Cervical vertebrae have always been an area of interest in routine diagnostic lateral cephalogram for evaluating optimal treatment timing in orthodontics. The morphological changes in cervical vertebrae seen on these radiographs have been correlated with the skeletal maturation stages, and the same has been studied using visual examinations,[2,3] as well as with regression formulas.[4–6]
Skeletal malocclusion which occurs as a result of interplay of genetic and environmental influences has also been linked to the postural and morphological deviations in cervical vertebral column in healthy individuals. Studies have established an association between the morphology of cervical vertebrae and craniofacial skeleton thereby indirectly affecting the length of maxilla and mandible. However, contradictory results have also been reported in the literature.[9–11]
Since the cervical vertebral morphology plays a crucial role in determining the craniofacial skeletal maturation, understanding of the association between vertebral morphology and maxillomandibular length will further aid an orthodontist in the formulation of specific treatment plan based on growth status of the patient. Therefore, with the null hypothesis that the length of maxilla and mandible does not vary with the morphology of C3 and C4 vertebrae among various sagittal skeletal malocclusions with no gender variation, the present study aimed to investigate the association between the morphology of C3 and C4 vertebrae with the maxillomandibular length among different sagittal skeletal malocclusion along with gender association for the same.
Materials and Methods
The ethical clearance was obtained from institutional ethical committee prior to the initiation of study (IEC/Dental/IEC/Dental/21005 dated October 01, 2021 dated October 01, 2021). This retrospective study was carried out on lateral cephalogram of patients who reported to orthodontic clinic of this tertiary care hospital between January 2020 and August 2021. The lateral cephalogram and orthopantomogram (OPG) were obtained following standard protocols by a qualified and trained radiographer, the same machine being manufactured by M/s. Cefla Dental Group Italy, Model-NEW TOM GIANO: G-XR-46893, with exposure parameters of 80 kVp, 10 mA, and 1.6 s. The demographic data such as age and gender were extracted from the patients’ record file. A total of 315 records were screened from the archive, out of which 76 records were included in the study based on the following inclusion and exclusion criteria.
- Adult >17 years (Cervical Vertebral Maturation Index 5 or 6) including males and females
- Availability of complete set of pretreatment records including medical case sheet
- Availability of good quality, digital copy of pretreatment OPG, and lateral cephalogram (with first four cervical vertebrae clearly visible).
- Medical history suggestive of any systemic disease/condition affecting bone morphology
- Medical history of neck and cervical disorders or any neuromuscular disorder
- Syndromic patients including cleft lip and palate
- Evident facial asymmetry
- History of previous orthopedic therapy or orthognathic surgery.
Segregation of subjects in sagittal relations
Standard cephalometric landmarks were manually identified on the digital image of the lateral cephalogram in the Nemoceph™ software (Nemotec, version 6.0) and automated McNamara analysis was carried out to segregate the cephalograms based on maxillomandibular differential (MMD), i.e., difference between the effective length of mandible (Co-Gn) and maxilla (Co-A) which was recorded for each subject. Accordingly, 76 subjects were segregated into different sagittal skeletal relations, i.e., Class I (MMD 25–30 mm), Class II (MMD <25 mm), and Class III (MMD >30 mm), thereby comprising 30 cephalograms each in Class I and Class II and 16 cephalograms in Class III, respectively.
Assessment of cervical vertebral morphology
The morphology of C3 and C4 vertebrae was studied on digital image of lateral cephalogram on NNT VIEWER (NewTom image analysis software) using methodology as discussed by Alkan et al. The vertebral index (height/width) was calculated in percentage (%) for C3 and C4 vertebrae, respectively [Figure 1 and Table 1].
The data assessment for all the subjects was carried out by the same operator. All the measurements were reassessed after 2 weeks by the same and another trained operator, in order to ascertain intra- and interoperator reliability.
The entire data were statistically analyzed using Statistical Package for the Social Sciences (SPSS I. IBM SPSS statistics for windows. Armonk, New York, USA: IBM SPSS. 2013;2:119) for MS Windows. The intergroup statistical comparison of means of continuous variables was done using independent sample t-test for two groups and by analysis of variance (ANOVA) with post hoc Bonferroni test for multiple group comparisons for more than two groups. The underlying normality assumption was tested before subjecting the study variables to t-test and ANOVA. The level of significance (P value) was set to be <0.05 for all statistical analysis. All hypotheses were formulated using two tailed alternatives against each null hypothesis (hypothesis of no difference).
