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Bone age estimation by cervical vertebral dimensions in lateral cephalometry
progress in orthodontics 1 3 ( 2 0 1 2 ) 126–131
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Original article
Bone age estimation by cervical vertebral dimensions in lateral cephalometry Masoud Varshosaz a , Sara Ehsani b,∗ , Mahtab Nouri c , Mohammad A. Tavakoli d a
Dentomaxillofacial Radiologist, Assistant professor, Dentomaxillofacial Radiology Department, Dental school, Shaheed Beheshti University, M.C. Evin, Tehran, Iran b Dentomaxillofacial Radiologist, Researcher, Iran Center for Dental Research, Shaheed Beheshti University, M.C. Evin, Tehran, Iran c Associate Professor, Orthodontic Department, Shaheed Beheshti University, M.C. Evin, Tehran, Iran d Professor, Dentomaxillofacial Radiology Department, Shaheed Beheshti University, M.C. Evin, Tehran, Iran
a r t i c l e
i n f o
a b s t r a c t
Article history:
Objectives: A critical issue in contemporary orthodontics is bone age estimation. The most
Received 18 May 2011
reliable method for skeletal age evaluation is hand–wrist radiography; but it requires further
Accepted 12 September 2011
radiation. There is an increasing attention for evaluating cervical vertebrae to reduce the radiation to the patients. The aim of this study was to estimate bone age by measuring 3rd
Keywords:
and 4th cervical vertebrae (C3, C4) dimensions.
Bone age Measurement
Materials and methods: We conducted a correlational study on 91 Iranian individuals aged
Cervical vertebrae
8-18 years. After taking lateral cephalometry and hand-wrist radiographs, C3 and C4 were
Radiography
measured using Vixwin 2000 software. Hand-wrist bone age, determined on Greulich Atlas, was the reference test. Stepwise multiple linear regression model demonstrated the correlation between the two measurements. Results: Anterior height of the fourth cervical vertebrae (AH4) had the strongest simple correlation with hand-wrist bone age (r = 0.831, P<0.001) and was the only variable that remained in stepwise multivariate regression model. The regression model was: Bone age = 0.989 × AH4 + 3.308. Adjusted R2 was 0.686 (p<0.001). Conclusions: Lateral cephalometric radiographs are useful for bone age estimation, and might be an alternative for hand-wrist radiography, with the advantage of radiation reduction. © 2011 Società Italiana di Ortodonzia SIDO. Published by Elsevier Srl. All rights reserved.
Introduction Evaluation of skeletal maturation is of paramount importance in orthodontic treatment planning and the eventual outcome in most cases.1 Given that facial growth does not follow a steady course,2,3 proper timing of the treatment onset plays a critical role in determining the final results of orthodontic
procedures, since it contributes to the correction of skeletal discrepancies.4 Furthermore, the assessment of skeletal maturity allows for evaluation, follow up, and timing of therapy in young patients with growth disorders or endocrinological diseases.5 The therapeutic effect of a considerable number of appliances is most favorable when these appliances are used during the individual pubertal growth spurt.3
∗ Corresponding author. Dentomaxillofacial Radiologist, Iran Center for Dental Research, Shaheed Beheshti University, M.C. Evin, Tehran, Iran. E-mail address: [email protected] (S. Ehsani). 1723-7785/$ – see front matter © 2011 Società Italiana di Ortodonzia SIDO. Published by Elsevier Srl. All rights reserved. doi:10.1016/j.pio.2011.09.003
progress in orthodontics 1 3 ( 2 0 1 2 ) 126–131
Consequently, various maturity indicators were brought into play to assess skeletal maturation. Many researchers have used parameters such as chronological age, secondary sexual characteristics, body weight and height, menarche or voice changes, dental development, skeletal development and vertebral development, to determine a reliable indicator for maturity and/or growth potential.4,6–10 Hand-wrist radiographs have been used routinely to assess individual skeletal age9,11 though there are concerns about the extra radiation required and the routine use of hand radiographs has been questioned from the radiation safety point of view. The British Orthodontic Society guidelines states that there are no orthodontic indications for the hand and wrist radiographs to predict the onset of the pubertal growth spurt.12 Lateral cephalometric radiographs, which are one of the routine records in orthodontics, include cervical vertebrae and many researchers have shown the morphologic changes in cervical vertebral bodies during growth.6,10,13 In 1972, Lamparski published an atlas to show changes in cervical vertebral bodies for evaluating skeletal maturations.10 Some investigations reported a high correlation between cervical vertebral maturation, using the Atlas and skeletal maturation of hand-wrist; the coefficient of correlation varied from 0.45 to 0.97.14 The shortcoming of this method is its subjective nature. In 1991, Hellsing found that there is significant correlation between dimensions of the cervical vertebral bodies and statural height during adulthood.15 In 1995, Hassel and Farman suggested six stages for cervical vertebral maturation and found a high correlation between cervical vertebral and hand-wrist maturation;6 but stage differentiation is difficult because it is a subjective method, and quantitative evaluation of growth is not possible. Cattel,16 Ogden,17 and Bailey18 reported several normal variations in cervical vertebral bodies which may cause further limitations in using qualitative methods. Mito et al. used cervical vertebral dimensions to predict bone age. The cases, however, were Japanese and the resultant model required several measurements.19 The purpose of this study was to estimate bone age, measuring dimensions of the cervical vertebral bodies, on Lateral cephalometric radiographs and to investigate its correlation with hand-wrist bone age in an Iranian sample.
