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Reproducibility of skeletal and dental maturation parameters

Reprodutibilidade de parâmetros de maturação esqueléticos e dentários

ABSTRACT

Objective:

Amongst other factors, the effectiveness of orthodontic treatment in children and adolescents depends on the identification of most appropriate intervention timing, which has been traditionally based on the identification of maturational stages. There is a wide variety of radiographic methods to identify these phases, either through skeletal parameters, or dental calcification. Considering that the reliability of any given assessment tool is required to enable its safe clinical use, and aiming an appropriate implementation of these parameters in future researches, this study was performed to assess the reproducibility of radiographic growth evaluation methods.

Methods:

Lateral teleradiographs, hand-wrist, and panoramic radiographs of sixty-eight orthodontic patients randomly selected from files of the Orthodontics Graduation Course (Guarulhos University, Guarulhos, SP, Brazil) were evaluated by two examiners to access both intra- and inter-examiner reproducibility of the assessment methods conceived by Baccetti et al.; Fishman; Greulich and Pyle; Nolla and Demirjian et al.

Results:

All methods analyzed showed satisfactory intra- and inter-examiner reliability. Among those that evaluated skeletal maturity, a relatively better performance was observed for Baccetti’s method. Fishman’s and Greulich’s parameters presented similar rates, as did Nolla’s and Demirjian’s.

Conclusion:

The assessment tools analyzed presented adequate reproducibility and might potentially be used as assessment tools to evaluate children and adolescent’s craniofacial growth. Further researches could evaluate the accuracy of radiographic dental calcification parameters for the identification of craniofacial growth stages.

Indexing terms
Diagnostic imaging; Growth and development; Orthodontics; Reproducibility of results

RESUMO

Objetivo:

Entre outros fatores, a efetividade do tratamento ortodôntico em crianças e adolescentes depende da identificação do momento de intervenção mais apropriado, que tem sido baseado nos estágios de maturação. Uma variedade de métodos radiográficos identifica essas fases através de parâmetros esqueléticos e da calcificação dentária. Considerando que a confiabilidade de qualquer ferramenta de avaliação é necessária para permitir seu uso clínico e aplicação segura de seus parâmetros em pesquisas futuras, este estudo acessou a reprodutibilidade de métodos radiográficos de avaliação do crescimento.

Métodos:

Telerradiografias laterais, radiografias carpais e panorâmicas de 68 pacientes ortodônticos randomicamente selecionados dos arquivos do Curso de Graduação em Ortodontia (Universidade de Guarulhos, Guarulhos, SP, Brasil) foram avaliadas por dois examinadores para acessar a reprodutibilidade intra e inter-examinador dos métodos de avaliação concebidos por Baccetti et al.; Fishman; Greulich e Pyle; Nolla e Demirjian et al.

Resultados:

Todos os métodos analisados mostraram confiabilidade intra e inter-examinador satisfatória. Dentre os que avaliam maturidade esquelética, um desempenho relativamente melhor foi observado para o método de Baccetti e colaboradores. Os parâmetros de Fishman e de Greulich e Pyle apresentaram valores similares, assim como os de Nolla e de Demirjian e colaboradores.

Conclusão:

As ferramentas de avaliação analisadas apresentaram reprodutibilidade adequada e podem ser utilizadas para avaliação do crescimento craniofacial de crianças e adolescentes. Pesquisas futuras poderiam avaliar a acurácia dos parâmetros radiográficos de calcificação dentária para a identificação dos estágios de crescimento craniofacial.

Termos de indexação
Diagnóstico por imagem; Crescimento e desenvolvimento; Ortodontia; Reprodutibilidade de resultados

INTRODUCTION

The orthopedic/ orthodontic treatment of children and adolescents must consider, amongst other factors, the appropriate timing for the intervention of malocclusions [11 Sadowsky PL. Craniofacial growth and the timing of treatment. Am J Orthod Dentofacial Orthop. 1998;113(1):19-23. https://doi.org/10.1016/S0889-5406(98)70272-0
https://doi.org/10.1016/S0889-5406(98)70...
,22 Dadgar S, Hadian H, Ghobadi M, Sobouti F, Rakhshan V. Correlations among chronological age, cervical vertebral maturation index, and Demirjian developmental stage of the maxillary and mandibular canines and second molars. Surg Radiol Anat. 2021;43(1):131-143. https://doi.org/10.1007/s00276-020-02541-4
https://doi.org/10.1007/s00276-020-02541...
], which have been traditionally based on growth stages, as assessed by skeletal parameters [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.

