Skip to main content

Comparison of spheno-occipital synchondrosis maturation stages with three-dimensional assessment of mandibular growth

Abstract

Background

This study aimed to compare spheno-occipital synchondrosis (SOS) maturation stages with a three-dimensional assessment of mandibular growth.

Methods

This is a cross-sectional study of a retrospective type, in which cone-beam computed tomography (CBCT) images of 500 patients aged 6 to 25 years (226 males and 274 females) were analyzed. The SOS was evaluated using the four-stage scoring system; completely open, partially fused, semi-fused, or completely fused. The SOS scoring and three-dimensional cephalometric measurements were analyzed by Invivo 6.0.3 software. Descriptive and analytical statistics were performed, and a P-value < 0.05 was considered statistically significant.

Results

There was a statistically significant difference in mandibular measurements among SOS maturation stages in both sexes (P < 0.05). The skeletal growth increments of mandibular variables across the SOS stages had higher mean differences between SOS stages 2 and 3 than those between stages 1 and 2 and stages 3 and 4 in both sexes. The mandibular growth curves increased with chronological age (earlier in females) and SOS maturation stages (mostly in stages 1, 2, and 3 than stage 4).

Conclusions

The SOS maturation stages are valid and reliable mandibular skeletal indicators as evaluated with three-dimensional cephalometric mandibular measurements. The findings of growth increments and constructed growth curves of mandibular growth might be helpful in diagnosis and treatment planning.

Peer Review reports

Introduction

The spheno-occipital synchondrosis (SOS) is located in the midline between the sphenoid and occipital bones. It is considered the most important growth center in the cranial base because of its late ossification and contribution to post-natal cranial base growth [1, 2]. The cranial base is the template for facial development; therefore, it is directly related to the maxillary and mandibular growth and displacement. In individuals with craniofacial syndromes like Apert, Crouzon, Down, or Pfeiffer syndromes, the SOSs showed early ossification correlated with a shorter cranial base and midface hypoplasia [3, 4].

The evaluation of craniofacial skeletal growth has critical importance in orthodontic, dentofacial orthopedic, orthognathic diagnosis, treatment planning, and evaluation of treatment result's prognosis and stability [5, 6]. The main area of interest for the orthodontist is to know whether a patient has attained peak pubertal growth or passed that point. This, in turn, determines whether growth modification is still a viable treatment option [7, 8].

The most commonly used craniofacial skeletal maturation indicators were hand-wrist (HW) and cervical vertebrae maturation (CVM) methods. However, each method has its inherited limitations [9, 10]. The hand-wrist method requires expert knowledge and expenditure of time by the operator, the method's accuracy is not very high, and it exposes the patient to an unnecessary radiation dose [11]. The CVM method possesses poor reproducibility attributed to the level of training, clinician experience, and assessment methods [12,13,14]. Furthermore, the CVM method could not predict the amount of craniofacial growth in girls with Class II malocclusion [15, 16]. It is generally believed in the orthodontic community that there is still a need for a reliable skeletal maturity indicator that shows efficacy in detecting mandibular growth and should not depend on only one skeletal indicator for clinical decisions [17,18,19]. Based on recent high level evidence the CVMI and the HW radiograph still not guarantee to provide a reliable tool for skeletal age assessment and it was recommended that further studies are warranted to confirm these findings or to validate another more effective tool and it was also suggested to use a combination of maturation signs along with development stages of cervical vertebrae in order to determine skeletal maturation until a quantitative and valid method is presented [11, 20].

The CBCT images provide accurate three-dimensional anatomic details and facilitate visualization of small osseous structures and high-resolution images compared to conventional radiographs [21]. Recently, the SOS method has been considered a valid and reliable indicator of skeletal age compared with the CVM, HW methods, and chronological age [10, 22,23,24,25,26]. Jabour studied mandibular growth and the SOS fusion stages, but he used two-dimensional lateral cephalometric radiographs (LC) to measure the total mandibular length [22]. Up to date, the available literature neither compared the SOS maturation stages with the three-dimensional growth of the mandible nor included the reliability between them. Therefore, this study aimed to evaluate three-dimensional mandibular growth during SOS fusion stages in both sexes, assessing the reliability of the SOS method as a skeletal indicator of 3D mandibular growth, calculating mandibular growth potential (growth increments), and constructing a mandibular growth curve.

Materials and methods

Sample selection

This cross-sectional study of a retrospective type was approved by the Ethics Committee of the School of Stomatology at Lanzhou University in a group of the Chinese population (No: LZUKQ-2019-042). The sample size primarily depended on previous studies [27, 28], the G* power 3.0.10 software (ver. 3.1.9.7; Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany) was used to calculate the sample size based on the length of mandible (the primary outcome of this study). The a priori sample size estimation, performed at a 5% level of significance (α = 0.05), with a power of 99%, with mean vales of length of mandible were 96.27 ± 4.95 in SOS stage I and 101.57 ± 5.39 in SOS stage II, effect sizes (d = 1.02), and a two-sided test comparing two independent samples. The calculation revealed that a minimum of 37 subjects were necessary per SOS stage group (four group for each sex).