Materials and methods In this study, we evaluated 91 individuals admitted in the Orthodontics Department in Shaheed Beheshti University M.C. (after their parents signed a consent letter). The cases were 8- to 18-years –old (chronological age). Cases with the history of hormone therapy, previous orthodontic treatment, head and neck trauma, and systemic diseases with effect on growth were excluded from the study. We took all lateral cephalometric and hand-wrist radiographs by Proline Planmeca (PM 2002 CC, Helsinki, Finland), 18×24 caliber and Kodak, green 400, screen regular films, scanned them with 300 dpi resolution (Microtek, 9600XL), and analyzed them by Wixwin 2000 software (Gendex, Desplaines, IL). We measured six dimensions (mm) for each case: anterior height of the third and fourth cervical vertebrae (AH3
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Fig. 1 – Dimensions of the vertebral bodies, measured on a lateral cephalometric radiograph: anterior height of the third and fourth cervical vertebrae (AH3 and AH4), posterior height of the third and fourth cervical vertebrae (PH3 and PH4) and antero-posterior length of the third and fourth cervical vertebrae (A-P3 and A-P4).
and AH4), posterior height of the third and fourth cervical vertebrae (PH3 and PH4) and antero-posterior length of the third and fourth cervical vertebrae (A-P3 and A-P4) (Fig. 1). To eliminate the magnification of radiographs, we used Wixwin 2000 software, which has an internal scale for calibration. We estimated bone age according to the Greulich & Pyle’s “Radiographic Atlas of Skeletal Development of Hand and Wrist”.9 All radiographs were assessed by a maxillofacial radiologist. Another maxillofacial radiologist considered numerical codes for all radiographs, which remained unknown to the operator. Then, the operator was always blind to the results of the other test.
Intra-observer reliability To evaluate the intra-observer reliability, we randomly selected 20 cephalometric radiographs and measured all six parameters three times (baseline, after 2 and 4 weeks). Intraclass correlation coefficients (ICC) were calculated. In all cases, p value was less than 0.001.
Statistical analysis Statistical analysis was performed with SPSS14 software (SPSS, Chicago). All data series had normal distribution, as shown by one-sample Kolmogorov- Smirnov test. The prediction model was assessed by means of multiple linear
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progress in orthodontics 1 3 ( 2 0 1 2 ) 126–131
Table 1 – The statistics of each variable.
Mean Std. Deviation Minimum Maximum ∗ † ‡
§ || ¶
Bone age
AH3*
PH3†
A-P3‡
AH4§
PH4||
A-P4¶
12.437 3.1518 4.5 18.0
9.751 2.8656 4.8 15.1
11.029 2.4094 6.7 15.8
12.491 1.2949 9.7 16.1
9.210 2.6215 5.3 14.3
11.199 2.2570 6.1 15.6
12.584 1.2816 9.9 15.6
Anterior height of the third cervical vertebrae. Posterior height of the third cervical vertebrae. Antero-posterior length of the third cervical vertebrae. Anterior height of the forth cervical vertebrae. Posterior height of the forth cervical vertebrae. Antero-posterior length of the forth cervical vertebrae.
Table 2 – Pearson’s correlation coefficients of each variable with bone age.
Pearson’s r ∗ † ‡
§ || ¶
AH3*
PH3†
A-P3‡
AH4§
PH4||
A-P4¶
0.782
0.778
0.405
0.831
0.787
0.444
Anterior height of the third cervical vertebrae. Posterior height of the third cervical vertebrae. Antero-posterior length of the third cervical vertebrae. Anterior height of the forth cervical vertebrae. Posterior height of the forth cervical vertebrae. Antero-posterior length of the forth cervical vertebrae.
regression (stepwise method). Type I error (␣) was set at 0.05 and p value less than ␣ was statistically significant.
Results Minimum and maximum of the Intra-class correlation coefficients (ICC) were 0.909 (in cases of AP4) and 0.989 (in cases of PH3). The subjects included 41 male and 50 female cases (45.1% and 54.9%, respectively). The mean bone age was 12.4 years (SD= 3.15). Each case underwent both tests in the same day. We used stepwise multiple regression analysis to assess the correlation between each cervical vertebral dimension, and bone age. The results indicated that among these variables, the “AH4” is so prominent that including other predictors does not improve the prediction model. Analysis of variance revealed the significance of regression (p<0.001). The highest correlation coefficient was observed between AH4 and the estimated bone age from Greulich’s Atlas (r=0.831, p<0.001). Standard error for the coefficient of AH4 was 0.071. The linear model achieved was as follows: Bone age = 0.989 × AH4 + 3.308. Adjusted R2 was 0.686 (p<0.001). Sex was not a significant variable in predicting bone age (p>0.05). The statistics of variables are given in Table 1. Table 2 demonstrates the Pearson’s correlation coefficients of the variables with bone age.
