Comparison_of_three-dimensional_maxillary_growth_a
Comparison_of_three-dimensional_maxillary_growth_a
Comparison_of_three-dimensional_maxillary_growth_a
Abstract
Background This study aimed to three-dimensionally compare the maxillary growth among the spheno-occipital
synchondrosis (SOS) maturation stages in both genders.
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 maxillary measurements among SOS maturation stages in
both genders (P < 0.05). The mean differences in the maxillary growth among the SOS maturation stages between
SOS stages 2 and 3 were higher than those between stages 1and 2 and stages 3 and 4 for maxillary length and height
in both genders. However, the mean difference in the maxillary width was higher between SOS stages 1 and 2 than
those stages 2 and 3 and stages 3 and 4. On other hand, there may be lesser maxillary growth between SOS stages 3
and 4 for maxillary width, length (in males), and height. The growth curves showed high active growth of the maxilla
as the SOS was still fusing (especially stage 2 and 3) than those of the fused (stage 4). Moreover, the acceleration of
growth occurred earlier in females than males regarding chronological age but not for SOS maturation stages.
Conclusions The SOS maturation stages are valid and reliable maxillary skeletal maturation indicators for three-
dimensional maxillary growth in both genders.
Keywords Maxillary growth, Spheno-occipital synchondrosis, Stages of fusion, CBCT, Three-dimensional
† 3
Waseem S. Al-Gumaei and Hu Long co-first authors equally contributed to Department of Dental Implant, School of Stomatology, Lanzhou
this work. University, Lanzhou, China
4
State Key Laboratory of Oral Diseases and National Clinical Research
*Correspondence: Center for Oral Diseases and Department of Oral and Maxillofacial
Wenli Lai Surgery, West China Hospital of Stomatology, Sichuan University,
[email protected] Chengdu, China
Yan Zheng 5
Orthodontics and Dentofacial Orthopedics, Department of Preventive
[email protected]
1 Dental Sciences, College of Dentistry, Jazan University, Jazan, Saudi Arabia
Department of Orthodontics and Dentofacial Orthopedics, School 6
Department of Orthodontics, Faculty of Dentistry, First Affiliated
of Stomatology, Lanzhou University, Lanzhou, China
2 Hospital of Zhengzhou University, Henan, China
State Key Laboratory of Oral Diseases and National Clinical Research 7
Department of Orthodontics, School of Stomatology, China Medical
Center for Oral Diseases and Department of Orthodontics, West China University, Shenyang, Liaoning, China
Hospital of Stomatology, Sichuan University, Chengdu, China
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The CBCTs were taken for evaluation of delayed erup- SOS fusion staging
tion teeth, root resorption, survey whole dentition, third Digital Imaging and Communications in Medicine
molar extraction, and diagnosis of nasomaxillary com- (DICOM) files of the CBCT images were obtained and
plex problem. then imported into Invivo 6.0.3 software (Anatomage,
Informed consents were obtained from all subjects and San Jose, CA, USA). The spheno-occipital synchondro-
their parents or legal guardians. Moreover, all methods sis four-stage system of Franklin and Flavell [31] (Table 1
were carried out in accordance with the principles of the & Fig. 1) was followed. Lottering et al. [34] 6-stage
declaration of Helsinki. SOS scoring system assumes the presence of fusion
scar, which might persist for decades after fusion, has
Three‑dimensional imaging occurred [35]. Moreover, the four-stage scoring approach
CBCT acquisition reduces assessment subjectivism, resulting in increased
CBCT images were acquired using I-CAT Imaging Sys- inter-observer agreement [31]. Moreover, it may be easier
tem (Imaging Sciences International Inc. Hatfield, USA). and needs less training by clinician and recommended by
Each patient was scanned using a standard protocol that previous studies [24, 31, 32, 36, 37]. All 3D virtual models
included a standardized head position, maximal intercus- were oriented at a standardized position, then adjusted to
pation with the Frankfort horizontal plane parallel to the the mid-sagittal plane (MSP) view (Fig. 2) [24, 31–33, 38,
floor with a crossing laser guide. According to the imag- 39]. All CBCTs were assessed blindly with a coding sys-
ing protocol, the patient was instructed not to swallow tem to mask the patient’s demographic data and recorded
or move during the scanning process. The acquisition in a separate data extraction sheet. Two well-trained
parameters used were: 16 × 13 cm field of view, 120 kV, observers, W.A. and R.A. independently scored the entire