Data were randomly collected based on the pre-existing records between January 2016 and July 2021 according to a known patient age, sex, dental and medical history, and CBCT scan. The inclusion criteria were (1) age range from 6 to 25 years in which the upper and lower limits were determined following previous studies [29,30,31]; and (2) clear reporting of sex, dental and medical history. Exclusion criteria included (1) patients with reported cleft lip or cleft palate [32]; (2) craniofacial syndromes; (3) head trauma and/or deformity; (4) gross asymmetry; (5) previous orthodontic or orthopedic treatment, or (6) inadequate diagnostic quality radiographs. The huge amount of data in the institutional data-base were retrieved and analyzed for the preset selection criteria. Most of the retrieved CBCT were taken as per the institutional policy upon patients’ registration that comprehensive investigations to exclude and/or assess any pathology in the craniofacial region (delayed eruption teeth, root resorption, whole survey dentition, third molar extraction, bone anomaly, impacted teeth, TMJ, construction customized maxillary speed expansion (MSE), and diagnosis of nasal-complex problems) and clearly mentioned the benefits and possible risks of CBCT giving the condition that the patient has not been referred for CBCT in the last 6 months. The information of 572 subjects were collected, of which 72 were excluded, the remaining five hundred subjects, 274 females and 226 males were included in this study. Sample grouping was based on SOS scoring into four groups for each sex.

Informed consent was obtained from all subjects and their parents or legal guardians. Moreover, all methods were carried out in accordance with the principles of the declaration of Helsinki.

Three-dimensional imaging

CBCT acquisition

I-CAT Imaging System (Imaging Sciences International Inc. Hatfield, U.S.A.) was used to acquire CBCT images. Each patient had a scan utilizing a standard technique that comprised a standard head position, maximum intercuspation with the Frankfort horizontal plane parallel to the floor, and a crossing laser guide. Based on the imaging protocol, the patient was warned neither to swallow nor move throughout the scanning process[33]. The parameters of acquisition were16 × 13 cm field of view, 120 kV, 18.54 mAs, and 8.9 s exposure time. The selected slice thickness was 2 mm, and the voxel dimension was 0.3 mm[26].

SOS fusion staging

Digital Imaging and Communications in Medicine (DICOM) files of the CBCT images were obtained and then imported into Invivo 6.0.3 software (Anatomage, San Jose, CA, USA). The spheno-occipital synchondrosis four-stages system of Franklin and Flavell [29] (Table 1, Fig. 1) was followed. Lottering et al.[34] 6-stage SOS scoring system assumes the presence of fusion scar, which might persist for decades after fusion, has occurred [35]. Moreover, the four-stage scoring approach reduces assessment subjectivism, resulting in increased inter-observer agreement [29]. Moreover, it may be easier and needs less training by clinician and recommended by previous studies [24, 29, 30, 36, 37]. All 3D virtual models were oriented at a standardized position, then adjusted to the mid-sagittal plane (MSP) view (Fig. 2) [24, 29,30,31, 38, 39]. All CBCTs were assessed blindly with a coding system to mask the patient's demographic data and recorded in a separate data extraction sheet. Two well-trained observers, WA and RA independently scored the entire sample. Separated by a 1-month interval, both observers randomly selected 100 images and re-evaluated for intra-observer and inter-observer agreement of SOS staging. In the cases of disagreement, the axial view was used to assess the synchondrosis to reach a consensus as recommended by Okamoto et al.[40].

Table 1 Description of the fusion of the spheno-occipital synchondrosis scoring
Fig. 1
figure 1

Stages of SOS fusion in the mid-sagittal plane (3D multi-planar reconstruction)

Fig. 2
figure 2

Mid-sagittal CBCT evaluation of spheno-occipital synchondrosis with the head in the default orientation

Three-dimensional measurements

The 3D analysis involved the identification of anatomical landmarks (see Additional file 1: Table S1), reference planes (see Additional file 1: Table S2), and 3D linear and angular measurements presented in Table 2 and graphically presented in Fig. 3 [27, 41, 42].

Table 2 Definitions of the three-dimensional skeletal measurements of mandible
Fig. 3
figure 3

Three-dimensional cephalometric measurements of the mandible

With the nasion point centered as the origin of the 3D mold at the center of three planes X, Y, and Z (coronal, axial, sagittal), then was calculated by the 3D equation of distance formula to provide a more reliable and accurate measuring:

$$d = \sqrt {\left( {{\text{x1 }}{-}{\text{ x2}}} \right){2 } + { }\left( {{\text{y1 }}{-}{\text{ y2}}} \right){2 } + { }\left( {{\text{z1 }}{-}{\text{ z2}}} \right){2}}$$

where d is the distance (in millimeters) between two anatomic landmarks, and × 1, y1, and z1 and × 2, y2, and z2 are the coordinates of the two landmarks at the two ends of the linear measurement.