Discussion Assessment of skeletal maturation in the individual patient provides the orthodontists with essential information for orthodontic treatment planning and anticipation of the possible outcomes of dentofacial orthopedics.2 Evidence shows
that the greatest effects of functional appliances occur around the peak in mandibular growth.3 An assessment of skeletal age must be based on structures within the skeletal system.11 The most common method for this purpose is hand-wrist radiography.11 However, as mentioned before, hand-wrist radiography requires an additional exposure to radiation. Since the early 70s, when Lamparski suggested the cervical vertebrae as indicators of individual skeletal maturation, many investigators have tried to substitute the vertebrae for the hand-wrist analysis. The increasing interest in monitoring the cervical vertebrae as indicators of individual skeletal maturation in orthodontic subjects is a result of the fact that the analyses may be performed on the lateral cephalometric radiograph which is of routinely use in orthodontic diagnosis and it does not require further radiation. The relationship between the maturation of hand wrist and cervical vertebrae is well established. Researchers have also demonstrated its effectiveness in determining the maturational status required in orthodontics. In 2000, Franchi et al. analyzed the validity of a modification of the method suggested by Lamparski as a biologic indicator for skeletal maturity. They studied annual cephalograms and dental casts of 24 orthodontically untreated children (3- to 18-years-old) and measured mandibular size and mandibular position in relation to other craniofacial structures. They found that 100% of boys and 87% of girls presented with the peak in statural height at growth interval Cvs3 to Cvs4. The greatest increment for all examined cephalometric variables took place at the same interval.2 Baccetti et al. conducted a study to define the optimal timing for Twin-block therapy. They evaluated changes induced by the Twin-block appliance in two groups of subjects treated at different skeletal maturation stages, based on their cervical vertebrae maturation according to the evaluation method by Lamparski.3
progress in orthodontics 1 3 ( 2 0 1 2 ) 126–131
In the past few decades, different methods for assessment of cervical vertebrae in lateral cephalometric radiograph have been introduced.11 Hassel and Farman in 1995,6 and Baccetti et al. in 200213 introduced methods that were investigated in several studies. In 2005, Baccetti et al. introduced a modified version of the Cervical Vertebral Maturation (CVM) method,4 which is now considered as the most widely accepted method.20 Nevertheless, these methods are qualitative. Therefore, their subjective nature as well as the normal variations may cause some limitations. In 2002, Mito et al. tried to establish a new objective index for evaluating skeletal maturation on cephalometric radiographs. They evaluated maturity in a detailed and objective manner in Japanese girls.19 In an attempt to investigate their method in an Iranian sample, we used a quantitative method, as what Mito et al had done in Japan. Since it has been reported that comparison of an individual’s status with standards from other racial groups may overestimate or underestimate a patient’s degree of maturation,5 the present study was carried out to estimate bone age with the help of dimensions of the cervical vertebrae, and to investigate the correlation between the bone age assessed by this method and hand-wrist bone age among Iranian individuals. We evaluated the third and fourth cervical vertebrae. These two vertebrae are visible in lateral cephalometric radiographs despite using thyroid-protecting collar. The body of the first cervical vertebra is not usually seen; and the second cervical vertebra shows a limited morphological change. The fifth vertebra may appear incomplete or unclear. We used Greulich & Pyle’s Atlas, because it is the bestestablished method used on an international scale,21 and according to previous studies, it is simpler and less time consuming than other methods, and is more reliable.21–24 We evaluated individuals 8-years-old and above, because orthodontists believe that growth modification treatments should begin before completion of adolescent growth spurt and supposedly, the treatment can be done at any time before that point.20 On the other hand, Hellsing showed that there are some differences between 15-years-old boys and “adult” boys, concerning body height and cervical vertebral dimensions.15 So; we chose 18 years as the highest border of the study population. In the study reported by Hassel and Farman, the age range was 8-18 years.6 Gandini et al. studied samples with 7–18 years of age,25 Roman et al. selected the age range of 5 to 18 years,26 and in a study by Uysal et al. the age range was 5 to 24.7 Because of the limited sample size, we evaluated all individuals in a single age group. Nevertheless, we know that, as Franchi et al. demonstrated in their study,2 human growth and development shows some accelerations and decelerations and is not necessarily uniform. Therefore, the wide age range of the subjects might affect the result and lower the correlation. It has been reported that the sensitivity of the CVM method4 away from the circumpubertal period is low. Investigations correlating the hand wrist and the cervical vertebrae maturation resulted in lower correlation coefficients when studied a wider age range.27,28
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We used the stepwise regression analysis for this study. This method, selects the variable with highest correlation with the dependent variable, and then considers the next variable if it significantly increases R2 . In this study, the correlation coefficients between dimensions of the third and fourth cervical vertebral bodies and bone age were statistically significant (in all cases p<0.001), but the coefficients were less than 0.5 in cases of antero-posterior lengths of the both vertebrae (A-P3 and A-P4). The anterior and posterior heights of the bodies had stronger correlations with bone age (r>0.75). Anterior height of the fourth vertebra had the highest simple correlation coefficient with bone age (r=0.831) and was the only variable that remained in stepwise multivariate regression model. By this model we could predict the bone age from anterior height of the fourth vertebra with an acceptable precision (adjusted R2 =0.595, while R2 value is considered high between 0.30 and 0.67).29 The differences in results compared to the study reported by Mito et al. may be ascribed to the different characteristics of the study samples. They studied 8- to 14-years-old girls in Japan.19 It should be kept in mind that most of bones are initially cartilaginous and their ossification is endochondral.30 However, facial bones’ ossification is intramembranous. Thus, it can be concluded that the facial growth may be regulated by factors other than the general growth.31 On the other hand, in the method we used, qualitative changes and shape of the bones may be neglected. In addition, we did not measure the growth potential which needs longitudinal studies. We also recommend that further investigations study the patients in different age groups to eliminate the effect of age on these results.