4 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...

5 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
-66 Baccetti T, Franchi L, McNamara JA Jr. The cervical vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11(3):119-29. https://doi.org/10.1053/j.sodo.2005.04.005
https://doi.org/10.1053/j.sodo.2005.04.0...
]. Alternatively, dental calcification categorization systems have also been explored as a proxy tool to guide the orthodontic intervention, due to its prompt accessibility [77 Chen J, Hu H, Guo J, Liu Z, Liu R, Li F, et al. Correlation between dental maturity and cervical vertebral maturity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;110(6):777-83. https://doi.org/10.1016/j.tripleo.2010.08.006
https://doi.org/10.1016/j.tripleo.2010.0...

8 Valizadeh S, Eil N, Ehsani S, Bakhshandeh H. Correlation between dental and cervical vertebral maturation in Iranian females. Iran J Radiol. 2013;10(1):1-7. https://doi.org/10.5812/iranjradiol.9993
https://doi.org/10.5812/iranjradiol.9993...

9 Oyonarte R, Sanchez-Ugarte F, Montt J, Cisternas A, Morales-Huber R, Ramirez-Lobos V, et al. Diagnostic assessment of tooth maturation of the mandibular second molars as a skeletal maturation indicator: A retrospective longitudinal study. Am J Orthod Dentofacial Orthop. 2020;158(3):383-90. https://doi.org/10.1016/j.ajodo.2019.09.012
https://doi.org/10.1016/j.ajodo.2019.09....
-1010 Mohammad RJ. Correlation between skeletal development and maxillary canine eruption. Indian J Dent Res. 2020;31:408-13. https://doi.org/10.4103/ijdr.IJDR_29_19
https://doi.org/10.4103/ijdr.IJDR_29_19...
]. Different parameters using cervical vertebrae [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
,66 Baccetti T, Franchi L, McNamara JA Jr. The cervical vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11(3):119-29. https://doi.org/10.1053/j.sodo.2005.04.005
https://doi.org/10.1053/j.sodo.2005.04.0...
] and carpal bones [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.,44 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
], as well as teeth calcification stages [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.,1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] - as observed in lateral teleradiographs, hand-wrist and panoramic radiographs, respectively, compose a wide variety of available methods to identify the biological age.

The method described by Baccetti et al. [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
], which is based on cervical vertebrae maturation, has been widely used by orthodontists because of its simplicity, objectivity, as well as the common routine use of lateral cephalograms [77 Chen J, Hu H, Guo J, Liu Z, Liu R, Li F, et al. Correlation between dental maturity and cervical vertebral maturity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;110(6):777-83. https://doi.org/10.1016/j.tripleo.2010.08.006
https://doi.org/10.1016/j.tripleo.2010.0...
]. The Greulich’s and Pyle’s method [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.] also provides an important clinical application, as it identifies [1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
] bone events on hand-wrist radiographs concerning the pubertal growth spurt [1313 Cunha A, Cevidanes LHS, Sant’Anna EF, Gudes FR, Luiz RR, McNamara JA, et al. Staging hand-wrist and cervical vertebrae images: a comparison of reproducibility. Dentomaxillofacial Radiol. 2018;47(5):47(5):20170301. https://doi.org/10.1259/dmfr.20170301
https://doi.org/10.1259/dmfr.20170301...
]. Posteriorly, Fishman [44 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
] proposed a different method using the same exam, and it has been mostly recommended, since such assessment tool is able to specify the relative growth speed and the percentage of remaining skeletal development [1414 Flores-Mir C, Nebbe B, Major PW. Use of skeletal maturation based on hand-wrist radiographic analysis as a predictor of facial growth: a systematic review. Angle Orthod. 2004;74(1):118-24. https://doi.org/10.1043/0003-3219(2004)074<0118:UOSMBO>2.0.CO;2
https://doi.org/10.1043/0003-3219(2004)0...
].