Inter- and intraobserver variability analysis did not show a statistically significant difference (P > 0.05). The intraclass correlation coefficient over 0.900 for all study parameters indicates almost perfect agreement between two observers. Table 2 and Figure 2 depict the chronological age and vertebral and cephalometric characteristics of the subjects in Class I, II, and III malocclusions, while gender-based distribution of the same in each Class is outlined in Table 3 and Figure 3.
The morphology of C3 and C4 vertebrae as evaluated by respective vertebral index did not differ significantly across different skeletal malocclusions studied [Table 4 and Figure 4] along with statistically nonsignificant correlation with length of maxilla, length of mandible, and MMD in all the skeletal relations [Table 5]. No significant association could be established between C3 and C4 vertebral index with specific gender in each skeletal relation [Table 6 and Figure 5].
The present study was designed taking into consideration the maturation status of craniofacial skeleton and cervical vertebrae to minimize the growth-related bias. Approximately 98% of facial growth is completed by 15 years in females and usually at the age of 17–18 years in males. The skeletal maturation of C3 and C4 vertebrae is also attained by this age. In our study, the mean chronological age of the subjects was 18.50 years, 18.33 years, and 21.25 years in skeletal Class I, II, and III malocclusion, respectively. Lateral cephalogram, a routinely used orthodontic diagnostic aid, was studied to establish any association between the morphology of C3 and C4 vertebrae and maxillomandibular length in various sagittal skeletal malocclusions, though the cervical vertebral morphology is influenced by various individual factors such as ethnicity.[15–17] gender,[15,16] and posture.[15,16] In the present study, the vertebral morphology was evaluated using cephalometric parameters to determine anterior height and width of lower border of cervical vertebrae. The ratio of these two parameters was then used to derive vertebral index to define the morphology of respective cervical vertebrae. Literature supports the association between deviation of cervical vertebral morphology and craniofacial anomalies/syndromes including cleft lip and palate.[18,19] However, data also exist regarding such association in various nonsyndromic sagittal[20,21] and vertical malocclusions.[22,23] Hence, it can be concluded that morphological deviation of upper cervical vertebrae has an association with craniofacial morphology along with malformation of jaws. Ectomesenchymal tissues derived from the neural crest cells are responsible for development of the maxilla and mandible. Therefore, aberration in timing and/or amount of migration of neural crest cells can influence development of craniofacial structures. Although the accurate signaling of this migration of cells has not been completely understood yet the embryogenesis between the notochord, para axial mesoderm, the neural tube and neural crest can explicate the connotation among cervical vertebrae, cranial base and craniofacial structures.
The present study could not establish any association between the morphology of C3 and C4 vertebrae with maxillomandibular length among three skeletal malocclusions studied along with nonsignificant gender correlation. Alkan et al. reported similar findings with nonsignificant differences in the C2, C3, and C4 vertebral measurements among adult Turkish females with different sagittal craniofacial patterns. Jain et al. reported nonsignificant correlation between cervical vertebral anomalies and skeletal malocclusions in Indian population. Similar findings were reported by Kamak and Yildırım in Turkish population.
Even though routinely used lateral cephalograms evaluate various craniofacial dimensions and morphological deviations in upper cervical vertebrae, their accuracy is questionable due to posed limitations such as distortion, magnification, superposition, and positioning errors along with difficulty in identifying and registering anatomical structures. However, these limitations can be abridged by use of 3D imaging in future studies. It is also recommended to validate the findings of the present study with a larger sample and multicentric settings.
Within the scope of the study, it can be concluded that the morphology of C3 and C4 vertebrae is not correlated with the length of maxilla and mandible and also it does not vary significantly among males and females with different sagittal skeletal malocclusions.
The study was approved by the institutional Ethics Committee of Department of dental surgery and oral health sciences, AFMC Pune (IEC/Dental/21005 dated October 01, 2021).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
1. Lamparski DG. Skeletal Age Assessment Utilizing Cervical Vertebrae
[Dissertation] Pittsburgh University of Pittsburgh 1972.
2. Hassel B, Farman AG. Skeletal maturation evaluation using cervical vertebrae
. Am J Orthod Dentofacial Orthop 1995;107:58–66.
