Correlation between Cervical Vertebral Maturation Stages and Dental Maturation in a Saudi Sample.

BACKGROUND: The aim of the present study was to compare the cervical vertebra maturation stages method and dental maturity using tooth calcification stages.
METHODS: The current study comprised of 405 subjects selected from orthodontic patients of Saudi origin coming to clinics of the specialized dental centers in western region of Saudi Arabia. Dental age was assessed according to the developmental stages of upper and lower third molars and skeletal maturation according to the cervical vertebrae maturation stage method. Statistical analysis was done using Kruskal-Wallis H, Mann-Whitney U test, Chi-Square test; t-test and Spearman correlation coefficient for inter group comparison.
RESULTS: The females were younger than males in all cervical stages. The CS1-CS2 show the period before the peak of growth, during CS3-CS5 it's the pubertal growth spurt and CS6 is the period after the peak of the growth. The mean age and standard deviation for cervical stages of CS2, CS3 and CS4 were 12.09 ±1.72 years, 13.19 ±1.62 and 14.88 ±1.52 respectively. The Spearman correlation coefficients between cervical vertebrae and dental maturation were between 0.166 and 0.612, 0.243 and 0.832 for both sexes for upper and lower third molars. The significance levels for all coefficients were equal at 0.01 and 0.05.
CONCLUSION: The results of this study showed that the skeletal maturity increased with the increase in dental ages for both genders. An early rate of skeletal maturation stage was observed in females. This study needs further analysis using a larger sample covering the entire dentition.

Introduction

Orthodontic treatment is most favorable and effective during pubertal growth and hence growth assessment and prediction are significant in planning treatments for dental and maxillofacial abnormities (, ). To evaluate the growth assessment and maturation many features such as body height, body weight, secondary sexual characteristics, dental and skeletal development are used. Dental maturity can be determined by the stage of tooth formation and numerous studies have found that dental maturity is associated with skeletal maturity. At present, analysis of cervical vertebrae is extensively used to evaluate skeletal maturity due to its simplicity and reproducibility from a routine diagnostic lateral cephalogram for orthodontic treatment (, ). Various authors have noted that developmental stages of certain teeth show a high correlation with skeletal maturity (). Yet few studies (, ) have been carried out to determine the association between tooth calcification stage and cervical vertebral maturation (CVM) stage. The aim of the present study was to investigate the correlation between the CVM stages method and dental maturity using tooth calcification stages of third molars.

Materials and methods

The present study consisted of a total of 405 patients attending orthodontic clinics of the specialized dental centers in western region of Saudi Arabia. All participants of the study were only of Saudi origin. Digital panoramic radiographs and lateral cephalograms along with clinical records of 255 girls and 150 boys aged 9-20 years were selected. The inclusion criteria were:

A high quality digital panoramic radiograph and lateral cephalogram

No history of medical or surgical disease affecting the presence and development of third molar teeth.

The following exclusion criteria were considered and the following patients were excluded from the investigation:

Patients with any congenital tooth anomalies or congenital anomalies of the 2nd, 3rd and 4th cervical vertebrae such as fusion between cervical vertebrae or presence of secondary ossicle were eliminated.

Patients having any systemic diseases that could affect growth (such as nutritional disturbance, endocrine disorders, syndromes, and long term consumption of medication) were excluded.

Dental maturity: The assessment of dental maturity was done according to the calcification stages of upper and lower third molar teeth. The development of teeth was categorized into different groups, ranging from A (least development) to H (complete development) ().

Skeletal maturity: The Skeletal maturity was evaluated by skeletal age using cervical vertebra maturation (CVM) stage method, assessing the morphology (shape and inferior border concavity) of three cervical vertebrae (C2, C3, and C4) consisting of six maturity stages (C1-C6) presented by Bacetti et al. (, ).

All digital radiographs were viewed on the same computer. The stages of cervical vertebra development and tooth formation of each patient were assessed by an orthodontist without having knowledge of age or gender.

Statistical method: The analysis was performed using the Statistical Package SPSS statistic V22.0 (IBM Corporation, New York, USA). The difference in proportion was tested using Kruskal-Wallis H followed by Mann-Whitney U test for inter group comparison, and Chi-Square tests. The difference in mean was tested using t-test. Molar stages were correlated with cervical vertebra developmental stages using the Spearman’s correlation coefficient. All statistical tests were two-sided, and the significance level was set at p < 0.05.