Nolla [1414 Flores-Mir C, Nebbe B, Major PW. Use of skeletal maturation based on hand-wrist radiographic analysis as a predictor of facial growth: a systematic review. Angle Orthod. 2004;74(1):118-24. https://doi.org/10.1043/0003-3219(2004)074<0118:UOSMBO>2.0.CO;2
https://doi.org/10.1043/0003-3219(2004)0...
] was one of the first authors to introduce a biological age estimation method according to teeth calcification, therefore being a time-tested tool [1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
]. This method has been traditionally taught during professional formation and used in clinical practice [1616 Bolanos MV, Manrique MC, Bolanos MJ, Briones MT. Approaches to chronological age assessment based on dental calcification. Forensic Sci Int. 2000;110(2):97-106. https://doi.org/10.1016/s0379-0738(00)00154-7
https://doi.org/10.1016/s0379-0738(00)00...
]. Posteriorly, Demirjian et al [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.]. created a simple, practical, and useful classification system for teeth calcification, which is considered as a reference method to predict dental age [1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
].

The reliability of any given assessment tool is essential to enable its safe clinical use [1717 Oakley C, Brunette DM. Diagnostic tests and measurements in clinical practice. In: Brunette DM. Critical thinking: understanding and evaluating dental research. 2nd ed. Quintessence Books; 2007. p. 163-84.]. Additionally, future researches aiming at employing consistent evaluation parameters might benefit from a comprehensive reproducibility analyses. Due to the lack of studies simultaneously evaluating a broad range of skeletal maturation and dental calcification radiographic parameters, with a significant and representative sample, this study was performed to assess the intra- and inter-examiner reproducibility of these examination methods. The null hypothesis was that these assessment tools [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.

4 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
-55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
,1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.,1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] do not present significant reproducibility.

METHODS

Sample

The Research Ethics Committee of Guarulhos University approved this cross-sectional observational analytical study (#48816415.7.0000.5506). Patients and legal guardians signed an informed consent term authorizing their participation in this research.

Sixty-eight orthodontic patients’ records, taken from 2005 to 2015, were randomly selected from files of the Orthodontics Graduation Course (Guarulhos University, Guarulhos, SP, Brazil). In order to be included, patients should have had their baseline lateral teleradiograph, hand-wrist and panoramic radiographs available and obtained in the same date. Inclusion criteria also comprised Brazilian patients of both genders, with ages ranging from 5 to 21 years, with no syndromes or craniofacial malformations, and no history of hand-wrist or face injuries.

Radiographic evaluation

Radiographic evaluation was performed by two undergraduate students in a dark room, on a negatoscope (Essence Dental VH, Araraquara, SP, Brazil) and with a magnifying glass. One of the examiners conducted two evaluation sessions with at least two weeks apart from each other. The examiners previous training and calibration was conducted after instructions were given by an experienced professional (orthodontist). Afterwards, the initial measurements were supervised and corrected by the same professional until the examiners mastered the evaluation methods. Cervical vertebrae (C2, C3 and C4) were analyzed according to Baccetti’s et al. [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
] method, in which maturation stages were categorized in five phases (chart 1). An alternative classification method [1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
], derived from the original [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
] was also evaluated. According to this modified classification system, individuals could be categorized as:

Chart 1
Developmental stages of cervical vertebrae, in chronological order, as determined by Baccetti et al. [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
].
Chart 2
Skeletal maturation stages, in chronological order, as determined by Fishman [44 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
].
  • undergoing pre-pubertal growth spurt period (CVMS I);

  • undergoing pubertal growth spurt period (CVMS II and CVMS III); or

  • undergoing post-pubertal growth spurt period (CVMS IV and V).

The hand-wrist radiography was analyzed according to Fishman [44 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
], in which ossification centers were used to identify 11 possible skeletal maturity stages (chart 2). The method proposed by Greulich and Pyle [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.] was also used, as detailed in chart 3.

Chart 3
Skeletal maturation stages, in chronological order, as determined by Greulich and Pyle [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.].

The calcification of mandibular teeth (canine, first premolar, second premolar and second molar) was categorized according to Nolla’s [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.] (chart 4), as well as Demirjian’s et al. [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] method (chart 5).

Chart 4
Dental calcification stages, in chronological order, as determined by Nolla [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.].
Chart 5
Dental calcification stages, in chronological order, as determined by Demirjian et al. [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.].

Data analysis

Intra- and inter-examiner reproducibility analyses were calculated by kappa (k) coefficient. Kappa value was rated as “low” (k ≤ 0.20), “fair” (0.20 < k ≤ 0.40), “moderate” (0.40 < k ≤ 0.60), “substantial” (0.60 < k ≤ 0.80) or “nearly perfect” (0.80 < k ≤ 1.00) [1919 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-74.]. The data were analyzed with SPSS software (version 25 for Windows; SPSS Inc, Chicago, IL, USA) with a 5% (α ≤ 0.05) significance level.