3. Baccetti T, Franchi L, McNamara JA Jr. An improved version of the Cervical Vertebral Maturation (CVM) method for the assessment of mandibular growth. Angle Orthod 2002;72:316–23.
4. Mito T, Sato K, Mitani H. Cervical vertebral bone age in girls. Am J Orthod Dentofacial Orthop 2002;122:380–5.
5. Chen LL, Xu TM, Jiang JH, Zhang XZ, Lin JX. Quantitative cervical vertebral maturation assessment in adolescents with normal occlusion:A mixed longitudinal study. Am J Orthod Dentofacial Orthop 2008;134:720.e1–720.e7.
6. Chandrasekar R, Chandrasekhar S, Sundari KK, Ravi P. Development and validation of a formula for objective assessment of cervical vertebral bone age. Prog Orthod 2020;21:38.
7. Proffit WR. The development of dentofacial deformity:Influences and etiologic factors Proffit WR, White RP, Sarver DM. Contemporary Treatment of Dentofacial Deformity St Louis Mosby 2003 29–68.
8. Sonnesen L, Pedersen CE, Kjaer I. Cervical column morphology related to head posture, cranial base angle, and condylar malformation. Eur J Orthod 2007;29:398–403.
9. Alkan Ö, Aydoğan C, Akkaya S. Morphological comparison of cervical vertebrae
in adult females with different sagittal craniofacial patterns:A cross-sectional study. J Craniovertebr Junction Spine 2016;7:135–9.
10. Kamak H, Yildırım E. The distribution of cervical vertebrae
anomalies among dental malocclusions. J Craniovertebr Junction Spine 2015;6:158–61.
11. Jain RK, Pandian SM, Dinesh S, Kumar MP. Cervical vertebral morphology in different skeletal patterns –A cephalometric study. Drug Invent Today 2019;11:587–90.
12. McNamara JA Jr. A method of cephalometric evaluation. Am J Orthod 1984;86:449–69.
13. Wolford LM, Karras SC, Mehra P. Considerations for orthognathic surgery during growth, part 1:Mandibular deformities. Am J Orthod Dentofacial Orthop 2001;119:95–101.
14. Altan M, Nebioğlu Dalci Ö, İseri H. Growth of the cervical vertebrae
in girls from 8 to 17 years. A longitudinal study. Eur J Orthod 2012;34:327–34.
15. Solow B, Barrett MJ, Brown T. Craniocervical morphology and posture in Australian aboriginals. Am J Phys Anthropol 1982;59:33–45.
16. Cooke MS, Wei SH. Intersex differences in craniocervical morphology and posture in Southern Chinese and British caucasians. Am J Phys Anthropol 1988;77:43–51.
17. Grave B, Brown T, Townsend G. Comparison of cervicovertebral dimensions in Australian aborigines and caucasians. Eur J Orthod 1999;21:127–35.
18. Sandham A. Cervical vertebral anomalies in cleft lip and palate. Cleft Palate J 1986;23:206–14.
19. Vastardis H, Evans CA. Evaluation of cervical spine abnormalities on cephalometric radiographs. Am J Orthod Dentofacial Orthop 1996;109:581–8.
20. Arntsen T, Sonnesen L. Cervical vertebral column morphology related to craniofacial morphology and head posture in preorthodontic children with class II malocclusion and horizontal maxillary overjet. Am J Orthod Dentofacial Orthop 2011;140:e1–7.
21. Sonnesen L, Kjaer I. Cervical column morphology in patients with skeletal class III malocclusion and mandibular overjet. Am J Orthod Dentofacial Orthop 2007;132:12.e7–12.
22. Sonnesen L, Kjaer I. Cervical column morphology in patients with skeletal open bite. Orthod Craniofac Res 2008;11:17–23.
23. Sonnesen L, Kjaer I. Cervical vertebral body fusions in patients with skeletal deep bite. Eur J Orthod 2007;29:464–70.
24. Kjaer I. Neuro-osteology. Crit Rev Oral Biol Med 1998;9:224–44.
25. Sonnesen L, Nolting D, Kjaer KW, Kjaer I. Association between the development of the body axis and the craniofacial skeleton studied by immunohistochemical analyses using collagen II, Pax9, Pax1, and Noggin antibodies. Spine (Phila Pa 1976) 2008;33:1622–6.
26. Ahlqvist J, Eliasson S, Welander U. The effect of projection errors on cephalometric length measurements. Eur J Orthod 1986;8:141–8.