Intra- and inter-observer reliability of three-dimensional measurements was assessed by re-measuring 10% of the sample (50 CBCTs) by two observers (W.A and R.A) at one-month intervals.

Statistical analysis

IBM SPSS Statistics for Windows, Version 26.0 (Armonk, NY: IBM Corp.), was used. Intra- and inter-observer reliability analysis for the SOS scoring was calculated using Cohen's Kappa coefficient [26]. In contrast, the three-dimensional measurements' reliability was calculated by absolute and relative technical measurement errors (TEM and RTEM) and Interclass Correlation Coefficient (ICC) test. Descriptive statistics, including each variable's mean and standard deviation, were calculated and presented. Dahlberg's formula was also used to calculate the Standard Deviation of Measurement Error (SE) [43]. Quantitative data for the normal state was explored by the verification distribution of data. Depending on Shapiro–Wilk test and Kolmogorov–Smirnov test, all groups showed a normal distribution. The data were presented as mean and standard deviation (SD) for comparative analysis.

One-way ANOVA test was used to compare between the SOS maturation stages (four SOS groups per sex: independent variables) regarding the linear and angular measures of the mandible (dependent variables) for males and females separately. Two-way ANOVA was used to compare SOS’s four groups and sex (independent variables) regarding the linear and angular measures of the mandible (dependent variables). The problem of comparisons was treated by using Bonferroni correction, adjusting the P-value for multiple comparison tests, to avoid type I error.

The growth curves for mandibular parameters based on SOS maturation stages and chronological age were determined following a previous study [44]. R-statistical programing language was used for graphing and computing R2. P-value < 0.05 was considered statistically significant.

Results

CBCT scans of 500 patients aged 6 to 25 years; with a mean age of 13.89 ± 1.13 years were analyzed. It included 274 females and 226 males with mean ages of 13.68 ± 5.30 and 14.14 ± 4.99 years, respectively. The results of the intra- and inter-examiner reliability analysis for the SOS scoring were "almost perfect"; weighted Kappa agreement measures were more than 0.900 for each observer (see Additional file 1: Table S3). Three-dimensional mandibular cephalometric measurement's reliability was "excellent agreement"; R* values of TEM and RTEM were higher than 0.95% and ICC above 98% with P < 0.05 (see Additional file 1: Table S4).

The results showed that there were statistically significant differences in millimetric mandibular measurements (Co–Gn, Go–Me, Ag–Ag, Go–Go, Co–Co, Co–Go, Ag-R/FHP, and Ag-L/FHP), as well as the angular measurements (MP/FHP and Ag–Ag/FHP) for both sexes as presented in Table 3. The pair-wise comparison showed differences across different SOS stages. In contrast, the two-way ANOVA results showed no statistically significant difference in all used mandibular measurements according to sex and SOS stages interactions except for these parameters; Go–Go, Co–Co, Co–Go, Ag-R/FHP, and Ag-L/FHP.

Table 3 Descriptive statistics and the results of the One-way ANOVA test (for males and females separately) and two-way ANOVA test (for both sexes) between SOS fusion stages and 3D measurements of mandibular growth pattern

Regarding the skeletal growth increments (mean differences) of the mandible among the SOS stages (Table 4, Fig. 4); the results showed there were statistically significant mean differences between SOS stages 2 and 3 that were larger than those between stages 1 and 2 and stages 3 and 4 in males and females for mandibular measurements in millimetric (Co–Gn, Go–Me, Ag-R-Ag-L, Go–Go, Co–Co in males, Co–Go, Ag-R/FHP & Ag-L/FHP in males). However, mean differences between SOS stages 3 and 4 were larger than those between stages 1 and 2 and stages 2 and 3 (Co–Co, Ag-R/FHP & Ag-L/FHP in females).

Table 4 The growth increments of the mandible across the SOS maturation stages
Fig. 4
figure 4

The growth increments of the mandible across the SOS maturation stages

The mandibular growth curves according to SOS stages and chronological age for females and males with the effect size R2 and P < 0.05 are graphically presented in Fig. 5.