RESULTS

Sixty-eight patients were included in this study, (females: 53.0%; males: 47.0%). Patients’ mean age was 11.1 years (standard deviation: 1.79 years).

The kappa values obtained after intra- and inter-examiner analyses for Baccetti’s et al. [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
] method were 0.84 (nearly perfect) and 0.78 (substantial), respectively. For the cervical vertebrae simplified classification system [1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
], intra- and inter-examiner k-values were 0.74 and 0.68, respectively (both substantial). The p-values for all of the above-mentioned analyses were below 0.001.

Intra- and inter-examiner analyses for both hand-wrist classification methods were rated as substantial, displaying satisfactory values (table 1). Intra-examiner kappa values for both methods analyzed on panoramic radiographs were categorized as nearly perfect; and inter-examiner values varied from substantial to nearly perfect (table 2).

Table 1
Intra- and inter-examiner reproducibility analyses of hand-wrist radiographic parameters.
Table 2
Reproducibility intra and inter-examiner of radiographic parameters in panoramic radiography according to each method analyzed.

The null hypothesis, according to which the evaluation methods [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.

4 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
-55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
,1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.,1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] investigated here do not present significant reproducibility, was thus rejected.

DISCUSSION

The reliability of skeletal and dental classification systems [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.

4 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...

5 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
-66 Baccetti T, Franchi L, McNamara JA Jr. The cervical vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11(3):119-29. https://doi.org/10.1053/j.sodo.2005.04.005
https://doi.org/10.1053/j.sodo.2005.04.0...
,1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.,1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] must be considered in order to determine its quality as an assessment tool and to guide its potential clinical use. Previous studies have already determined the reliability of skeletal and dental maturation radiographic parameters [77 Chen J, Hu H, Guo J, Liu Z, Liu R, Li F, et al. Correlation between dental maturity and cervical vertebral maturity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;110(6):777-83. https://doi.org/10.1016/j.tripleo.2010.08.006
https://doi.org/10.1016/j.tripleo.2010.0...
,88 Valizadeh S, Eil N, Ehsani S, Bakhshandeh H. Correlation between dental and cervical vertebral maturation in Iranian females. Iran J Radiol. 2013;10(1):1-7. https://doi.org/10.5812/iranjradiol.9993
https://doi.org/10.5812/iranjradiol.9993...
,1313 Cunha A, Cevidanes LHS, Sant’Anna EF, Gudes FR, Luiz RR, McNamara JA, et al. Staging hand-wrist and cervical vertebrae images: a comparison of reproducibility. Dentomaxillofacial Radiol. 2018;47(5):47(5):20170301. https://doi.org/10.1259/dmfr.20170301
https://doi.org/10.1259/dmfr.20170301...
,1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
,1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
,2020 Gabriel DB, Southard KA, Qian F, Marshall SD, Franciscus RG, Southard TE. Cervical vertebrae maturation method: poor reproducibility. Am J Orthod Dentofacial Orthop. 2009;136(4):478.e1-7. https://doi.org/10.1016/j.ajodo.2007.08.028
https://doi.org/10.1016/j.ajodo.2007.08....

21 Nestman TS, Marshall SD, Qian F, Holton N, Franciscus RG, Southard TE. Cervical vertebrae maturation method morphologic criteria: poor reproducibility. Am J Orthod Dentofacial Orthop. 2011;140(2):182-8. https://doi.org/10.1016/j.ajodo.2011.04.013
https://doi.org/10.1016/j.ajodo.2011.04....

22 Bagherpour A, Pousti M, Adelianfar E. Hand skeletal maturity and its correlation with mandibular dental development. J Clin Exp Dent. 2014;6(3):e275-9. https://doi.org/10.4317/jced.51433
https://doi.org/10.4317/jced.51433...

23 Sohrab A, Ahari SB, Moslemzadeh H, Rafighi A, Aghazadeh A. The reliability of clinical decisions based on the cervical vertebrae maturation staging method. Eur J Orthod. 2016;38(1):8-12. https://doi.org/10.1093/ejo/cjv030
https://doi.org/10.1093/ejo/cjv030...

