Quantitative skeletal evaluation based on cervical vertebral maturation: a longitudinal study of adolescents with normal occlusion

Article Outline

• Abstract
• Materials and methods
• Results
• Discussion
• Funding
• Competing interests
• Ethical approval
• References
• Copyright

Abstract 

The study aims were to investigate the correlation between vertebral shape and hand–wrist maturation and to select characteristic parameters of C2–C5 (the second to fifth cervical vertebrae) for cervical vertebral maturation determination by mixed longitudinal data. 87 adolescents (32 males, 55 females) aged 8–18 years with normal occlusion were studied. Sequential lateral cephalograms and hand–wrist radiographs were taken annually for 6 consecutive years. Lateral cephalograms were divided into 11 maturation groups according to Fishman Skeletal Maturity Indicators (SMI). 62 morphological measurements of C2–C5 at 11 different developmental stages (SMI1–11) were measured and analysed. Locally weighted scatterplot smoothing, correlation coefficient analysis and variable cluster analysis were used for statistical analysis. Of the 62 cervical vertebral parameters, 44 were positively correlated with SMI, 6 were negatively correlated and 12 were not correlated. The correlation coefficients between cervical vertebral parameters and SMI were relatively high. Characteristic parameters for quantitative analysis of cervical vertebral maturation were selected. In summary, cervical vertebral maturation could be used reliably to evaluate the skeletal stage instead of the hand–wrist radiographic method. Selected characteristic parameters offered a simple and objective reference for the assessment of skeletal maturity and timing of orthognathic surgery.

Key words: skeletal evaluation, cervical vertebrae, adolescents

Orthognathic surgery is generally performed in patients affected by dental–skeletal facial abnormalities, which can affect their mastication, aesthetic appearance, self-esteem, confidence and lifestyle¹³, ¹⁴, ¹⁸. Increasing numbers of adolescents and young adults are undergoing facial skeletal surgical procedures.

Body image can affect behaviour and emotional development, especially for female patients², ¹⁸. Their primary motives for seeking surgery are aesthetic and they hope to solve the problem as soon as possible², ²⁰. Orthognathic surgery should be carried out once growth and development are complete, so that the minimum relapse and maximum stability can be assured. This raises a question about when growth and development end. What is the earliest sign that establishes the end of growth and development so that orthognathic surgery can be started?

Clinically, it is often recommended that jaw surgery should be carried out after the age of 18 years, because that is the age at which growth and development are considered to have finished. It has long been recognized, however, that an individual's chronological age does not necessarily correlate well with their maturational age⁸.

Traditionally, maturational status has been evaluated by hand–wrist radiographs, which are considered the gold standard⁶, ⁸, ²⁴, even though their clinical usefulness has been questioned¹¹, ²³. There are also concerns about extra radiation exposure. The shape of the cervical vertebrae is related to skeletal maturation, permitting skeletal age assessment from cephalograms, instead of subjecting the patient to the additional radiation of a hand–wrist radiograph⁸, ²⁴.

It is not known whether the cervical vertebral maturation (CVM) method provides the same accurate and simple information as an assessment based on hand–wrist radiographs. If hand–wrist and cervical maturation methods were highly correlated, there would be no justification in taking a hand–wrist radiograph for skeletal maturation determination. Comparisons of skeletal maturation between hand–wrist and cervical vertebrae indicators have been made⁸, ²⁴, but no comparison based on longitudinal data was reported. Longitudinal data presented on a yearly basis are of great value to orthodontists interested in the detailed study of facial growth²⁵.

Regarding the morphometric issues of cervical vertebrae, shape measurements have either been confined to the height–width ratio of limited vertebral bodies (the third to fourth cervical vertebra)⁵, ¹⁶, or just used or referred to the atlas reported by Lamparski¹, ⁹, ¹². Using the limited cervical measurements might affect the correlation obtained because much useful information will be missed.

Cervical vertebrae have fewer indicators of skeletal maturity compared with the hand–wrist, but they have obvious morphological changes at different developmental stages. The use of an atlas is convenient because changes in cervical vertebral bodies can be evaluated with regard to growth in the atlas. However, an atlas cannot be used to evaluate growth in an objective and detailed manner because it uses all vertebrae as a group. The observation of different vertebral bodies is sometimes contradictory. This leads to confusion between various indicators and inaccurate or subjective results¹⁵. A more comprehensive shape analysis and more specific parameters could provide additional information to show the underlying morphometric relationship and increase the predictive power.