Conclusions Lateral cephalometric radiographs are useful for bone age estimation, and might be an alternative for hand-wrist radiography. By replacing the hand-wrist method with analysis of cervical vertebrae, an additional radiograph can be avoided. In addition, it might be possible to evaluate maturity in an objective manner with the help of dimensions of cervical vertebrae.
Conflict of interest The authors have no conflicts of interest.
Riassunto Obiettivi: Una problematica cruciale nella terapia ortodontica è la stima dell’età ossea. Il metodo più affidabile per la valutazione dell’età scheletrica è la radiografia della mano e del polso, ma richiede una ulteriore esposizione alle radiazioni. La valutazione delle vertebre cervicali è ogetto di una crescente attenzione come metodica per ridurre l’esposizione dei pazienti alle radiazioni. Lo scopo del presente studio è quello di stimare l’età ossea misurando le dimensioni delle terza e quarta vertebra cervicale (C3, C4). Materiali e metodi: È stato condotto uno studio di correlazione su 91 soggetti iraniani di età compresa tra gli 8 e i 18 anni. Dopo aver eseguito la teleradiografia latero-laterale con le misurazioni cefalometriche e la radiografia della mano e del polso sono state misurale la
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progress in orthodontics 1 3 ( 2 0 1 2 ) 126–131
C3 e la C4 utilizzando il software Vixwin 2000. L’atlante di Greulich è stato utilizzato come riferimento per il confronto con l’età ossea della mano e del polso. Applicando ai risultati il modello di regressione lineare multipla stepwise è stata dimostrata la correlazione tra le due misurazioni. Risultati: L’altezza anteriore della quarta vertebra cervicale (AH4) mostra la correlazione semplice più marcata con l’età ossea di mano e polso (r = 0.831, P<0.001) ed è l’unica variabile presente nel modello di regressione multivariata stepwise. Il modello di regressione è il seguente: Età ossea = 0.989 x AH4 + 3.308. Con rettifica R2 è pari a 0.686. Conclusioni: La radiografia latero-laterale con cefalometria è un valido strumento per una stima dell’età ossea e può costituire un’alternativa alla radiografia della mano e del polso con il vantaggio di una riduzione dell’esposizione alle radiazioni.
atlas de Greulich fue utilizado como prueba de referencia para la ˜ comparación con la edad ósea de mano-muneca. El modelo de regresión lineal múltiple paso a paso destacó la correlación entre las dos mediciones. Resultados: La altura anterior de la cuarta vértebra cervical (AH4) experimenta la correlación sencilla más marcada con la edad ósea de ˜ mano-muneca (r = 0.831, P<0.001) y es la única variable presente en el modelo de regresión multivariada paso a paso. El modelo de regresión ha sido el siguiente: Edad ósea = 0.989 x AH4 + 3.308. Cuando ajustado, R2 es igual a 0.686. Conclusiones: La radiografía cefalométrica lateral es una herramienta útil para determinar la edad ósea, y puede ser una ˜ alternativa a la radiografía mano-muneca, con la ventaja de reducir las radiaciones.
Résumé Objectifs: Une problématique cruciale dans la thérapie orthodontique est l’estimation de l’âge osseux. La méthode la plus fiable pour évaluer l’âge squelettique est la radiographie de la main et du poignet, mais cela demande une exposition supplémentaire aux radiations. L’évaluation des vertèbres cervicales fait l’objet d’une attention croissante comme méthode pour réduire l’exposition des patients aux radiations. Le but de la présente étude est de déterminer l’âge osseux en mesurant les dimensions de la troisième et de la quatrième vertèbre cervicale (C3, C4). Matériels et méthodes: Une étude de corrélation a été menée chez 91 sujets iraniens dont l’âge allait de 8 à 18 ans. Après avoir effectué la céphalométrie latérale et la radiographie de la main et du poignet, les vertèbres C3 et C4 ont été mesurées en utilisant le logiciel d’imagerie Vixwin 2000. L’atlas de Greulich a été choisi comme point de repère pour comparer l’âge osseux de la main et du poignet. L’application du modèle de régression linéaire pas à pas a bien montré la corrélation entre les deux mesures. Résultats: La hauteur antérieure de la quatrième vertèbre cervicale (AH4) fait état d’une corrélation de plus en plus marquée avec l’âge osseux de la main et du poignet (r = 0.831, P<0.001) et c’est la seule variable présente dans le modèle de régression multivariée pas à pas. Le modèle de régression est le suivant: Age osseux = 0.989 x AH4 + 3.308. Avec rectification R2 est égal à 0.686. Conclusions: La radiographie céphalométrique latérale est un outil valable pour une détermination de l’âge osseux et peut constituer une alternative à la radiographie de la main et du poignet, cela ayant l’avantage d’obtenir une réduction de l’exposition aux radiations.