24 Lecca-Morales RM, Carruitero MJ. Relationship between dental calcification and skeletal maturation in a Peruvian sample. Dental Press J Orthod. 2017;22(3):89-96. https://doi.org/10.1590/2177-6709.22.3.089-096.oar
https://doi.org/10.1590/2177-6709.22.3.0...

25 Kamal AT, Shaikh A, Fida, M. Assessment of skeletal maturity using the calcification stages of permanent mandibular teeth. Dental Press J Orthod. 2018;23(4):44.e1-8. https://doi.org/10.1590/2177-6709.23.4.44.e1-8.onl
https://doi.org/10.1590/2177-6709.23.4.4...
-2626 Ozturk T, Gumus H, Ozturk G. Are dental maturation, skeletal maturation, and chronological age associated with complete cleft lip and palate? Cleft Palate Craniofac J. 2020. https://doi.org/10.1177/1055665620944776
https://doi.org/10.1177/1055665620944776...
], although mostly individually. However, in order to compare the available diagnostic methods, this study investigated, in a relatively larger sample, the intra- and inter-examiner reproducibility of a large number of relevant parameters. Considering that reproducibility is one of the essential requirements for a diagnostic assessment tool [1717 Oakley C, Brunette DM. Diagnostic tests and measurements in clinical practice. In: Brunette DM. Critical thinking: understanding and evaluating dental research. 2nd ed. Quintessence Books; 2007. p. 163-84.,2727 Conger AJ. Kappa and rater accuracy: paradigms and parameters. Educ Psychol Meas. 2017;77(6):1019-47. https://doi.org/10.1177/0013164416663277
https://doi.org/10.1177/0013164416663277...
], the results provided by this study can guide practitioners towards the selection of a reliable diagnostic test.

In the lateral teleradiographic examination, excellent reproducibility was found for Baccetti’s et al. classification method, for both intra and inter-examiner coefficients, which confirms the reliability of this diagnostic tool [66 Baccetti T, Franchi L, McNamara JA Jr. The cervical vertebral maturation (CVM) method for the assessment of optimal treatment timing in dentofacial orthopedics. Semin Orthod. 2005;11(3):119-29. https://doi.org/10.1053/j.sodo.2005.04.005
https://doi.org/10.1053/j.sodo.2005.04.0...
]. Previous studies presented similar kappa values [88 Valizadeh S, Eil N, Ehsani S, Bakhshandeh H. Correlation between dental and cervical vertebral maturation in Iranian females. Iran J Radiol. 2013;10(1):1-7. https://doi.org/10.5812/iranjradiol.9993
https://doi.org/10.5812/iranjradiol.9993...
,1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
]. Valizadeh, et al. [88 Valizadeh S, Eil N, Ehsani S, Bakhshandeh H. Correlation between dental and cervical vertebral maturation in Iranian females. Iran J Radiol. 2013;10(1):1-7. https://doi.org/10.5812/iranjradiol.9993
https://doi.org/10.5812/iranjradiol.9993...
] reported intra-observer kappa of 0.92 for the cervical maturation classification system, which is in accordance with the nearly perfect results observed in the current study. However, in their research, slightly higher values could be explained by the small sample analyzed in comparison with ours (68 subjects).

Contrastingly, a couple of studies reported relatively lower reproducibility values for cervical vertebrae maturation method [2020 Gabriel DB, Southard KA, Qian F, Marshall SD, Franciscus RG, Southard TE. Cervical vertebrae maturation method: poor reproducibility. Am J Orthod Dentofacial Orthop. 2009;136(4):478.e1-7. https://doi.org/10.1016/j.ajodo.2007.08.028
https://doi.org/10.1016/j.ajodo.2007.08....
,2121 Nestman TS, Marshall SD, Qian F, Holton N, Franciscus RG, Southard TE. Cervical vertebrae maturation method morphologic criteria: poor reproducibility. Am J Orthod Dentofacial Orthop. 2011;140(2):182-8. https://doi.org/10.1016/j.ajodo.2011.04.013
https://doi.org/10.1016/j.ajodo.2011.04....
]. Both of them used the original CVMS method6 comprising six growth phases, which might explain this difference. In addition, the authors reported that more than two examiners were involved in their analyses; thus, it is speculated that agreement tends to become relatively smaller, as a consequence. According to Nestman, et al. [2121 Nestman TS, Marshall SD, Qian F, Holton N, Franciscus RG, Southard TE. Cervical vertebrae maturation method morphologic criteria: poor reproducibility. Am J Orthod Dentofacial Orthop. 2011;140(2):182-8. https://doi.org/10.1016/j.ajodo.2011.04.013
https://doi.org/10.1016/j.ajodo.2011.04....
], the difficulty in identifying C3 and C4 bodies shape might justify their inferior results.