18.54 mAs, and 8.9 s exposure time. The selected voxel sample. Separated by a 1-month interval, both observ-
dimension was 0.3 mm, and the slice thickness was 2 mm. ers randomly selected 100 images and re-evaluated for
1 Un-fused Opened entirely with no sign of closure or presence of bone in the gap between the endocranial and ectocranial borders
2 Partial-fused Fused endocranially but not more than half the length of the synchondrosis (Fusing endocranially, ≤ 50%)
3 Semi-fused Fusing ectocranially with more than half the length of the synchondrosis but without fusing of the inferior (ectocranial)
border. (Fusing ectocranially, > 50% and less than 100% fusion)
4 Complete fusion Fused entirely with normal bone appearance throughout the synchondrosis, but a fusion scar may be existing
Fig. 1 Stages of SOS fusion in the mid-sagittal plane (3D multi-planar reconstruction)
Fig. 2 Mid-sagittal CBCT evaluation of spheno-occipital synchondrosis with the head in the proper orientation
intra-observer and inter-observer agreement of SOS equation of distance formula to provide a more reliable
staging. In the cases of disagreement, the axial view was and accurate measuring:
used to assess the synchondrosis to reach a consensus as
recommended by Okamoto et al. [40]. d= (x1 − x2)2 + y1 − y2 2 + (z1 − z2)2
Three‑dimensional measurements where d is the distance (in millimeters) between two ana-
The 3D analysis involved identification of anatomical tomic landmarks, and × 1, y1, and z1 and × 2, y2, and z2
landmarks (Additional file 1: Table S1), reference planes are the coordinates of the two landmarks at the two ends
(Additional file 1: Table S2), and 3D linear and angular of the linear measurement.
measurements presented in Table 2 and graphically pre- Intra- and inter-observer reliability of three-dimen-
sented in Fig. 3 [27, 41, 42]. sional measurements was assessed by re-measuring 10%
With the nasion point centered as the origin of the of the sample (50 CBCTs) by two observers (W.A. and
3D mold at the center of the three planes X, Y, and Z R.A.) at one-month intervals.
(coronal, axial, sagittal), then was calculated by the 3D
Maxillary length ANS-PNS (mm) Distance between the projection of PNS and ANS points onto the sagittal plane
Maxillary width J-J (mm) Distance between the right and the left Jugale points (J) along the transverse axis
Maxillary height J-FHP (mm) The perpendicular distance from Jugale points (J) to the FH plane
Maxillary antero-posterior inclination (PP/FHP) ° The angle between of palatal plane (PP) and Frankfort plane (FHP) antero-posteriorly
onto the sagittal plane
Maxillary medio-lateral inclination (J-J /FHP) ° The angle between J-J line and Frankfort plane (FHP) medio-lateraly onto coronal plane
Fig. 3 The three-dimensional cephalometric measurements of the maxilla; a maxillary length, b maxillary width, c maxillary height, d maxillary
antero-posterior inclination, e maxillary medio-lateral inclination
Statistical analysis computing R2. P-value < 0.05 was considered statisti-
IBM SPSS Statistics for Windows, Version 26.0 (Armonk, cally significant.
NY: IBM Corp.), was used. Intra- and inter-observer reli-
ability analysis for the SOS scoring was calculated using Results
Cohen’s Kappa coefficient [26]. In contrast, the three- CBCT scans of 500 patients aged 6 to 25 years; with a
dimensional measurements’ reliability was calculated mean age of 13.89 ± 1.13 years were analyzed. It included
by absolute and relative technical measurement errors 274 females and 226 males with mean ages of 13.68 ± 5.30
(TEM and RTEM) and Intra-class Correlation Coefficient and 14.14 ± 4.99 years, respectively. The distribution of
(ICC) test. Descriptive statistics, including each vari- subjects according to the spheno-occipital synchondrosis
able’s mean and standard deviation, were calculated and fusion stages, age and gender is presented in (Additional
presented. Dahlberg’s formula was also used to calculate file 1: Table S3). The results of the intra- and inter-exam-
the Standard Deviation of Measurement Error (SE) [43]. iner reliability analysis for the SOS scoring were "almost
Quantitative data for the normal state was explored by perfect"; weighted Kappa agreement measures were more
the verification distribution of data. Depending on Sha- than 0.900 for each observer (Additional file 1: Table S4).
piro–Wilk test and Kolmogorov–Smirnov test, all groups Three-dimensional maxillary cephalometric measure-
showed a normal distribution. The data were presented ment’s reliability was "excellent agreement"; R* values of
as mean and standard deviation (SD) for comparative TEM and RTEM were higher than 0.95% and ICC above
analysis. 98% with P < 0.05 (Additional file 1: Table S5).