Results

Table 1 and 2 show the distribution of upper and lower third molar stages according to age and gender. In 9-12 years group the common upper third molar stages were C, B and D respectively, while the common lower third molar stages were C and D and B, there were no F, G and H stages in this age group. In 13-16 years group all third molar stages were present, the most common stage was stage D. In the age group more than 17 years, H stage of third molar was the most common in upper and lower third molars. In the female group of this Saudi sample the most common stage of third molar was stage D, while in the male group the common stages were stage D and H.

Table 1

Distribution subjects with upper third molar stages according to age and gender:

Age in years	Upper third molar stages									Total
	A	B	C	D	E	F	G	H	NA
9-12	6	32	38	28	8	0	0	0	28	140
13-16	0	12	52	138	72	38	8	10	12	342
≥ 17	0	0	0	34	28	76	66	122	2	328
Kruskal-Wallis H, p value 0.0001
Gender	A	B	C	D	E	F	G	H	NA
Male	2	20	42	60	36	38	8	68	26	300
Female	4	24	48	140	72	76	66	64	16	510
Chi-square, p value 0.0001

Table 2

Distribution subjects with lower third molar stages according to age and gender:

Age in years	Lower third molar stages									Total
	A	B	C	D	E	F	G	H	NA
9-12	6	28	48	34	8	0	0	0	16	140
13-16	4	16	48	148	90	12	4	14	6	342
≥ 17	0	0	4	30	40	72	60	122	0	328
Kruskal-Wallis H, p value 0.0001
Gender	A	B	C	D	E	F	G	H	NA
Male	6	18	50	70	46	20	8	68	14	300
Female	4	26	50	142	92	64	56	68	8	510
Chi-square, p value 0.0001

Table 3 shows the distribution of chronological ages for all subjects grouped by cervical vertebra developmental stages. The mean age and standard deviation for cervical stage 3 and 4 were 13.19 ±1.62 and 14.88 ±1.52 respectively; the females were younger than males in these cervical stages.

Table 3

Distribution of chronological ages for all subjects grouped by CVS:

Cervical vertebra developmental stages	n	Age(Mean ± SD)	Gender	n	Age(Mean ± SD)	P valvet-test
CS1	34	10.62 ±1.2	Male	22	10.73 ±1.31	0.12
			Female	12	10.42 ±1.06
CS2	34	12.09 ±1.72	Male	21	12.14 ±1.67	0.16
			Female	13	12 ±1.85
CS3	50	13.19 ±1.62	Male	25	14.14 ±1.19	0.07
			Female	25	12.24 ±1.43
CS4	88	14.88 ±1.52	Male	26	15.08 ±0.87	0.18
			Female	62	14.79 ±1.72
CS5	67	16.97 ±2.05	Male	23	18.17 ±1.92	0.08
			Female	44	16.34 ±1.84
CS6	132	18.55 ±1.52	Male	33	19.05 ±1.38	0.14
			Female	99	18.39 ±1.54

Table 4 shows the correlation coefficients between cervical vertebra developmental stages and third molar stages of subjects in both upper and lower third molars.

Table 4

Correlation coefficients between cervical vertebra developmental stages and third molar stages of subjects:

	Cervical vertebra developmental stages
	CS1	CS2	CS3	CS4	CS5	CS6
Upper third molar stages	0.267a	0.166b	0.287a	0.246a	0.612a	0.198b
Lower third molar stages	0.287a	0.243a	0.471a	0.634a	0.536a	0.832a
Age in years	0.732a	0.542a	0.532a	0.486a	0.631a	0.429a

a correlation is significant at 0.01 level, b correlation is significant at 0.05 level.

Discussion

Many biological indicators such as skeletal maturation of hand-wrist (), cervical vertebrae (, ) and dental development () have been used to evaluate for developmental age estimation. In addition to hand-wrist radiographs, the evaluation of CVM was used for assessing the skeletal maturation. On cephalometric radiographs, the developmental changes of cervical vertebrae were used to evaluate the degree of physiological maturity of a growing individual and also to calculate the bone age. Many researchers agree that evaluation of cervical vertebrae with routine lateral skull cephalograms are correlated and can be used to predict mandibular growth (, -). CVM explains the complete pubertal growth period by recording all significant phases in craniofacial growth during adolescence and young adulthood which is valid for both genders (, , ). Few researchers suggested a slight association between dental and skeletal maturity (, ). According to some studies, dental maturity with levels of calcification of teeth is considered to be a significant biologic factor (). Some researchers have found that CVM is a reliable method for skeletal maturity assessment (5, 9, 16, 17, 19]) Furthermore, they concluded that an additional x-ray exposure, apart from the routine lateral cephalometric projection, is not required.