Resumen Objetivos: Un aspecto trascendente y crítico en el tratamiento ortodóntico es la estimación de la edad ósea. El método más fiable ˜ para medir la edad esquelética es la radiografía de mano-muneca, pero lo anterior requiere una exposición adicional a radiaciones. La determinación de las vértebras cervicales es objeto de una atención creciente para reducir las radiaciones en los pacientes. El objetivo de ˜ de la este estudio es determinar la edad ósea midiendo el tamano tercera y la cuarta vértebra cervical (C3, C4). Materiales y métodos: Se llevó a cabo un estudio correlacional en ˜ 91 sujetos iraníes cuya edad variaba de 8 a 18 anos. Después de la ˜ cefalometría lateral y la radiografía de mano-muneca, fueron medidas las vértebras C3 y C4, utilizando el software Vixwin 2000. El
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journal homepage: www.elsevier.com/locate/pio
Original article
Bone age estimation by cervical vertebral dimensions in lateral cephalometry Masoud Varshosaz a , Sara Ehsani b,∗ , Mahtab Nouri c , Mohammad A. Tavakoli d a
Dentomaxillofacial Radiologist, Assistant professor, Dentomaxillofacial Radiology Department, Dental school, Shaheed Beheshti University, M.C. Evin, Tehran, Iran b Dentomaxillofacial Radiologist, Researcher, Iran Center for Dental Research, Shaheed Beheshti University, M.C. Evin, Tehran, Iran c Associate Professor, Orthodontic Department, Shaheed Beheshti University, M.C. Evin, Tehran, Iran d Professor, Dentomaxillofacial Radiology Department, Shaheed Beheshti University, M.C. Evin, Tehran, Iran
a r t i c l e
i n f o
a b s t r a c t
Article history:
Objectives: A critical issue in contemporary orthodontics is bone age estimation. The most
Received 18 May 2011
reliable method for skeletal age evaluation is hand–wrist radiography; but it requires further
Accepted 12 September 2011
radiation. There is an increasing attention for evaluating cervical vertebrae to reduce the radiation to the patients. The aim of this study was to estimate bone age by measuring 3rd
Keywords:
and 4th cervical vertebrae (C3, C4) dimensions.
Bone age Measurement
Materials and methods: We conducted a correlational study on 91 Iranian individuals aged
Cervical vertebrae
8-18 years. After taking lateral cephalometry and hand-wrist radiographs, C3 and C4 were
Radiography
measured using Vixwin 2000 software. Hand-wrist bone age, determined on Greulich Atlas, was the reference test. Stepwise multiple linear regression model demonstrated the correlation between the two measurements. Results: Anterior height of the fourth cervical vertebrae (AH4) had the strongest simple correlation with hand-wrist bone age (r = 0.831, P<0.001) and was the only variable that remained in stepwise multivariate regression model. The regression model was: Bone age = 0.989 × AH4 + 3.308. Adjusted R2 was 0.686 (p<0.001). Conclusions: Lateral cephalometric radiographs are useful for bone age estimation, and might be an alternative for hand-wrist radiography, with the advantage of radiation reduction. © 2011 Società Italiana di Ortodonzia SIDO. Published by Elsevier Srl. All rights reserved.
Introduction Evaluation of skeletal maturation is of paramount importance in orthodontic treatment planning and the eventual outcome in most cases.1 Given that facial growth does not follow a steady course,2,3 proper timing of the treatment onset plays a critical role in determining the final results of orthodontic
procedures, since it contributes to the correction of skeletal discrepancies.4 Furthermore, the assessment of skeletal maturity allows for evaluation, follow up, and timing of therapy in young patients with growth disorders or endocrinological diseases.5 The therapeutic effect of a considerable number of appliances is most favorable when these appliances are used during the individual pubertal growth spurt.3
∗ Corresponding author. Dentomaxillofacial Radiologist, Iran Center for Dental Research, Shaheed Beheshti University, M.C. Evin, Tehran, Iran. E-mail address: [email protected] (S. Ehsani). 1723-7785/$ – see front matter © 2011 Società Italiana di Ortodonzia SIDO. Published by Elsevier Srl. All rights reserved. doi:10.1016/j.pio.2011.09.003
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Consequently, various maturity indicators were brought into play to assess skeletal maturation. Many researchers have used parameters such as chronological age, secondary sexual characteristics, body weight and height, menarche or voice changes, dental development, skeletal development and vertebral development, to determine a reliable indicator for maturity and/or growth potential.4,6–10 Hand-wrist radiographs have been used routinely to assess individual skeletal age9,11 though there are concerns about the extra radiation required and the routine use of hand radiographs has been questioned from the radiation safety point of view. The British Orthodontic Society guidelines states that there are no orthodontic indications for the hand and wrist radiographs to predict the onset of the pubertal growth spurt.12 Lateral cephalometric radiographs, which are one of the routine records in orthodontics, include cervical vertebrae and many researchers have shown the morphologic changes in cervical vertebral bodies during growth.6,10,13 In 1972, Lamparski published an atlas to show changes in cervical vertebral bodies for evaluating skeletal maturations.10 Some investigations reported a high correlation between cervical vertebral maturation, using the Atlas and skeletal maturation of hand-wrist; the coefficient of correlation varied from 0.45 to 0.97.14 The shortcoming of this method is its subjective nature. In 1991, Hellsing found that there is significant correlation between dimensions of the cervical vertebral bodies and statural height during adulthood.15 In 1995, Hassel and Farman suggested six stages for cervical vertebral maturation and found a high correlation between cervical vertebral and hand-wrist maturation;6 but stage differentiation is difficult because it is a subjective method, and quantitative evaluation of growth is not possible. Cattel,16 Ogden,17 and Bailey18 reported several normal variations in cervical vertebral bodies which may cause further limitations in using qualitative methods. Mito et al. used cervical vertebral dimensions to predict bone age. The cases, however, were Japanese and the resultant model required several measurements.19 The purpose of this study was to estimate bone age, measuring dimensions of the cervical vertebral bodies, on Lateral cephalometric radiographs and to investigate its correlation with hand-wrist bone age in an Iranian sample.