The purpose of this study, using mixed longitudinal samples, was twofold. First, to determine whether the morphological changes seen in the cervical vertebrae were as useful as those from hand–wrist radiographs to determine the growth stage in Chinese subjects. Second, to select characteristic parameters from the second to fifth cervical vertebrae (C2–C5) to evaluate skeletal maturation objectively from lateral cephalometric radiographs.

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Materials and methods 

This study was a retrospective review of available data. Longitudinal population data were derived from Beijing University Research Center of Craniofacial Growth and Development. More than 900 patients born in 1977–1978 were reviewed initially. The final study population consisted of 87 adolescents (32 males, 55 females) aged 8–18 years with normal occlusion because of the problems of longitudinal radiographical recordings. They formed two groups depending on the age at which the recordings began. Observation began for group 1 (43 adolescents, 16 males, 27 females) at 8–9 years, and for group 2 (44 adolescents, 16 males, 28 females) at 12–13 years of age. Sequential lateral cephalograms (LCR) and hand–wrist films were taken once a year, for 6 consecutive years. Informed consent was obtained from all 87 adolescents and their parents. The study protocol was reviewed and approved by the Institutional Review Board.

The 87 subjects fulfilled the following criteria: deciduous, mixed, or permanent dentition; normal occlusion (<3mm overjet, and overbite less than one-third coverage of mandibular incisor); harmonious facial profile and lip competence at rest; and no orthodontic treatment or extractions of permanent teeth.

Most previous studies were based on Lamparski's atlas by direct image-reading¹, ⁹, ¹². In this study, Lamparski's atlas was not used. The samples were divided into 11 maturation groups according to the Fishman Skeletal Maturity Indicators (SMI)⁷, which was thought to be the gold standard for skeletal maturation evaluation⁶, ⁸, ²⁴.

The SMI system uses only 4 stages of bone maturation, all found at 6 anatomical sites located on the thumb, third finger, fifth finger and radius. The 11 discrete adolescent SMI, covering the entire period of adolescent development, are (in chronological order): (1) width of epiphysis as wide as diaphysis in the third finger, proximal phalanx; (2) width of epiphysis as wide as diaphysis in the third finger, middle phalanx; (3) width of epiphysis as wide as diaphysis in the fifth finger, middle phalanx; (4) ossification of adductor sesamoid of thumb; (5) capping of epiphysis in the third finger, distal phalanx; (6) capping of epiphysis in the third finger, middle phalanx; (7) capping of epiphysis in the fifth finger, middle phalanx; (8) fusion of epiphysis and diaphysis in the third finger, distal phalanx; (9) fusion of epiphysis and diaphysis in the third finger, proximal phalanx; (10) fusion of epiphysis and diaphysis in the third finger, middle phalanx; (11) fusion of epiphysis and diaphysis in radius.

LCRs of all subjects, coupled with hand-wrist radiographs, totalled 522, of which 4 radiographs did not reach even SMI1 and 7 radiographs were discarded because they were fuzzy. The remaining 511 LCRs were divided into 11 maturation groups by a calibrated technician according to SMI assessed from their hand–wrist radiographs, as shown in Table 1. 62 morphological characteristic parameters of C2–C5 at 11 different developmental stages (SMI1–11) were measured and analysed.

Table 1. Demographic distribution of 511 lateral cephalograms in 11 groups according to the SMI (mean±SD).

SMI	N	Average age (year)		Age range (year)
		Females (X±SD)	Males (X±SD)	Females	Males
1	31	9.01±1.47	9.81±1.41	7.00–10.49	7.83–11.25
2	28	9.67±1.02	10.83±0.93	8.50–11.07	9.65–11.80
3	30	10.01±1.50	11.29±1.15	8.52–12.08	10.15–12.50
4	28	10.71±0.45	11.61±0.54	10.28–11.97	11.03–13.17
5	28	11.18±1.19	12.28±0.60	10.07–13.17	12.00–13.57
6	32	11.92±1.46	12.81±0.67	10.25–14.17	12.08–14.33
7	28	12.29±0.91	13.65±0.95	11.28–14.33	12.25–15.75
8	30	12.98±0.61	14.19±1.23	12.05–13.75	13.00–16.07
9	38	13.64±1.20	15.17±0.79	12.25–15.50	14.10–16.20
10	52	14.93±0.90	16.22±1.10	13.88–16.33	14.93–17.50
11	49	16.41±1.39	17.60±0.50	13.98–17.92	16.00–18.18

The parameters correlated with SMI were selected using a new modelling method based on a nonparametric method, called locally weighted scatterplot smoothing (LOESS), which is very flexible and can account for a much wider range of component patterns than any single parametric model¹⁰. The characteristic parameters for assessing cervical vertebral maturation were selected by correlation coefficient analysis and variable cluster analysis.