One-way ANOVA test was used to compare between The results showed that there was a statistically sig-
the SOS maturation stages (four SOS groups per gen- nificant differences in the millimetric maxillary meas-
der: independent variables) regarding the linear and urements (ANS-PNS, J-J, and J-FHP), but there was no
angular measures of the maxilla (dependent variables) statistically significant differences in the angular maxil-
for males and females separately. The problem of com- lary measurements (PP/FHP, and J-J/FHP) for both gen-
parisons was treated by using Bonferroni correction, ders as presented in Table 3. The pair-wise comparison
adjusting the P-value for multiple comparison tests, to (Bonferroni Post hoc analysis) showed differences across
avoid type I error. different SOS stages.
The growth curves for maxillary parameters based Regarding the mean differences in the maxillary growth
on SOS maturation stages and chronological age were among the SOS stages (Table 4 and Fig. 4); the results
determined following a previous study [44]. R-statis- showed there were statistically significant mean dif-
tical programing language was used for graphing and ferences between SOS stages 2 and 3, that were larger
than those stages 1 and 2 and stages 3 and 4 in males
Table 3 Descriptive statistics and the results of the One-way ANOVA test between SOS fusion stages and 3D measurements of
maxillary growth pattern for males and females separately
Measurement Gender Stage 1 Stage 2 Stage 3 Stage 4 SOS groups
Comparison One-
way ANOVA
Mean ± SD Mean ± SD Mean ± SD Mean ± SD p-value
a b cd d
ANS-PNS (mm) M 44.15 ± 3.22 46.01 ± 3.31 48.85 ± 3.18 50.34 ± 2.88 0.000**
F 42.36 ± 2.82a 43.47 ± 2.64a 45.56 ± 2.91b 46.98 ± 2.56c 0.000**
J-J(mm) M 62.98 ± 2.94a 66.44 ± 3.02ab 67.93 ± 3.44bc 68.76 ± 3.53c 0.000**
F 59.80 ± 3.31a 62.99 ± 2.93b 64.56 ± 2.67 cd 65.18 ± 3.06d 0.000**
J-FHP (mm) M 25.16 ± 3.05a 27.01 ± 3.43b 29.62 ± 3.05 cd 30.12 ± 2.76d 0.000**
F 23.32 ± 2.46a 25.06 ± 2.43b 27.73 ± 3.12 cd 28.13 ± 2.83d 0.000**
(PP/FHP) ° M 1.73 ± 1.86 1.70 ± 2.00 2.01 ± 2.17 2.25 ± 2.34 0.432
F 2.32 ± 2.18 1.86 ± 1.85 2.16 ± 2.02 1.92 ± 1.85 0.559
(J-J/FHP) ° M 1.17 ± 0.83 1.17 ± 1.05 1.12 ± 0.80 1.35 ± 1.03 0.568
F 1.04 ± 0.70 1.17 ± 1.00 1.29 ± 1.08 1.15 ± 0.78 0.515
*
Indicate significance at the 0.05 level (2-tailed). **. Indicate significance at the 0.01 level (2-tailed). (a, b, c, d) Superscripts in the same row represent a statistically
significant difference between SOS stages according to multiple comparisons of Bonferroni Post hoc analysis
and females for maxillary measurements in millimetric method requires expert knowledge and expenditure
(ANS-PNS and J-FHP). However, the maxillary millimet- of time by the operator, and their accuracy is not very
ric measurement) J-J (was higher between SOS stages 1 high. It also had the drawback of unnecessary radio-
and 2 than those between stages 2 and 3, and stages 3 and graphic dose in an area away from the area of interest
4. Otherwise, the maxillary millimetric measurement (J-J, [11].
ANS-PNS (in males), and J-FHP) had no significant mean There were significant differences in the mean max-
difference between SOS stages 3–4 in both genders. illary linear parameters among SOS maturation stages
The basic maxillary growth curves according to SOS for males and females as the following: maxillary length,
stages, chronological age for females and males with the width, and height. However, there was no statistically
effect size R2 and P < 0.05 are graphically presented in significant difference for maxillary angular parameters
Fig. 5. in anteroposterior and mediolateral directions. This
might indicate that the SOS maturation stages have
similar proportional growth increases with significant
Discussion maxillary parameters. So, this may support the use of
The evaluation of skeletal maturation of craniofacial the SOS maturation stages as a valid method to assess
complex has critical importance in orthodontic, and the three-dimensional maxillary growth. This finding
dentofacial orthopedic. Recently, the SOS method has is comparable with gold standard method of validity of
been considered as a reliable tool and correlated well CVM method for assessment of facial growth [18, 48].