Fig. 5
figure 5

Female and male mandibular growth curves according to the SOS maturation (stages 1–4) and chronological age (6 through 25 years)

Discussion

The evaluation of skeletal maturation of craniofacial complex has critical importance in orthodontic, dentofacial orthopedic, orthognathic diagnosis, treatment, and prognosis. Recently, the SOS method has been considered as a reliable tool and correlated well with other established methods; Hand-wrist maturation and CVM index in assessment of skeletal age [10, 18, 22, 23, 25, 45,46,47,48,49]. However, through the literature, only two studies considered the SOS maturation stages and craniofacial morphology, but they neither compared the SOS maturation stages with the three-dimensional growth of the mandible nor included the reliability between them.[22, 27].

The superiority of SOS method may relate to the critical location of SOS in cranial base. In which its late ossification and contribution to post-natal cranial base growth play critical role in facial development[1, 2, 50,51,52]. Moreover, the CBCT have been used widely in dental field, so the SOS may be considered as suitable method as CBCT provides the benefits of low-cost, high-resolution, accurate three-dimensional imaging (3D) without the risk of increased radiation exposure to the patient, and easy visualization of superimposed bony structures[53]. On other hand, Hand -wrist method requires expert knowledge and expenditure of time by the operator, and their accuracy is not very high. It also had the drawback of unnecessary radiographic dose [11].

There were significant differences in the means of mandibular parameters among SOS stages for males and females as the following: the total mandibular length, body length, width (biantegonial, bigonial, and bicondylar), ramal height, mandibular height, anteroposteior inclination, and medio-lateral inclination. This might indicate that the SOS maturation stages have similar proportional growth increases with the significant mandibular parameters. So, this supports using the SOS stages as a valid method to assess mandibular growth. This finding is comparable with the standard gold method of validity of the CVM method for the assessment of facial growth [18, 48].

There was no significant difference in all used mandibular measurements according to sex and SOS stages interaction except for the bigonial width, bicondylar width, and mandibular height. This might indicate no sexual dimorphism in all analyzed mandibular cephalometric parameters according to SOS maturation stages except for the mentioned variables. There was no study that mentioned sexual dimorphism in mandibular parameters growth based on SOS maturation stages.

The calculated growth increments between SOS stage 2 and 3 were larger than those between stages 1 and 2 or stages 3 and 4 in males and females for total mandibular length, mandibular body length, mandibular width (biantegonial, bigonial, the male's bicondylar), ramal length, and the male's mandibular height. This might indicate that the mandibular growth peak is between stages 2 and 3. This is in agreement with Jabour [22], who found that the mandibular length growth peak occurred during the fusing stages (stages 2 and 3). Moreover, this finding is supported by the theory that spheno-occipital synchondrosis begins to fuse around puberty [24, 35]. However, mean differences between SOS stages 3 and 4 were larger than those between stages 1 and 2 and stages 2 and 3 for the female's mandibular height and the female's bicondylar width.

Sato et al. [44] constructed growth curves to predict the total mandibular length using the hand-wrist method. In this study, mandibular growth curves were constructed based on SOS maturation stages which were adjusted by incorporating the SOS maturation stages with smoothed fitted values of mandibular parameters considering the effect size (R2) on these parameters. This type of adjusting had not been mentioned in any previous studies [44, 54]. The aim behind this adjustment was to evaluate the effect of SOS maturation stages on the mandibular parameters directly; these curves showed that the following mandibular parameters (the total mandibular length, body length, width, ramal height, and mandibular height) increased with increasing of chronological age and it was earlier in females than males. The increase for these parameters with SOS was in stage 1, 2, and 3 (mostly accelerated in stages 2 and 3) then tended to be steadier in stage 4 for males and females in a similar pattern. These findings indicated that these mandibular parameters are more growing as the SOS is un-fused than in the fused stage (stage 4) for both sexes. This is similar to Jabour’s [22] finding of the mandibular length and SOS fusion stages. Moreover, it supported with idea of using the SOS fusion stages as a biological indicator for craniofacial and mandibular growth spurt prediction[24, 36].

A sexual dimorphism was found in this study as the fusion of SOS and growth of mandible were earlier in females than males. This sexual dimorphism is consistent with previous research, which reported that the SOS fuses earlier in females than males [24, 29, 30]. The effect size (R2) of SOS stages on mandibular parameters; the total mandibular length, body length, width (biantegonial, bigonial, and bicondylar), ramal height, and mandibular height were between 45 and 62% for females and between 50 and 62% for males. These percentages represent the variation of these mandibular parameters related to the SOS maturation stages. Previous studies reported that the R2 was high for biological data (used the CVM method), ranging from 30 to 67% [13, 55]. This may reflect the applicability of the present study growth curves as their effect sizes of SOS on mandibular parameters were mostly high.