All points and lines shown in Fig. 1, Fig. 2 and defined in Table 2 were traced with a pencil by one observer under optimal conditions and then measured with micrometer callipers. The ratios of these parameters, as defined in Table 2, were calculated.

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• Fig. 1. 

  Measuring points used in the cephalometric analysis. C2d–C5d, the most superior point of the lower border of the body of C2–C5; C2a, C2p, C3la, C3lp, C4lp, C5la, C5lp, the most posterior and the most anterior points on the lower border of the body of C2–C5; C3ua, C3up, C4ua, C4up, C5ua, C5up, the most superior points of the posterior and anterior borders of the body of C3–C5; C3um, C4um, C5um, the middle of the upper border of the body of C3–C5; C3am, C4am, C5am, the middle of the anterior border of the body of C3–C5.

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• Fig. 2. 

  Measuring lines used in the cephalometric analysis. UW, vertical distance of Cua to the connection of Cup and Clp; W, vertical distance of Cam to the connection of Cup and Clp; LW, vertical distance of Cla to the connection of Cup and Clp; PH, vertical distance of Cup to the connection of Clp and Cla; H, vertical distance of Cum to the connection of Clp and Cla; AH, vertical distance of Cua to the connection of Clp and Cla; AD, distance between Cla and Cua; PD, distance between Clp and Cup.

Table 2. Measuring lines and ratios used in the cephalometric analysis.

The data were analysed using statistical software SPSS Version 13.0 for Windows. The arithmetic mean and standard deviation were calculated for all 62 variables. The statistical analyses used included locally weighted scatterplot smoothing (LOESS), correlation coefficient analysis (CC) and variable cluster analysis.

Intraobserver reliability and reproducibility of the linear measurements were checked on 20 randomly selected cephalometric radiographs that were retraced and redigitized 2 weeks later. The method error did not exceed 0.2mm for all linear variables.

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Results 

After statistical analysis of LOESS smoothing (Fig. 3), among 62 parameters, 44 parameters were positively correlated with SMI, 6 were negatively correlated and 12 were not correlated (Table 3). Those that were not relevant were parameters relating to cervical vertebral width (UW, W, LW, UW/LW), although the ratios of cervical vertebral width such as H4/W4, H3/W3, had a strong correlation with SMI (0.9107 and 0.9091, respectively) as shown in Table 3. Parameters of inter-vertebral distance had a negative correlation with SMI, meaning that the vertebral space became smaller with growth.

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• Fig. 3. 

  (a) @2: Antero-superior angle of C2d–C2p connection to C2p–C2a connection. (b) H4/W4: ratio of H4 to W4. (c) PI4–5: Distance between C4lp and C5up. (d) UW3: Vertical distance of C3ua to the connection of C3up and C3lp.

Table 3. Correlation coefficient (CC) between 50 correlated parameters and SMI.

The CC between 50 correlated parameters and SMI was derived through correlation coefficient analysis. These parameters were arranged in descending order according to CC (Table 3). The CC were relatively high; the highest was 0.9107 and 34 were above 0.8008 (Table 3).

The external environment such as X-ray projection angles, distance, pressure, corporal position or disease may have an influence on the height of the vertebral bodies. Facial pattern could also modify the height of cervical vertebrae. Considering the distortion and magnification of LCR, ratio and angle measurements would be better than linear measurements for comparability and validity. 25 parameters of ratio and angle were selected to calculate cervical vertebral maturation, which meant the shape of the cervical vertebrae rather than their size would be taken into account. By the method of variable cluster analysis, 25 parameters could be divided either into three groups with total variance explained being 97% or four groups with total variance explained being 98% (Table 4). The parameters in one group had a similar correlation trend with SMI and were arranged in descending order according to CC. Thus the first of each group could be chosen to assess cervical vertebral maturation, which were H4/W4, AH3/PH3, @2 or H4/W4, AH3/PH3, @2, AD3/PD3, respectively.