The merging of Baccetti’s method in three growth stages (pre-pubertal, pubertal, and post-pubertal growth spurt periods), as also utilized by Litsas, et al. [1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
], is intended to simplify the clinical use of this diagnostic tool towards the straightforward identification of orthodontic interventional timing. According to the data presented, this simplified assessment tool provided substantial intra- and inter-examiner k values, indicating high reproducibility and similar results to the previously cited research [1818 Litsas G, Athanasiou, AE, Papadopoulos MA, Ioannidou-Marathiotou I, Karagiannis V. Dental calcification stages as determinants of the peak growth period. J Orofac Orthop. 2016;77(5):341-9. https://doi.org/10.1007/s00056-016-0040-6
https://doi.org/10.1007/s00056-016-0040-...
]. Sohrab, et al [2323 Sohrab A, Ahari SB, Moslemzadeh H, Rafighi A, Aghazadeh A. The reliability of clinical decisions based on the cervical vertebrae maturation staging method. Eur J Orthod. 2016;38(1):8-12. https://doi.org/10.1093/ejo/cjv030
https://doi.org/10.1093/ejo/cjv030...
]. found a moderate inter-examiner reproducibility for C3 and C4 shape evaluation – the sole differential sign between stages IV and V, indicating a difficulty of this cervical vertebrae maturation method, even as Nestman, et al. [2121 Nestman TS, Marshall SD, Qian F, Holton N, Franciscus RG, Southard TE. Cervical vertebrae maturation method morphologic criteria: poor reproducibility. Am J Orthod Dentofacial Orthop. 2011;140(2):182-8. https://doi.org/10.1016/j.ajodo.2011.04.013
https://doi.org/10.1016/j.ajodo.2011.04....
]. In relation to that same research, CVMS classification reliability is higher, when concerning to clinical decisions, rather than just a grading system. Therefore, in the simplified method, stages IV and V are grouped into post-pubertal growth spurt period, once both results in the same clinical decision.

Although the method described by Greulich and Pyle [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.] has more categories, which could anticipate less agreement, the results of both hand-wrist radiographic methods’ reproducibility were very similar, with high k-values for intra- and inter-examiner analyses. Fishman’s method presented satisfactory reproducibility in several researches [2222 Bagherpour A, Pousti M, Adelianfar E. Hand skeletal maturity and its correlation with mandibular dental development. J Clin Exp Dent. 2014;6(3):e275-9. https://doi.org/10.4317/jced.51433
https://doi.org/10.4317/jced.51433...
,2424 Lecca-Morales RM, Carruitero MJ. Relationship between dental calcification and skeletal maturation in a Peruvian sample. Dental Press J Orthod. 2017;22(3):89-96. https://doi.org/10.1590/2177-6709.22.3.089-096.oar
https://doi.org/10.1590/2177-6709.22.3.0...
,2626 Ozturk T, Gumus H, Ozturk G. Are dental maturation, skeletal maturation, and chronological age associated with complete cleft lip and palate? Cleft Palate Craniofac J. 2020. https://doi.org/10.1177/1055665620944776
https://doi.org/10.1177/1055665620944776...
]. Greulich’s and Pyle’s method had substantial reproducibility values, for both intra and inter-examiner analyses, and another study also found similar results [1313 Cunha A, Cevidanes LHS, Sant’Anna EF, Gudes FR, Luiz RR, McNamara JA, et al. Staging hand-wrist and cervical vertebrae images: a comparison of reproducibility. Dentomaxillofacial Radiol. 2018;47(5):47(5):20170301. https://doi.org/10.1259/dmfr.20170301
https://doi.org/10.1259/dmfr.20170301...
]. Nevertheless, as a negative implication, the routine clinical use of hand-wrist radiographic methods involves additional radiation exposure to patients [2828 Joshi VV, Iyengar AR, Nagesh KS, Gupta J. Comparative study between cervical vertebrae and hand-wrist maturation for the assessment of skeletal age. Rev Clín Pesq Odontol. 2010;6(3):207-13.,2929 Manosudprasit M, Wangsrimongkol T, Pisek P, Chantaramungkorn M. Comparative study between the hand-wrist method and cervical vertebral maturation method for evaluation skeletal maturity in cleft patients. J Med Assoc Thai. 2013;96(Suppl 4):S19-24.], while the lateral teleradiograph is readily available to orthodontists [1313 Cunha A, Cevidanes LHS, Sant’Anna EF, Gudes FR, Luiz RR, McNamara JA, et al. Staging hand-wrist and cervical vertebrae images: a comparison of reproducibility. Dentomaxillofacial Radiol. 2018;47(5):47(5):20170301. https://doi.org/10.1259/dmfr.20170301
https://doi.org/10.1259/dmfr.20170301...
].