Regarding ethical concerns that CBCT is taken in all cases, the policy of the institution that all patients upon registration should sign an informed consent which included their approval for referral to comprehensive investigations to exclude any pathology in the craniofacial region and clearly mentioned the benefits and possible risks of CBCT giving the condition that the patient has not been referred for CBCT in the last 6 months. In addition, the patients’ need any interventions either orthodontic or surgical; all CBCT images used as pre-treatment records are required for the planned treatment without the need for any other radiographic records. Moreover, this is a retrospective study, and the research team didn’t expose patients to extra radiation for the research purpose as all data were collected retrospectively and the study was also approved by the Ethics Committee of the School of Stomatology at Lanzhou University in a group of the Chinese population (No: LZUKQ-2019-042). Finally, retrieving this number of cases isn’t doubtful especially in large population community as Chinese population.

The clinical application of these findings suggests that if SOS is fusing, the individual would have the maximum amount of mandibular growth; in total mandibular length, mandibular body length, mandibular width, mandibular height, and mandibular ramal height. So, these findings may be useful in the three-dimensional growth prediction of the mandible during treatment planning for orthodontic, dentofacial orthopedic, or orthognathic surgery for both sexes.

Regarding the clinical implications and questionability of using the SOS fusion stages as a mandibular skeletal indicator; the study was designed to compare different categories of ages based on the expected mandibular growth changes during these different ages and because age is a weak determinant, a more standardized and well-established method was selected to answer this question (SOS) so that the clinician can decide whether to proceed with the growth modification mechanics. The use of SOS is considered as a reliable tool and correlated with other established methods; Hand-wrist maturation and CVM indices [10, 18, 22, 23, 25, 36, 45,46,47,48,49]. Finally, we didn’t absolutely judge the exact final mandibular size or the absolute residual growth which was difficult compared to the limited range of stages [22, 24, 36].

In this study, it is worthy to mention that regarding the new information added to the orthodontic literature, we gave a view about three-dimensional mandibular growth during SOS fusion stages in both sexes, assessing the reliability of the SOS method as a skeletal indicator of 3D mandibular growth, and 3D mandibular growth spurt based on SOS fusion stages, which aren’t available in the published in the literature. This may have important for the orthodontist in diagnosis or considered as a base for further research in the future.

The limitation of this study starts with its nature as a cross-sectional study; there is no doubt that the longitudinal studies of mandibular growth and development provide a more thorough understanding. However, the challenges of acquiring high sample numbers for a longitudinal study, the related increase in the number of radiographic exposures, and the ethical considerations are likely to rule out this approach and use the cross-sectional direction. So, the cross-sectional design was selected based on similar published study about maxillary and mandibular growth [28]. Also, this study might be considered as primary reporting in this field, and we hope there more detailed studies in future of a longitudinal design. Another limitation is that the ethnic group is limited to the Chinese population, making it less practical for other ethnicities. The sample had no skeletal classes or facial pattern specifications, which might affect the current findings. Detailed description of the SOS method can only be done with CBCT imaging, and it is not very obvious in plain x- ray.

Conclusions

The SOS maturation stages suggested to be a valid and reliable craniofacial skeletal indicator as evaluated and compared with three-dimensional cephalometric measurements of the mandibular in both sexes.

There was no sexual dimorphism regarding SOS maturation stages for total mandibular length and mandibular body width, while had sexual dimorphism for mandibular height, inter-gonial, and inter-condylar width.

The growth increments between SOS stages 2 and 3 were higher than those between stages 1 and 2 and staged 3 and 4 in most of the three-dimensional cephalometric dimensions of the mandible in both sexes.

The growth curves showed high active growth of the mandible as the SOS was still fusing (especially stages 2 and 3) than those of the fused (stage 4). Moreover, growth acceleration occurred earlier in females than males regarding chronological age but not for SOS maturation stages.

Availability of data and materials

All data and materials are available in the Orthodontics Department of stomatology school, Lanzhou University, China. Please get in touch with the corresponding author for any requests.

Abbreviations

SOS:

Spheno-occipital synchondrosis

DICOM:

Digital Imaging and Communications in Medicine

CBCT:

Cone beam computed tomography

CT:

Computed tomography

3D:

Three dimensional

ICC:

Intra-class correlation coefficient

References

  1. Ford EHR. Growth of the human cranial base. Am J Orthod. 1958;44(7):498–506.

    Article  Google Scholar 

  2. Afrand M, Oh H, Flores-Mir C, Lagravere-Vich MO: Growth changes in the anterior and middle cranial bases assessed with cone-beam computed tomography in adolescents. Am J Orthod Dentofacial Orthop 2017, 151(2):342–50.

  3. Goldstein JA, Paliga JT, Wink JD, Bartlett SP, Nah H-D, Taylor JA. Earlier evidence of spheno-occipital synchondrosis fusion correlates with severity of midface hypoplasia in patients with syndromic craniosynostosis. Plast Reconstr Surg. 2014;134(3):504–10.

    Article  Google Scholar 

  4. Adem C, Lafitte F, Jarquin S, Guillem P, Chiras J. The persistence of a spheno-occipital synchondrosis in an adult. J Radiol. 1999;80(8):863–5.