Materials and methods In this study, we evaluated 91 individuals admitted in the Orthodontics Department in Shaheed Beheshti University M.C. (after their parents signed a consent letter). The cases were 8- to 18-years –old (chronological age). Cases with the history of hormone therapy, previous orthodontic treatment, head and neck trauma, and systemic diseases with effect on growth were excluded from the study. We took all lateral cephalometric and hand-wrist radiographs by Proline Planmeca (PM 2002 CC, Helsinki, Finland), 18×24 caliber and Kodak, green 400, screen regular films, scanned them with 300 dpi resolution (Microtek, 9600XL), and analyzed them by Wixwin 2000 software (Gendex, Desplaines, IL). We measured six dimensions (mm) for each case: anterior height of the third and fourth cervical vertebrae (AH3
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Fig. 1 – Dimensions of the vertebral bodies, measured on a lateral cephalometric radiograph: anterior height of the third and fourth cervical vertebrae (AH3 and AH4), posterior height of the third and fourth cervical vertebrae (PH3 and PH4) and antero-posterior length of the third and fourth cervical vertebrae (A-P3 and A-P4).
and AH4), posterior height of the third and fourth cervical vertebrae (PH3 and PH4) and antero-posterior length of the third and fourth cervical vertebrae (A-P3 and A-P4) (Fig. 1). To eliminate the magnification of radiographs, we used Wixwin 2000 software, which has an internal scale for calibration. We estimated bone age according to the Greulich & Pyle’s “Radiographic Atlas of Skeletal Development of Hand and Wrist”.9 All radiographs were assessed by a maxillofacial radiologist. Another maxillofacial radiologist considered numerical codes for all radiographs, which remained unknown to the operator. Then, the operator was always blind to the results of the other test.
Intra-observer reliability To evaluate the intra-observer reliability, we randomly selected 20 cephalometric radiographs and measured all six parameters three times (baseline, after 2 and 4 weeks). Intraclass correlation coefficients (ICC) were calculated. In all cases, p value was less than 0.001.
Statistical analysis Statistical analysis was performed with SPSS14 software (SPSS, Chicago). All data series had normal distribution, as shown by one-sample Kolmogorov- Smirnov test. The prediction model was assessed by means of multiple linear
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Table 1 – The statistics of each variable.
Mean Std. Deviation Minimum Maximum ∗ † ‡
§ || ¶
Bone age
AH3*
PH3†
A-P3‡
AH4§
PH4||
A-P4¶
12.437 3.1518 4.5 18.0
9.751 2.8656 4.8 15.1
11.029 2.4094 6.7 15.8
12.491 1.2949 9.7 16.1
9.210 2.6215 5.3 14.3
11.199 2.2570 6.1 15.6
12.584 1.2816 9.9 15.6
Anterior height of the third cervical vertebrae. Posterior height of the third cervical vertebrae. Antero-posterior length of the third cervical vertebrae. Anterior height of the forth cervical vertebrae. Posterior height of the forth cervical vertebrae. Antero-posterior length of the forth cervical vertebrae.
Table 2 – Pearson’s correlation coefficients of each variable with bone age.
Pearson’s r ∗ † ‡
§ || ¶
AH3*
PH3†
A-P3‡
AH4§
PH4||
A-P4¶
0.782
0.778
0.405
0.831
0.787
0.444
Anterior height of the third cervical vertebrae. Posterior height of the third cervical vertebrae. Antero-posterior length of the third cervical vertebrae. Anterior height of the forth cervical vertebrae. Posterior height of the forth cervical vertebrae. Antero-posterior length of the forth cervical vertebrae.
regression (stepwise method). Type I error (␣) was set at 0.05 and p value less than ␣ was statistically significant.
Results Minimum and maximum of the Intra-class correlation coefficients (ICC) were 0.909 (in cases of AP4) and 0.989 (in cases of PH3). The subjects included 41 male and 50 female cases (45.1% and 54.9%, respectively). The mean bone age was 12.4 years (SD= 3.15). Each case underwent both tests in the same day. We used stepwise multiple regression analysis to assess the correlation between each cervical vertebral dimension, and bone age. The results indicated that among these variables, the “AH4” is so prominent that including other predictors does not improve the prediction model. Analysis of variance revealed the significance of regression (p<0.001). The highest correlation coefficient was observed between AH4 and the estimated bone age from Greulich’s Atlas (r=0.831, p<0.001). Standard error for the coefficient of AH4 was 0.071. The linear model achieved was as follows: Bone age = 0.989 × AH4 + 3.308. Adjusted R2 was 0.686 (p<0.001). Sex was not a significant variable in predicting bone age (p>0.05). The statistics of variables are given in Table 1. Table 2 demonstrates the Pearson’s correlation coefficients of the variables with bone age.