This study investigated the interrelationship between cervical vertebrae maturation and dental ages of Saudi children. Some authors have found that developmental stages of certain teeth such as canines and second molars have a strong correlation with skeletal maturity (, , , ). However, the timing of third molar development showed the highest variability compared to all other developing teeth ().

In the present study, an assessment of skeletal maturity was done using the CVM on lateral cephalogram, and a routine diagnostic radiograph was used for orthodontic treatment. The study investigated the interrelationship of dental age using the third molars and skeletal maturity by assessing the maturity stages of cervical vertebrae. A recent study by Chen J et al, dental calcification stages were used to determine dental maturity, while skeletal maturity was evaluated by CVM method and statistically significant correlation was found between tooth calcification stage and cervical vertebra maturation stage ().

A distribution of chronological ages of all subjects according to cervical vertebra maturation stages is shown in Table-3. Based on CVM assessment, the mean chronologic age of girls was slightly lower than that of boys, with each stage being constantly earlier in female than in male subjects. In stage CS2 and CS4, the mean chronologic age was 12.09 ±1.72 years and 14.88 ±1.52 years respectively (Table-3). In CVM method, CS1-CS2 show the period before the peak of growth, during CS3-CS5 it’s the pubertal growth spurt and CS6 is the period after the peak of the growth (Table-3). The results of the present study are in compliance with those obtained in earlier studies by Baccetti et al (, ). The results of Spearman correlation coefficients between cervical vertebrae and dental maturation were between 0.166 and 0.612, 0.243 and 0.832 for both genders for upper and lower third molars respectively. The significance levels for all coefficients were the same at 0.01 and 0.05 (Table-4).

According to a number of researchers, the study of several selected teeth rather than the entire dentition gives higher correlation coefficients between dental and skeletal maturity since the probability of accidental errors will be reduced (, , ). The association between the teeth and skeleton also appear to vary among geographic regions and races/ethnic groups ().

In the current study, dental calcification stages were used to determine dental maturity and skeletal maturity was evaluated by CVM method, which is a widely used method. A low but statistically significant correlation was found between tooth calcification stage and cervical vertebra maturation stage. The correlation coefficients between calcification stages of upper third molars and skeletal maturity was a weak positive and was ranging from 0.166 to 0.0287, except for CS5 stage in which there was a moderate positive correlation [Table-4]. For lower third molars, there was a moderate positive correlation between cervical vertebra (CS4, CS5 and CS6) and the developmental stages ranging from 0.471 to 0.832.

A study by Chen et al, the CVM and dental calcification stages of the teeth except the third molars showed correlations ranging from 0.601 to 0.911. Krailassiri et al () and Uysal et al () have reported weak correlations, while Ëngstrom et al () found a strong correlation. In this Saudi sample there was a weak positive correlation between CVM stages and upper molar ranging from 0.166 to 0.0287, except for CS5 stage in which there was a moderate positive correlation. For lower third molar stages, there was a moderate positive correlation between cervical vertebra developmental stages CS4, CS5 and CS6, ranging from 0.471 to 0.832. It has been recommended by many researchers that the maturation of the mandibular canine is more strongly associated with the pubertal growth spurt than any other teeth () and some investigators have suggested that the second premolar has the highest correlation with skeletal maturation (). It has been concluded that the second molar has an advantage over other teeth because of its longer period of development until a later age (, , ).

Skeletal maturity increased together with the increase in dental ages for both genders. A constantly earlier occurrence for each skeletal maturation stage was observed in females. At some stage, in the peak growth period, these differences were more marked. All correlations between skeletal and dental stages were statistically significant. Further research using a larger sample of Saudi children is needed to come to more reliable conclusions.

Conclusions

Due to its practical applications, the CVM stage method appears to be a powerful diagnostic tool. The CVM stage method may be helpful for the assessment of period active growth for long term effects of orthodontic/orthopedic treatment approach. It can be used to identify the sufficient time for intervention for the late correction of facial deformities. Tooth calcification stage was significantly correlated with CVM stage in a study of Saudi sample. When planning the orthodontic treatment, it is useful to consider both dental and skeletal maturity.