The panoramic radiography, an accessible exam to pediatricians and general dentists, has been alternatively used to determine craniofacial development according to dental calcification as it correlates to the growth pubertal stages [77 Chen J, Hu H, Guo J, Liu Z, Liu R, Li F, et al. Correlation between dental maturity and cervical vertebral maturity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;110(6):777-83. https://doi.org/10.1016/j.tripleo.2010.08.006
https://doi.org/10.1016/j.tripleo.2010.0...

8 Valizadeh S, Eil N, Ehsani S, Bakhshandeh H. Correlation between dental and cervical vertebral maturation in Iranian females. Iran J Radiol. 2013;10(1):1-7. https://doi.org/10.5812/iranjradiol.9993
https://doi.org/10.5812/iranjradiol.9993...

9 Oyonarte R, Sanchez-Ugarte F, Montt J, Cisternas A, Morales-Huber R, Ramirez-Lobos V, et al. Diagnostic assessment of tooth maturation of the mandibular second molars as a skeletal maturation indicator: A retrospective longitudinal study. Am J Orthod Dentofacial Orthop. 2020;158(3):383-90. https://doi.org/10.1016/j.ajodo.2019.09.012
https://doi.org/10.1016/j.ajodo.2019.09....
-1010 Mohammad RJ. Correlation between skeletal development and maxillary canine eruption. Indian J Dent Res. 2020;31:408-13. https://doi.org/10.4103/ijdr.IJDR_29_19
https://doi.org/10.4103/ijdr.IJDR_29_19...
], and it might guide timely patient referral to orthodontist [11 Sadowsky PL. Craniofacial growth and the timing of treatment. Am J Orthod Dentofacial Orthop. 1998;113(1):19-23. https://doi.org/10.1016/S0889-5406(98)70272-0
https://doi.org/10.1016/S0889-5406(98)70...
,22 Dadgar S, Hadian H, Ghobadi M, Sobouti F, Rakhshan V. Correlations among chronological age, cervical vertebral maturation index, and Demirjian developmental stage of the maxillary and mandibular canines and second molars. Surg Radiol Anat. 2021;43(1):131-143. https://doi.org/10.1007/s00276-020-02541-4
https://doi.org/10.1007/s00276-020-02541...
]. Intra- and inter-examiner reproducibility of Nolla’s [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.] method was evaluated, and the tooth 33 had relatively larger reproducibility rates. For Demirjian’s et al. [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] method, the best performance was observed for the tooth 44. Both methods were rated from substantial to nearly perfect intra- and inter-examiner reliability; and these results are in accordance with previous ones [2525 Kamal AT, Shaikh A, Fida, M. Assessment of skeletal maturity using the calcification stages of permanent mandibular teeth. Dental Press J Orthod. 2018;23(4):44.e1-8. https://doi.org/10.1590/2177-6709.23.4.44.e1-8.onl
https://doi.org/10.1590/2177-6709.23.4.4...
] that reported high degree of correlation in intraclass correlation coefficient for Nolla’s and Demirjian’s scores (0.915 and 0.800, respectively). Al-Balbeesi, et al. [3030 Al-Balbeesi HO, Al-Nahas NW, Baidas LF, Bin Huraib SM, Alhaidari R, Alwadai G. Correlation between skeletal maturation and developmental stages of canines and third molars among Saudi subjects. Saudi Dent J. 2018;30(1):74-84. https://doi.org/10.1016/j.sdentj.2017.11.003
https://doi.org/10.1016/j.sdentj.2017.11...
] stated that these two methodologies were used in their investigation because of their simplicity and reliability.