    Google Scholar 

  5. Lewis AB, Roche AF. Cranial base elongation in boys during pubescence. Angle Orthod. 1974;44(1):83–93.

    Google Scholar 

  6. Krieg WL. Early facial growth accelerations: a longitudinal study. Angle Orthod. 1987;57(1):50–62.

    Google Scholar 

  7. Faltin KJ, Faltin RM, Baccetti T, Franchi L, Ghiozzi B, McNamara JA Jr. Long-term effectiveness and treatment timing for Bionator therapy. Angle Orthod. 2003;73(3):221–30.

    Google Scholar 

  8. Baccetti T, Franchi L, Toth LR, McNamara JA. Treatment timing for Twin-block therapy. Am J Orthod Dentofac Orthop. 2000;118(2):159–70.

    Article  Google Scholar 

  9. Farman AG, Scarfe WC. The basics of maxillofacial cone beam computed tomography. Semin Orthod. 2009;15(1):2–13.

    Article  Google Scholar 

  10. Fernandez-Perez MJ, Alarcon JA, McNamara JA Jr, Velasco-Torres M, Benavides E, Galindo-Moreno P, Catena A. Spheno-occipital synchondrosis fusion correlates with cervical vertebrae maturation. PLoS ONE. 2016;11(8):e0161104.

    Article  Google Scholar 

  11. Ferrillo M, Curci C, Roccuzzo A, Migliario M, Invernizzi M, de Sire A. Reliability of cervical vertebral maturation compared to hand-wrist for skeletal maturation assessment in growing subjects: A systematic review. J Back Musculoskelet Rehabil. 2021;34(6):925–36.

    Article  Google Scholar 

  12. Gabriel DB, Southard KA, Qian F, Marshall SD, Franciscus RG, Southard TE. Cervical vertebrae maturation method: poor reproducibility. Am J Orthod Dentofacial Orthop. 2009;136(4):478 e471–477; discussion 478–480.

  13. Chen F, Terada K, Hanada K. A new method of predicting mandibular length increment on the basis of cervical vertebrae. Angle Orthod. 2004;74(5):630–4.

    Google Scholar 

  14. Nestman TS, Marshall SD, Qian F, Holton N, Franciscus RG, Southard TE. Cervical vertebrae maturation method morphologic criteria: poor reproducibility. Am J Orthod Dentofacial Orthop. 2011;140(2):182–8.

    Article  Google Scholar 

  15. Gray S, Bennani H, Kieser JA, Farella M. Morphometric analysis of cervical vertebrae in relation to mandibular growth. Am J Orthod Dentofacial Orthop. 2016;149(1):92–8.

    Article  Google Scholar 

  16. Engel TP, Renkema AM, Katsaros C, Pazera P, Pandis N, Fudalej PS. The cervical vertebrae maturation (CVM) method cannot predict craniofacial growth in girls with Class II malocclusion. Eur J Orthod. 2016;38(1):1–7.

    Article  Google Scholar 

  17. Grave KC, Brown T. Skeletal ossification and the adolescent growth spurt. Am J Orthod. 1976;69(6):611–9.

    Article  Google Scholar 

  18. Baccetti T, Franchi L, McNamara JA. The cervical vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11(3):119–29.

    Article  Google Scholar 

  19. Simpson SW, Kunos CA. A radiographic study of the development of the human mandibular dentition. J Hum Evol. 1998;35(4–5):479–505.

    Article  Google Scholar 

  20. Mahdian A, Kavousinejad S, Dashti M, Behnaz M. A systematic review of methods to determine skeletal maturation based on cervical vertebrae. J Regen Reconstruct Restor (Triple R), 3(1).

  21. Honda K, Bjørnland T. Image-guided puncture technique for the superior temporomandibular joint space: value of cone beam computed tomography (CBCT). Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;102(3):281–6.

    Article  Google Scholar 

  22. Jabour AS. Assessment of spheno-occipital synchondrosis fusion timing and an evaluation of its relationship with skeletal maturity, dental maturity and mandibular growth. Diss. US.: Case Western Reserve University; 2017.

  23. Dillon ME. Comparison of spheno-occipital synchondrosis closure, cervical vertebrae maturation and hand-wrist maturation as skeletal maturation indicators. M.S. Ann Arbor, US: University of Minnesota; 2018.

  24. Alhazmi A, Vargas E, Palomo JM, Hans M, Latimer B, Simpson S. Timing and rate of spheno-occipital synchondrosis closure and its relationship to puberty. PLoS ONE. 2017;12(8):e0183305.