Table 4. Parameters classification by variable cluster analysis.

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Discussion 

Orthognathic surgery has a positive impact on the quality of life in patients with jaw deformity and facial asymmetry, improving physical and social aspects and, in female patients in particular, it improves emotional disturbance¹⁸, ²². For adolescents who are often eager to achieve a face with stable occlusion and improved appearance as soon as possible, pre-surgical orthodontic treatment and orthognathic surgery can begin at an earlier age, if there is an accurate prediction of the remaining growth. The success of orthodontic or surgical (or both) treatment depends on understanding this⁸, ¹⁹.

It is important to determine which method is best for predicting remaining growth with more accuracy than chronological age, but not requiring extra radiation exposure as with hand–wrist radiography, and which parameters are the best indicators for predicting maturation level.

The methodology of this investigation differed from previous research. A new modelling method, LOESS, was used to study the relationship between cervical vertebral parameters and SMI. LOESS smoothing is a nonparametric method for estimating regression curves/surfaces¹⁰. The LOESS method allows great flexibility because no assumptions about the parametric form of the regression curve/surface are needed. It can also be used in situations in which a suitable parametric form of the regression curve/surface is not known. It is also suitable when there are outliers in the data and a robust fitting method is necessary. It provides more information than any single parametric model (Fig. 3).

Flores-Mir et al.,⁸ assessed the correlation between the SMI and the traditional CVM method proposed by Baccetti et al.¹ Flores-Mir found that all these correlation values were moderately high for early, average or late mature adolescents (early: 0.725, average: 0.698, late: 0.871). The present result was in accordance with this study and strong correlation could be found between cervical vertebral parameters and SMI as shown in Table 3. The morphological parameters of the cervical vertebral bodies could be used reliably to evaluate the maturation stage instead of the hand–wrist radiograph. Previous research found that correlation values between hand–wrist radiographs and cervical vertebrae evaluation were variable (from 0.45 to 0.97)³, ⁴, ¹⁵. Differences between studies can be expected on the basis of factors such as sample size, sex, or method used. Previous studies were based on cross-sectional data.

The size of the samples in the present study was comparatively small but an advantage was that they were based on mixed longitudinal data. Longitudinal research is an essential method for in-depth study of craniofacial growth and development, which can investigate the individual's unique development type and make a continuous comparison¹⁷, ²⁶. Investigations using this method are limited because of the problems of longitudinal radiographic recordings. As shown in this study, of more than 900 patients only 87 samples had at least 6 consecutive annual lateral cephalograms and hand–wrist radiographs.

The use of SMI has advantages over the other skeletal maturation determination methods, but current stringent ethical criteria from the institutional ethical boards make the use of hand–wrist skeletal maturation determination less feasible. Increased radiation exposure is the main objection. In some retrospective research, the lack of hand–wrist radiographs may limit the applicability of existing data. The use of cervical vertebrae maturation determination appeared to be a useful tool in situations where no hand–wrist radiographs were available.

Ideally, the correlations between vertebral shape and hand–wrist maturation should reflect the summation of the biological relationship between these two skeletal units. Each vertebra or vertebral body was independently evaluated, instead of using all vertebrae as a group. This gave information about which parameters were the best predictors of maturation level and allowed potential clinical application by using a select parameter from a vertebra. This new method would be more simple and accurate to use than considering all parameters together. The influence of subjectivity was limited through quantification and simplification of parameters.

Earlier researchers selected the third and fourth vertebral bodies for maturation assessment⁵, ¹⁶, but this would miss some useful information because of limited parameters. Concavity of the lower border was not considered in their studies. Concavity of the lower border has been recognized as one of the most important indicators from Lamparski's atlas in 1972 to the CVMS proposed by Baccetti in 2002¹, ¹². San Roman et al., studied the changes in concavity of the lower border, height, and shape of the vertebral body²¹. The result showed that concavity was the best of the three parameters, so it should not be ignored. In this study, 62 parameters of C2–C5 were measured. Morphological changes of C2 and C5 also have a strong correlation with hand–wrist bone age (Table 3). The study indicated that parameters of C2 and C5 could also be indicators for evaluation of cervical vertebral bone age. In the present study, @2 (Antero-superior angle of C2d–C2p connection to C2p–C2a connection, as defined in Table 2) had a strong correlation with SMI (CC: 0.8617) and this was in agreement with some other studies¹, ¹², ²¹. From SMI1 to SMI11, the @2 value increased gradually and was consistent with the generally accepted concept that the greater the maturation the higher the concavity. This demonstrated the validity of @2 in the evaluation of cervical vertebral bone age.