Discussion Assessment of skeletal maturation in the individual patient provides the orthodontists with essential information for orthodontic treatment planning and anticipation of the possible outcomes of dentofacial orthopedics.2 Evidence shows
that the greatest effects of functional appliances occur around the peak in mandibular growth.3 An assessment of skeletal age must be based on structures within the skeletal system.11 The most common method for this purpose is hand-wrist radiography.11 However, as mentioned before, hand-wrist radiography requires an additional exposure to radiation. Since the early 70s, when Lamparski suggested the cervical vertebrae as indicators of individual skeletal maturation, many investigators have tried to substitute the vertebrae for the hand-wrist analysis. The increasing interest in monitoring the cervical vertebrae as indicators of individual skeletal maturation in orthodontic subjects is a result of the fact that the analyses may be performed on the lateral cephalometric radiograph which is of routinely use in orthodontic diagnosis and it does not require further radiation. The relationship between the maturation of hand wrist and cervical vertebrae is well established. Researchers have also demonstrated its effectiveness in determining the maturational status required in orthodontics. In 2000, Franchi et al. analyzed the validity of a modification of the method suggested by Lamparski as a biologic indicator for skeletal maturity. They studied annual cephalograms and dental casts of 24 orthodontically untreated children (3- to 18-years-old) and measured mandibular size and mandibular position in relation to other craniofacial structures. They found that 100% of boys and 87% of girls presented with the peak in statural height at growth interval Cvs3 to Cvs4. The greatest increment for all examined cephalometric variables took place at the same interval.2 Baccetti et al. conducted a study to define the optimal timing for Twin-block therapy. They evaluated changes induced by the Twin-block appliance in two groups of subjects treated at different skeletal maturation stages, based on their cervical vertebrae maturation according to the evaluation method by Lamparski.3
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In the past few decades, different methods for assessment of cervical vertebrae in lateral cephalometric radiograph have been introduced.11 Hassel and Farman in 1995,6 and Baccetti et al. in 200213 introduced methods that were investigated in several studies. In 2005, Baccetti et al. introduced a modified version of the Cervical Vertebral Maturation (CVM) method,4 which is now considered as the most widely accepted method.20 Nevertheless, these methods are qualitative. Therefore, their subjective nature as well as the normal variations may cause some limitations. In 2002, Mito et al. tried to establish a new objective index for evaluating skeletal maturation on cephalometric radiographs. They evaluated maturity in a detailed and objective manner in Japanese girls.19 In an attempt to investigate their method in an Iranian sample, we used a quantitative method, as what Mito et al had done in Japan. Since it has been reported that comparison of an individual’s status with standards from other racial groups may overestimate or underestimate a patient’s degree of maturation,5 the present study was carried out to estimate bone age with the help of dimensions of the cervical vertebrae, and to investigate the correlation between the bone age assessed by this method and hand-wrist bone age among Iranian individuals. We evaluated the third and fourth cervical vertebrae. These two vertebrae are visible in lateral cephalometric radiographs despite using thyroid-protecting collar. The body of the first cervical vertebra is not usually seen; and the second cervical vertebra shows a limited morphological change. The fifth vertebra may appear incomplete or unclear. We used Greulich & Pyle’s Atlas, because it is the bestestablished method used on an international scale,21 and according to previous studies, it is simpler and less time consuming than other methods, and is more reliable.21–24 We evaluated individuals 8-years-old and above, because orthodontists believe that growth modification treatments should begin before completion of adolescent growth spurt and supposedly, the treatment can be done at any time before that point.20 On the other hand, Hellsing showed that there are some differences between 15-years-old boys and “adult” boys, concerning body height and cervical vertebral dimensions.15 So; we chose 18 years as the highest border of the study population. In the study reported by Hassel and Farman, the age range was 8-18 years.6 Gandini et al. studied samples with 7–18 years of age,25 Roman et al. selected the age range of 5 to 18 years,26 and in a study by Uysal et al. the age range was 5 to 24.7 Because of the limited sample size, we evaluated all individuals in a single age group. Nevertheless, we know that, as Franchi et al. demonstrated in their study,2 human growth and development shows some accelerations and decelerations and is not necessarily uniform. Therefore, the wide age range of the subjects might affect the result and lower the correlation. It has been reported that the sensitivity of the CVM method4 away from the circumpubertal period is low. Investigations correlating the hand wrist and the cervical vertebrae maturation resulted in lower correlation coefficients when studied a wider age range.27,28
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We used the stepwise regression analysis for this study. This method, selects the variable with highest correlation with the dependent variable, and then considers the next variable if it significantly increases R2 . In this study, the correlation coefficients between dimensions of the third and fourth cervical vertebral bodies and bone age were statistically significant (in all cases p<0.001), but the coefficients were less than 0.5 in cases of antero-posterior lengths of the both vertebrae (A-P3 and A-P4). The anterior and posterior heights of the bodies had stronger correlations with bone age (r>0.75). Anterior height of the fourth vertebra had the highest simple correlation coefficient with bone age (r=0.831) and was the only variable that remained in stepwise multivariate regression model. By this model we could predict the bone age from anterior height of the fourth vertebra with an acceptable precision (adjusted R2 =0.595, while R2 value is considered high between 0.30 and 0.67).29 The differences in results compared to the study reported by Mito et al. may be ascribed to the different characteristics of the study samples. They studied 8- to 14-years-old girls in Japan.19 It should be kept in mind that most of bones are initially cartilaginous and their ossification is endochondral.30 However, facial bones’ ossification is intramembranous. Thus, it can be concluded that the facial growth may be regulated by factors other than the general growth.31 On the other hand, in the method we used, qualitative changes and shape of the bones may be neglected. In addition, we did not measure the growth potential which needs longitudinal studies. We also recommend that further investigations study the patients in different age groups to eliminate the effect of age on these results.