    Article  Google Scholar 

  25. Demirturk Kocasarac H, Altan AB, Yerlikaya C, Sinanoglu A, Noujeim M. Correlation between spheno-occipital synchondrosis, dental age, chronological age and cervical vertebrae maturation in Turkish population: is there a link? Acta Odontol Scand. 2017;75(2):79–86.

    Article  Google Scholar 

  26. Al-Gumaei WS, Al-Attab R, Alhammadi MS, Al-Rokhami RK, Almashraqi AA, Zhenlin G, Abdulghani EA, Zheng Y. Evaluation of spheno-occipital synchondrosis fusion in Chinese population using CBCT: a cross-sectional study. JCDP. 2022;23(1):8–13.

    Article  Google Scholar 

  27. Fortanely BE. The influence of the spheno occipital synchondrosis fusion on craniofacial form. UK: University of British Columbia; 2020.

    Google Scholar 

  28. Manabe A, Ishida T, Kanda E, Ono T. Evaluation of maxillary and mandibular growth patterns with cephalometric analysis based on cervical vertebral maturation: a Japanese cross-sectional study. PLoS ONE. 2022;17(4):e0265272.

    Article  Google Scholar 

  29. Franklin D, Flavel A. Brief communication: timing of spheno-occipital closure in modern Western Australians. Am J Phys Anthropol. 2014;153(1):132–8.

    Article  Google Scholar 

  30. Hisham S, Flavel A, Abdullah N, Noor MHM, Franklin D. Quantification of spheno-occipital synchondrosis fusion in a contemporary Malaysian population. Forensic Sci Int. 2018;284:78–84.

    Article  Google Scholar 

  31. Sinanoglu A, Kocasarac HD, Noujeim M. Age estimation by an analysis of spheno-occipital synchondrosis using cone-beam computed tomography. Leg Med. 2016;18:13–9.

    Article  Google Scholar 

  32. Vale F, Francisco I, Lucas A, Roseiro A, Caramelo F, Sobral A. Timing of spheno-occipital synchondrosis ossification in children and adolescents with cleft lip and palate: a retrospective case-control study. Int J Environ Res Public Health. 2020;17(23).

  33. Alhammadi MS, Al-mashraqi AA, Alnami RH, Ashqar NM, Alamir OH, Halboub E, Reda R, Testarelli L, Patil S. Accuracy and reproducibility of facial measurements of digital photographs and wrapped cone beam computed tomography (CBCT) photographs. Diagnostics. 2021;11(5):757.

    Article  Google Scholar 

  34. Lottering N, MacGregor DM, Alston CL, Gregory LS. Ontogeny of the spheno-occipital synchondrosis in a modern Queensland, Australian population using computed tomography. Am J Phys Anthropol. 2015;157(1):42–57.

    Article  Google Scholar 

  35. Shirley NR, Jantz RL. Spheno-occipital synchondrosis fusion in modern Americans. J Forensic Sci. 2011;56(3):580–5.

    Article  Google Scholar 

  36. Alhazmi A, Aldossary M, Palomo JM, Hans M, Latimer B, Simpson S. Correlation of spheno-occipital synchondrosis fusion stages with a hand-wrist skeletal maturity index: a cone beam computed tomography study. Angle Orthod. 2021;91(4):538–43.

    Article  Google Scholar 

  37. Bassed RB, Briggs C, Drummer OH. Analysis of time of closure of the spheno-occipital synchondrosis using computed tomography. Forensic Sci Int. 2010;200(1–3):161–4.

    Article  Google Scholar 

  38. Baker MJ. Analysis of spheno-occipital synchondrosis (SOS) fusion in a contemporary southern Nevada subadult Hispanic population using archival cone-beam computerized tomography (CBCT) images. US: University of Nevada; 2019.

    Google Scholar 

  39. Ok G, Sen Yilmaz B, Aksoy DO, Kucukkeles N. Maturity evaluation of orthodontically important anatomic structures with computed tomography. Eur J Orthod. 2021;43(1):8–14.

    Article  Google Scholar 

  40. Okamoto K, Ito J, Tokiguchi S, Furusawa T. High-resolution CT findings in the development of the sphenooccipital synchondrosis. AJNR Am J Neuroradio. 1996;17(1):117–20.

    Google Scholar 

  41. Golchini E, Rasoolijazi H, Momeni F, Shafaat P, Ahadi R, Jafarabadi MA, Rahimian S. Investigation of the relationship between mandibular morphology and upper airway dimensions. J Craniofac Surg. 2020;31(5):1353–61.

    Google Scholar 

  42. Wang RH, Ho C-T, Lin H-H, Lo L-J. Three-dimensional cephalometry for orthognathic planning: Normative data and analyses. J Formos Med Assoc. 2020;119(1, Part 2):191–203.

  43. Park J, Baumrind S, Curry S, Carlson SK, Boyd RL, Oh H. Reliability of 3D dental and skeletal landmarks on CBCT images. Angle Orthod. 2019;89(5):758–67.