with other established methods; Hand-wrist maturation The mean differences in the maxillary growth
and CVM index in assessment of skeletal age [10, 18, 22, between SOS stage 2 and 3 were larger than those
23, 25, 45–49]. However, no study in the available litera- between stages 1and 2 or stages 3 and 4 in males and
ture related to the three-dimensional maxillary growth females for maxillary length and height. This might
and the SOS fusion stages. indicate that the maxillary growth peak is between
The superiority of SOS method may relate to the stages 2 and 3. This finding may be supported by the
critical location of SOS in cranial base. In which its theory that spheno-occipital synchondrosis begins to
late ossification and contribution to post-natal cranial fuse around growth puberty [22, 24, 35]. However, the
base growth play critical role in facial development [1, maxillary width’s mean difference was higher between
2, 50–52]. Moreover, the CBCT have been used widely SOS stages 1 and 2 than those stages 2 and 3, and stages
in dental field, so the SOS may be considered as suit- 3 and 4. This finding may reinforced by what reported
able method as CBCT provides the benefits of low-cost, in literature about facial growth sequence [54]; the
high-resolution, accurate three-dimensional imaging sequential completion of the cranium followed by facial
(3D) without the risk of increased radiation exposure width, then facial depth and height. Otherwise, the
to the patient, and easy visualization of superimposed maxillary millimetric measurement (width, length (in
bony structures [53]. On the other hand, Hand -wrist
Table 4 Female and male maxillary growth mean differences across the SOS maturation stages
Gender Stage 1-Stage 2 Stage 2-Stage 3 Stage3-Stage 4 P- value
Measurement Mean diff CI 95%; Min CI 95%; Max Mean diff CI 95%; Min CI 95%; Max Mean CI 95%; Min CI 95%; Max
ANS-PNS (mm) M 1.86AB 0.25 3.47 2.84BC 1.23 4.45 1.49DD − 0.07 3.06 P < 0.05*
AA AB BC
F 1.11 − 0.31 2.54 2.08 0.76 3.40 1.43 0.30 2.56
J-J(mm) M 3.46AA 1.79 5.13 1.49AB − 0.18 3.16 0.83CC − 0.80 2.45
F 3.19AB 1.61 4.76 1.57BC 0.12 3.03 0.62DD − 0.62 1.87
J-FHP (mm) M 1.86AB 0.28 3.43 2.61BC 1.03 4.18 0.50DD − 1.03 2.04
AB BC
F 1.74 0.28 3.20 2.67 1.32 4.02 0.40DD − 0.76 1.55
Bold value indicates P < 0.05
*
Indicate significance at the 0.05 level (2-tailed). (A, B, C, D) Superscripts in the same row represent a statistically significant difference between SOS stages according to multiple comparisons of Bonferroni Post hoc
analysis
Fig. 4 Female and male maxillary basic growth increments between the SOS maturation stages; a maxillary length increments, b maxillary width
increments, c maxillary height increments
Fig. 5 Female and male maxillary basic growth curves according to the SOS maturation (stages1-4) and chronological age (6 through 25 years); a
maxillary length curve, b maxillary width curve, c maxillary height curve
males), and height) had no significant mean difference Moreover, there was sexual dimorphism in mentioned
between SOS stages 3–4 in both genders. This may maxillary growth curves as the fusion of SOS and growth
indicate a lesser growth during this period and agree of maxilla were earlier chronological age in females than
with theory of the earlier maturation of maxilla for males. This sexual dimorphism consistent with previous
mentioned parameters [55, 56]. research that reported the SOS fuses earlier in females
The basic growth curves of maxillary parameters were than in males [24, 26, 31, 32]. The effect size ( R2) of SOS
constructed based on SOS maturation stages and chrono- fusion stages on the maxillary length, width, and height
logical age in both genders as the following: the maxillary ranged from 19 to 36% for females and from 32 to 39%
length, width, and height had increased with increasing for males. These percentages represent the variations of
chronological age, early in females than males. But the these maxillary parameters due to the SOS maturation
increasing for these parameters with SOS’s fusing were in stages. According to previous studies [13, 57], the R2
stages 1, 2, and 3 (primarily accelerated in stages 2 and 3); considered high for biological data (based on the CVM
they then tended to be steadier in stage 4 for males and method) when it ranges from 30 to 67%. So, this may
females in a similar pattern. These findings may indicate reflect the applicability of the presented growth curves as
that the maxillary parameters had maximum growth as the effect size of SOS on the maxillary parameters is rela-
the SOS was still fusing than the fused stage (stage 4) for tively moderate to high for females and high for males.
males and females. That is comparable with Jabour and As a clinician, it is worthy to mention that regard-
Anwar Shawqi’s finding of mandibular length and SOS ing the clinical implications of using the SOS fusion
fusing stages [22]. stages as a maxillary skeletal indicator; this study was
designed to compare different categories of ages based should be there for cases refereed to this imaging modal-
on the expected maxillary growth changes during these ity or specific CBCT parameters are to be set for this
different ages and because age is a weak determinant, purpose.
a more standardized and well-established method was
selected to answer this question (SOS) so that the cli- Conclusions
nician can decide whether to proceed with the growth The SOS maturation stages are valid and reliable maxil-
modification mechanics or to wait for proper stage of lary skeletal maturation indicators for three-dimensional
intervention. maxillary growth in both genders.