Conclusions Lateral cephalometric radiographs are useful for bone age estimation, and might be an alternative for hand-wrist radiography. By replacing the hand-wrist method with analysis of cervical vertebrae, an additional radiograph can be avoided. In addition, it might be possible to evaluate maturity in an objective manner with the help of dimensions of cervical vertebrae.
Conflict of interest The authors have no conflicts of interest.
Riassunto Obiettivi: Una problematica cruciale nella terapia ortodontica è la stima dell’età ossea. Il metodo più affidabile per la valutazione dell’età scheletrica è la radiografia della mano e del polso, ma richiede una ulteriore esposizione alle radiazioni. La valutazione delle vertebre cervicali è ogetto di una crescente attenzione come metodica per ridurre l’esposizione dei pazienti alle radiazioni. Lo scopo del presente studio è quello di stimare l’età ossea misurando le dimensioni delle terza e quarta vertebra cervicale (C3, C4). Materiali e metodi: È stato condotto uno studio di correlazione su 91 soggetti iraniani di età compresa tra gli 8 e i 18 anni. Dopo aver eseguito la teleradiografia latero-laterale con le misurazioni cefalometriche e la radiografia della mano e del polso sono state misurale la
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C3 e la C4 utilizzando il software Vixwin 2000. L’atlante di Greulich è stato utilizzato come riferimento per il confronto con l’età ossea della mano e del polso. Applicando ai risultati il modello di regressione lineare multipla stepwise è stata dimostrata la correlazione tra le due misurazioni. Risultati: L’altezza anteriore della quarta vertebra cervicale (AH4) mostra la correlazione semplice più marcata con l’età ossea di mano e polso (r = 0.831, P<0.001) ed è l’unica variabile presente nel modello di regressione multivariata stepwise. Il modello di regressione è il seguente: Età ossea = 0.989 x AH4 + 3.308. Con rettifica R2 è pari a 0.686. Conclusioni: La radiografia latero-laterale con cefalometria è un valido strumento per una stima dell’età ossea e può costituire un’alternativa alla radiografia della mano e del polso con il vantaggio di una riduzione dell’esposizione alle radiazioni.
atlas de Greulich fue utilizado como prueba de referencia para la ˜ comparación con la edad ósea de mano-muneca. El modelo de regresión lineal múltiple paso a paso destacó la correlación entre las dos mediciones. Resultados: La altura anterior de la cuarta vértebra cervical (AH4) experimenta la correlación sencilla más marcada con la edad ósea de ˜ mano-muneca (r = 0.831, P<0.001) y es la única variable presente en el modelo de regresión multivariada paso a paso. El modelo de regresión ha sido el siguiente: Edad ósea = 0.989 x AH4 + 3.308. Cuando ajustado, R2 es igual a 0.686. Conclusiones: La radiografía cefalométrica lateral es una herramienta útil para determinar la edad ósea, y puede ser una ˜ alternativa a la radiografía mano-muneca, con la ventaja de reducir las radiaciones.
Résumé Objectifs: Une problématique cruciale dans la thérapie orthodontique est l’estimation de l’âge osseux. La méthode la plus fiable pour évaluer l’âge squelettique est la radiographie de la main et du poignet, mais cela demande une exposition supplémentaire aux radiations. L’évaluation des vertèbres cervicales fait l’objet d’une attention croissante comme méthode pour réduire l’exposition des patients aux radiations. Le but de la présente étude est de déterminer l’âge osseux en mesurant les dimensions de la troisième et de la quatrième vertèbre cervicale (C3, C4). Matériels et méthodes: Une étude de corrélation a été menée chez 91 sujets iraniens dont l’âge allait de 8 à 18 ans. Après avoir effectué la céphalométrie latérale et la radiographie de la main et du poignet, les vertèbres C3 et C4 ont été mesurées en utilisant le logiciel d’imagerie Vixwin 2000. L’atlas de Greulich a été choisi comme point de repère pour comparer l’âge osseux de la main et du poignet. L’application du modèle de régression linéaire pas à pas a bien montré la corrélation entre les deux mesures. Résultats: La hauteur antérieure de la quatrième vertèbre cervicale (AH4) fait état d’une corrélation de plus en plus marquée avec l’âge osseux de la main et du poignet (r = 0.831, P<0.001) et c’est la seule variable présente dans le modèle de régression multivariée pas à pas. Le modèle de régression est le suivant: Age osseux = 0.989 x AH4 + 3.308. Avec rectification R2 est égal à 0.686. Conclusions: La radiographie céphalométrique latérale est un outil valable pour une détermination de l’âge osseux et peut constituer une alternative à la radiographie de la main et du poignet, cela ayant l’avantage d’obtenir une réduction de l’exposition aux radiations.
Resumen Objetivos: Un aspecto trascendente y crítico en el tratamiento ortodóntico es la estimación de la edad ósea. El método más fiable ˜ para medir la edad esquelética es la radiografía de mano-muneca, pero lo anterior requiere una exposición adicional a radiaciones. La determinación de las vértebras cervicales es objeto de una atención creciente para reducir las radiaciones en los pacientes. El objetivo de ˜ de la este estudio es determinar la edad ósea midiendo el tamano tercera y la cuarta vértebra cervical (C3, C4). Materiales y métodos: Se llevó a cabo un estudio correlacional en ˜ 91 sujetos iraníes cuya edad variaba de 8 a 18 anos. Después de la ˜ cefalometría lateral y la radiografía de mano-muneca, fueron medidas las vértebras C3 y C4, utilizando el software Vixwin 2000. El
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