant difference in terms of different developmental stages of SOS between females and males (P = 0.325).

Comparison of age between females and males by different stages of SOS indicated that females and males did not differ significantly in mean age (P > 0.05).

The mean age of females in SOS transmission in all stages of 0 to 1 and 1 to 2 was higher than males, but the differences were not statistically significant (P > 0.05). The age of onset of SOS closure was estimated at 11 years in females and 10.5 years in males.

In the present study, a 4-point system (from 0 to 3) was used to evaluate SOS, similar to the studies of Sinanoglu et al., Franklin et al., and Alhazmi et al. (1, 11, 23). The highest frequency was related to developmental stage zero with 217 subjects (42%) and the lowest frequency was related to developmental stage one with 94 subjects (18.2%). In the studies of Sinanoglu et al., Franklin et al. and Alhazmi et al., the highest frequency was related to developmental stage 3, in which the mean age and age range of participants were higher than the present study (1, 11, 23).

Analysis of the results of our study showed that the age of individuals in all stages of SOS were significantly different from each other, so that with the increasing degree of development, the age of participants increased significantly. This result is consistent with Sinanoglu et al., Franklin et al., and Alhazmi et al (1, 11, 23).

Some researchers examined the age of SOS maturation by sex in different populations (1, 11, 18), and hence the different results may be due to racial differences. Moreover, skeletal maturity is likely to be affected by socioeconomic conditions because these factors affect development, and thus population selection from an area with similar socioeconomic status should be suggested (1, 12, 18, 24). Due to the retrospective nature of our study, it was not possible to classify subjects according to their socioeconomic status. Nevertheless, most subjects were selected from one city.

Akhlagi et al., examined female corpses in forensics and using a triple classification system for SOS, stated that female corpses, which were thought to be between 8 and 26 years old, would be an average age of 8.10 if the spheno-occipital suture was open and the corpses of women with a matured suture would be an average age of 19.6 years (25).

This result is in accordance with the studies of Sinanoglu et al., Franklin et al., nd Alhazmi et al; although, in the mentioned studies, different investigative analyses were used and different numbers were reported (1, 11, 23).

A study found that younger children with early fusion of the SOS may show a skeletal Class III morphology. In addition, they showed that SOS stage is more closely correlated to increased mandibular length and transverse facial width (26). Another study demonstrated that developmental stage of spheno-occipital synchondrosis which determined by CBCT, is a good indicator of growth maturation (27).

5.1. Conclusions

Based on the results of this study, it can be concluded that: (1) The present study showed that in the mean age of 16.81 ± 1.12 years, most subjects were in developmental stage 3. Due to the fact that in developmental stage 3 SOS closes, there was no passive maxillary growth after this time. (2) In none of the SOS stages, females and males differed significantly in the mean age (P > 0.05). (3) The mean age of females in SOS transmission in stages of 0 to 1 and 1 to 2 was higher than males, but the differences were not statistically significant (P > 0.05). The age of onset of the SOS closure in females was 11 years and in males it was about 10.8 years.

Footnotes

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