In this study, the overall view about the three-dimen- The mean differences in the maxillary growth between
sional maxillary growth during SOS fusion stages SOS stages 2 and 3 were higher than those between
in both genders, assessing the reliability of the SOS stages 1and 2 and stages 3and 4 for maxillary length and
method as a skeletal indicator of 3D maxillary growth, height in both genders. However, the maxillary width’s
and 3D maxillary growth spurt based on SOS fusion mean difference was higher between SOS stages 1 and 2
stages, which aren’t available in the published litera- than those stages 2 and 3 and stages 3 and 4. On other
ture is now presented. This may have an importance in hand, there may be lesser maxillary growth between SOS
orthodontic diagnosis or considered as a base for fur- stages 3 and 4 for maxillary width, length (in males), and
ther research in the future. height.
The clinical application of these findings suggests The basic growth curves showed high active growth of
that if SOS is still fusing, the individual would have the maxilla as the SOS was still fusing (especially stage
the maximum maxillary growth in width, length, and 2 and 3) than those of the fused (stage 4). Moreover, the
height. Moreover, the maxillary growth completion acceleration of growth occurred earlier in females than
based on SOS fusion stages and chorological age follow males regarding chronological age but not for SOS matu-
sequences of width, then length and height. So, these ration stages.
findings may help understand the three-dimensional
growth pattern of the maxilla according to the SOS
Abbreviations
maturation stages during treatment planning for ortho- SOS Spheno-occipital synchondrosis
dontic, dentofacial orthopedic, or orthognathic treat- DICOM Digital imaging and communications in medicine
ment planning. CBCT Cone beam computed tomography
CT Computed tomography
The limitation of this study starts with its nature as a 3D Three-dimensional
cross-sectional study; there is no doubt that the longi- ICC Intra-class correlation coefficient
tudinal studies of the maxillary growth and develop-
ment provide a more thorough understanding. However, Supplementary Information
the challenges of acquiring high sample numbers for a The online version contains supplementary material available at https://doi.
longitudinal study, the related increase in the number org/10.1186/s12903-023-02774-w.
of radiographic exposures during the follow up time,
Additional file 1: Table S1. Definitions of the maxillary three-dimensional
and the ethical considerations are likely to rule out this skeletal landmarks; Table S2. Definitions of the three-dimensional
approach and to use the cross-sectional direction as an craniofacial reference planes and lines; Table S3. Distribution of subjects
alternative. Also, this study might be considered as pri- according to spheno-occipital synchondrosis fusion stage, age and gen‑
der; Table S4. The reliability SOS staging; Table S5. Reliability analysis of
mary reporting in this field, and we hope there will be three-dimensional maxillary measurements.
more detailed studies in future of a longitudinal design.
Another limitation is that the ethnic group is limited to
Acknowledgements
the Chinese population, making it less practical for other Not applicable.
ethnicities. The sample had no skeletal classes or facial
Author contributions
pattern specifications, which might affect the current
W.S.A., and R.A; collection of the data, analysis of the data and writing the
findings. Despite the advantages of CBCT of low-cost, original draft. M.S.A and W.S.A; Conceptualization and methodology. S.A.E, and
high-resolution, accurate three-dimensional imaging R.K.A; statistical analysis. I.A, M.S.A, and H. L; review and editing. Y.Z, and W.L;
supervision. All authors read and approved the final manuscript. All authors
(3D) without the risk of increased radiation exposure
read and approved by the final manuscript.
to the patient, easy visualization of superimposed
bony structures, and the highly used in the dental field, Funding
This project was supported by the Open Subject Foundation of Key Labora‑
detailed description of the SOS method can only be done
tory of Dental Maxillofacial Reconstruction and Biological Intelligence Manu‑
with CBCT imaging, and it is not very obvious in plain x- facturing (20JR10RA653-ZDKF20210101), School of Stomatology, Lanzhou
ray, but the use of this technology should be based on the University, Gansu Province, Lanzhou 730000, PR China.
benefit risk ratio. When this is the case, other problems
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