    Article  Google Scholar 

  44. Sato K, Mito T, Mitani H. An accurate method of predicting mandibular growth potential based on bone maturity. Am J Orthod Dentofacial Orthop. 2001;120(3):286–93.

    Article  Google Scholar 

  45. Uysal T, Ramoglu SI, Basciftci FA, Sari Z. Chronologic age and skeletal maturation of the cervical vertebrae and hand-wrist: is there a relationship? Am J Orthod Dentofacial Orthop. 2006;130(5):622–8.

    Article  Google Scholar 

  46. Lai EH, Liu JP, Chang JZ, Tsai SJ, Yao CC, Chen MH, Chen YJ, Lin CP. Radiographic assessment of skeletal maturation stages for orthodontic patients: hand-wrist bones or cervical vertebrae? J Formos Med Assoc. 2008;107(4):316–25.

    Article  Google Scholar 

  47. Hassel B, Farman AG. Skeletal maturation evaluation using cervical vertebrae. Am J Orthod Dentofacial Orthop. 1995;107(1):58–66.

    Article  Google Scholar 

  48. O’Reilly MT, Yanniello GJ. Mandibular growth changes and maturation of cervical vertebrae: a longitudinal cephalometric study. Angle Orthod. 1988;58(2):179–84.

    Google Scholar 

  49. Alhazmi A, Aldossary M, Palomo JM, Hans M, Latimer B, Simpson S. Correlation of spheno-occipital synchondrosis fusion stages with a hand-wrist skeletal maturity index: a cone beam computed tomography study. Angle Orthod. 2021;4:538–43.

    Article  Google Scholar 

  50. Powell TV, Brodie AG. Closure of the spheno-occipital synchondrosis. Anat Rec. 1963;147(1):15–23.

    Article  Google Scholar 

  51. Singh GD, McNamara JA Jr, Lozanoff S. Morphometry of the cranial base in subjects with Class III malocclusion. J Dent Res. 1997;76(2):694–703.

    Article  Google Scholar 

  52. Enlow D. Facial growth and development in the rhesus monkey. In: Handbook of Facial Gowth. 3rd edn. Philadelphia: WB Saunders Company; 1990: 444–54.

  53. Graf CC, Dritsas K, Ghamri M, Gkantidis N. Reliability of cephalometric superimposition for the assessment of craniofacial changes: a systematic review. Eur J Orthod 2022:cjab082.

  54. Law CJ, Baliga VB, Tinker MT, Mehta RS. Asynchrony in craniomandibular development and growth in Enhydra lutris nereis (Carnivora: Mustelidae): are southern sea otters born to bite? Biol J Linn Soc. 2017;121(2):420–38.

    Article  Google Scholar 

  55. Dibbets JM, Trotman CA, McNamara JA, van der Weele LT, Janosky JE. Multiple linear regression as an analytical tool in cephalometric studies. Br J Orthod. 1997;24(1):61–6.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Abdullah Albukhaiti and Dr. Esam Hulbob for their support during statistical analysis.

Funding

This project was supported by the Open Subject Foundation of Key Laboratory of Dental Maxillofacial Reconstruction and Biological Intelligence Manufacturing (20JR10RA653-ZDKF20210101), School of Stomatology, Lanzhou University, Gansu Province, Lanzhou 730000, PR China.

Author information

Authors and Affiliations

Authors

Contributions

W.S.A., R.A., and B.A.; a collection of the data. W.S.A. and R.A. analysis of the data and writing the original draft. M.S.A. and A.A.A.; Conceptualization and methodology. W.S.A., E.S.A., and S.A.A.; statistical analysis. W.S.A., M.S.A., N.A. and R.A.; review and editing. Y.Z.; supervision. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yan Zheng.

Ethics declarations

Ethics approval and consent to participate

This retrospective clinical study was approved by the ethical committee of clinical scientific research of the school of stomatology of Lanzhou University, China (No: LZUKQ-2019-042). The Informed consent was obtained from all subjects and their parents or legal guardians. Moreover, all methods were carried out in accordance with the principles of the declaration of Helsinki.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

Definitions of the three-dimensional skeletal landmarks of the mandible; Table S2. Definitions of the three-dimensional craniofacial reference planes; Table S3. Inter and intra-observer SOS staging reliability; and Table S4. Reliability analysis of three-dimensional mandibular measurements.

Additional file 2

: The raw data of 3D mandibular measurements across SOS fusion stages.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Gumaei, W.S., Al-Attab, R., Al-Tayar, B. et al. Comparison of spheno-occipital synchondrosis maturation stages with three-dimensional assessment of mandibular growth. BMC Oral Health 22, 654 (2022). https://doi.org/10.1186/s12903-022-02692-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12903-022-02692-3

Keywords