According to Kumaresan, et al. [1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
], Nolla’s [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.] method had a moderate reliability score. However, the authors also observed high values for intraclass correlation coefficient (considering both intra- and inter-examiner reliability analyses), which is analogous to the findings of the present research. In the same study [1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
], the reliability evaluation was performed with the calculation of the mean absolute error of observations, which might explain this difference in classification. Yet, Demirjian’s et al. [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.] method had the lowest reliability rate among those tested [1515 Kumaresan R, Cugati N, Chandrasekaran B, Karthikeyan P. Reliability and validity of five radiographic dental-age estimation methods in a population of Malaysian children. J Investigative Clin Dent. 2016;7(1):102-9. https://doi.org/10.1111/jicd.12116
https://doi.org/10.1111/jicd.12116...
], even though its intraclass correlation coefficients were satisfactory, which also analogous to results presented here.

In this current investigation, the diagnostic methods did not have their validity evaluated, which can be regarded as a limitation. The characteristics of an ideal assessment tool can only be entirely assessed if its validity is also considered [1717 Oakley C, Brunette DM. Diagnostic tests and measurements in clinical practice. In: Brunette DM. Critical thinking: understanding and evaluating dental research. 2nd ed. Quintessence Books; 2007. p. 163-84.]. The findings provided by this study encourage further researches with panoramic radiographs to evaluate craniofacial development through dental calcification staging and its correlation to growth phases, which can enable panoramic radiographic records as a validated tool to be reliably used for timely referrals.

The radiographic evaluation was performed by undergraduate students, which could be perceived as another limitation of this study. However, these examiners were previously trained and calibrated by an experienced professional (orthodontist), which might somehow enable the generalizability potential of the results for trained professionals in clinical situations.

Hand-wrist radiographic evaluation methods result in additional radiographic exposure to the patients. Therefore, considering they did not achieve better results in this study, their use for practical purposes is not recommended.

CONCLUSION

All methods analyzed here obtained satisfactory intra- and inter-examiner reproducibility performances. Fishman’s [44 Fishman LS. Radiographic evaluation of skeletal maturation. A clinically oriented method based on hand-wrist films. Angle Orthod 1982;52(2):88-112. https://doi.org/10.1043/0003-3219(1982)052<0088:REOSM>2.0.CO;2
https://doi.org/10.1043/0003-3219(1982)0...
] and Greulich’s and Pyle’s [33 Greulich WW, Pyle SI. Radiographic atlas of skeletal development of hand and wrist. 2a ed. Standford, Standford University Press; 1959.] methods had similar values, as did Nolla’s [1111 Nolla CM. The development of the permanent teeth. J Dent Child. 1960;27(4):254-63.] and Demirjian’s et al. [1212 Demirjian A, Goldstain H, Tanner JM. A new system of dental age assessment. Human Biol. 1973;45(2):211-27.]. Among the methods that evaluated skeletal maturity, relatively better reproducibility rates were observed for Baccetti’s et al. [55 Baccetti T, Franchi L, McNamara Jr JA. An improved version of the cervical vertebral maturation (CVM) method for the assessment of mandibular growth. Angle Orthod. 2002;72(4):316-23. https://doi.org/10.1043/0003-3219(2002)072<0316:AIVOTC>2.0.CO;2
https://doi.org/10.1043/0003-3219(2002)0...
] method, as compared to others.

Acknowledgment

The authors would like to thank the São Paulo Research Foundation (FAPESP) for the financial support (#2019/20923-2).

How to cite this article

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    » https://doi.org/10.1177/1055665620944776
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    Manosudprasit M, Wangsrimongkol T, Pisek P, Chantaramungkorn M. Comparative study between the hand-wrist method and cervical vertebral maturation method for evaluation skeletal maturity in cleft patients. J Med Assoc Thai. 2013;96(Suppl 4):S19-24.
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    Al-Balbeesi HO, Al-Nahas NW, Baidas LF, Bin Huraib SM, Alhaidari R, Alwadai G. Correlation between skeletal maturation and developmental stages of canines and third molars among Saudi subjects. Saudi Dent J. 2018;30(1):74-84. https://doi.org/10.1016/j.sdentj.2017.11.003
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Assistant editor: Marcelo Sperandio

Publication Dates

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    21 Nov 2022
  • Date of issue
    2022

History

  • Received
    04 June 2021
  • Reviewed
    30 Sept 2021
  • Accepted
    21 Dec 2021
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