The present study showed that the parameters of cervical vertebral width (UW, W, LW) had no correlation with SMI (Table 3), whereas the ratios of cervical vertebra width such as H4/W4 (ratio of H4 to W4, as defined in Table 2) had a strong correlation with SMI (CC: 0.9107). The results indicated that the growth of cervical vertebral width had been almost completed in earlier cervical growth so that the width parameters were not appropriate for cervical vertebral maturation evaluation. In later growth stages, the morphological changes of cervical vertebrae were mainly an increase of height. In the first stage of maturation the vertebral bodies were wedge-shaped with the superior vertebral borders tapered posterior to anterior. With growth, the vertebral bodies became rectangular shaped, square shaped, and finally rectangular with height greater than width.

As classified in Table 4, using three or four parameters rather than all of them, made maturation assessment more simple, accurate and objective. Figure 4 shows that those characteristic variables changed significantly from SMI1 to SMI11, which further confirmed the results.

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• Fig. 4. 

  (a) Initial stage of cervical vertebral maturation. (b) Progress stage of cervical vertebral maturation. (c) Final stage of cervical vertebral maturation.

The method provided useful clinical information for assessing the timing of orthognathic surgery. For example, for a young adult who requires surgery as soon as possible, if the lower border concavity of C2 is obvious, the superior vertebral border of C3 is flat and the shape of C4 is rectangular with height greater than width, it can be concluded that growth has terminated and orthognathic surgery is feasible, even though the patient is still young chronologically.

Further research should be conducted on purely longitudinal data and with larger samples. And a predictive algorithm should be derived using the characteristic variables (H4/W4, AH3/PH3, @2 or H4/W4, AH3/PH3, @2, AD3/PD3) to make these findings more useful for the clinical practices of orthognathic surgery and pre-surgical orthodontics.

In summary, the correlation coefficients between cervical vertebral parameters and SMI were relatively high. The morphological changes of the cervical vertebrae could be used reliably to evaluate the maturation stage instead of the hand–wrist radiograph. Selected characteristic parameters can be used to evaluate skeletal maturation in a more simple and objective way.

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Funding 

This article is funded by National Natural Science Foundation of China (No. 30801314).

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Competing interests 

The first author certifies that the authors have no commercial associations (e.g. consultancies, stock ownership, equity interests, patent licensing arrangements, etc.) that pose a conflict of interest in connection with the submitted article. The first author declares that the above statement is true on behalf of all the authors related to this study.

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Ethical approval 

The study protocol was reviewed and approved by the Research Subject Review Board and Ethical Scientific Board of Huazhong University of Science and Technology. Informed consent was obtained from all families of participants and volunteers prior to cephalometric analysis.

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References 

1. Baccetti T, Franchi L, Mcnamara JA. An improved version of the maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72:316–323
   • View In Article
   • MEDLINE
2. Bellucc CC, Kapp-Simon KA. Psychological considerations in orthognathic surgery. Clin Plast Surg. 2007;34:e11–e16
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (92 KB)
   • CrossRef
3. Caltabiano M, Leonnardi R, Zaborra G. Evaluation of cervical vertebrae for determination of skeletal age. Riv Ital Odontoiatr Infant. 1990;1:15–20
   • View In Article
   • MEDLINE
4. Chang HP, Liao CH, Yang YH. Correlation of cervical vertebra maturation with hand-wrist maturation in children. Kaohsiung J Med Sci. 2001;17:29–35
   • View In Article
   • MEDLINE
5. Chen F, Terada K, Hanada K. A special method of predicting mandibular growth potential for class III malocclusion. Angle Orthod. 2005;75:191–195
   • View In Article
   • MEDLINE
6. Chen LL, Xu TM, Jiang JH. Quantitative cervical vertebral maturation in adolescents with normal occlusion: a mixed longitudinal study. Am J Orthod Dentofacial Orthop. 2008;134:720.e1–720.e7
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (598 KB)
   • CrossRef
7. Fishman LS. Radiographic evaluation of skeletal maturation. Angle Orthod. 1982;52:88–112
   • View In Article
   • MEDLINE
8. Flores-Mir C, Burgess CA, Champney M. Correlation of skeletal maturation stages determined by cervical vertebrae and hand-wrist evaluations. Angle Orthod. 2006;76:1–5
   • View In Article
   • MEDLINE
9. Franchi L, Baccetti T, Mcnamara JA. Postpubertal assessment of treatment timing for maxillary expansion and protraction therapy followed by fixed appliances. Am J Orthod Dentofacial Orthop. 2004;26:555–568
   • View In Article
10. Hafen RP, Anderson DE, Cleveland WS. Syndromic surveillance: STL for modeling, visualizing, and monitoring disease counts. BMC Med Inform Decis Making. 2009;9:21
    • View In Article
11. Isaacson KG, Thom AR. Guidelines for the use of radiographs in clinical orthodontics. London: British Orthodontic Society; 2000;22
    • View In Article
12. Lamparski Jr. DG. Skeletal age assessment utilizing cervical vertebrae [thesis]. Pittsburgh, PA: University of Pittsburgh 1972.
    • View In Article
13. Lee S, Mcgrath C, Samman N. Quality of life in patients with dentofacial deformity: a comparison of measurement approaches. Int J Oral Maxillofac Surg. 2007;36:488–492
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (102 KB)
    • CrossRef
14. Marsav G, Oztas E, Kuvat SV. Changes in soft tissue profile after mandibular setback surgery in Class III subjects. Int J Oral Maxillofac Surg. 2009;38:236–240
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (206 KB)
    • CrossRef
15. Mito T, Sato K, Mitani H. Cervical vertebral bone age in girls. Am J Orthod Dentofacial Orthop. 2002;122:380–385
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (156 KB)
    • CrossRef
16. Mito T, Sato K, Mitani H. Predicting mandibular growth potential with cervical vertebral bone age. Am J Orthod Dentofacial Orthop. 2003;124:173–177
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (91 KB)
    • CrossRef
17. Moyers RE. Handbook of Orthodontics. 4th edn. Chicago: Year Book Medical Publisher, INC; 1988;6–17
    • View In Article
18. Nicodemo D, Pereira MD, Ferreira LM. Effect of orthognathic surgery for class III correction on quality of life as measured by SF-36. Int J Oral Maxillofac Surg. 2008;37:131–134
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (96 KB)
    • CrossRef
19. Nollet PJ, Katsaros C, Huyskens RW. Cephalometric evaluation of long-term craniofacial development in unilateral cleft lip and palate patients treated with delayed hard palate closure. Int J Oral Maxillofac Surg. 2008;37:123–130
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (270 KB)
    • CrossRef
20. Sadek H, Salem G. Psychological aspects of orthognathic surgery and its effect on quality of life in Egyptian patients. East Mediterr Health J. 2007;13:150–159
    • View In Article
    • MEDLINE
21. San Roman P, Palma JC, Oteo MD. Skeletal maturation determined by cervical vertebrae development. Eur J Orthod. 2002;24:303–311
    • View In Article
    • MEDLINE
    • CrossRef
22. Turker N, Varol A, Ogel K. Perceptions of preoperative expectations and postoperative outcomes from orthognathic surgery: part I: Turkish female patient. Int J Oral Maxillofac Surg. 2008;37:710–715
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (98 KB)
    • CrossRef
23. Turpin DL. British Orthodontic Society revises guidelines for clinical radiography. Am J Orthod Dentofacial Orthop. 2008;134:597–598
    • View In Article
    • Full Text
    • Full-Text PDF (39 KB)
    • CrossRef
24. Wong RK, Alkhal HA, Rabie AB. Use of cervical vertebral maturation to determine skeletal age. Am J Orthod Dentofacial Orthop. 2009;136:484.e1–484.e6
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (365 KB)
    • CrossRef
25. Yavuz I, Ikbal A, Bayda B. Longitudinal posteroanterior changes in transverse and vertical craniofacial structures between 10 and 14 years of age. Angle Orthod. 2004;74:624–629
    • View In Article
    • MEDLINE
26. Zhang XZ, Zhou YH, Lin JX. Facial growth in vertical dimension of Chinese adolescents from 13 to 15 years old with normal occlusion in Beijing. J Pract Stomatol. 2006;22:460–464
    • View In Article