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Anomalies of the cervical vertebrae in patients with skeletal Class II malocclusion and horizontal maxillary overjet
Liselotte Sonnesena and Inger Kjrb Copenhagen, Denmark Introduction: Cervical column morphology was examined in adult patients with skeletal Class II malocclusion and horizontal maxillary overjet; the ndings were compared with cervical column morphology in an adult control group with neutral occlusion and normal craniofacial morphology. This has not previously been investigated. Methods: The overjet group consisted of 34 patients: 28 women (ages, 18-42 years) and 6 men (ages, 18-38 years). Their horizontal overjets ranged from 5.47 to 15.29 mm. The control group consisted of 21 subjects: 15 women (ages, 23-40 years) and 6 men (ages, 25-44 years). A visual assessment of the cervical column was made, and craniofacial dimensions were measured on each subjects prole radiograph. Results: In the overjet group, 52.9% had fusion of the cervical column, and 5.9% had posterior arch deciency. Fusions occurred signicantly more often in the overjet group compared with the control group (P .01). Associations were found between fusions of the cervical column and mandibular retrognathia (P .05), large cranial base angle (P .05), and large horizontal overjet (P .05). Conclusions: The results could provide a new method to phenotypically subdivide skeletal maxillary overjets. This is important for the diagnosis and the correct treatment of these patients. (Am J Orthod Dentofacial Orthop 2008;133: 189.e15-189.e20)

eviations of cervical column morphology occur in healthy subjects with neutral occlusion and normal craniofacial morphology and in patients with craniofacial syndromes, deviating craniofacial morphology, and severe malocclusion traits. Recently, it was found that fusions between the second and third cervical vertebrae occur in 14.3% of healthy subjects.1 Thus, fusions of the upper cervical column in that range are considered normal. In previous studies, an association was found between malformations of the upper cervical vertebrae and patients with cleft lip or palate.2-4 Recently, an association was also found between malformation of the upper cervical vertebrae not only in patients with condylar hypoplasia1 but also in patients with skeletal deepbite5 and skeletal mandibular overjet.6 These studies showed that cervical column deviations occurred in 72.7% of those in the condylar hypoplasia group, in 41.5% of the deepbite group, and in 61.4% of the
From the Department of Orthodontics, School of Dentistry, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark. a Associate professor. b Professor. Reprint requests to: Liselotte Sonnesen, Department of Orthodontics, School of Dentistry, Faculty of Health Sciences, University of Copenhagen, 20 Nrre All, DK-2200 Copenhagen N, Denmark; e-mail, lls@odont.ku.dk. Submitted, May 09, 2007; revised and accepted, July 20, 2007. 0889-5406/$34.00 Copyright 2008 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2007.07.018

mandibular overjet group. Deviations occurred signicantly more often in all 3 patient groups compared with the control group. This indicates that the morphological deviations of the upper cervical vertebrae are associated not only with malformation of the jaws but also with craniofacial morphology and occlusion. Accordingly, it is relevant to focus on similar associations in patients with skeletal Class II and horizontal maxillary overjet. To our knowledge, no one has studied cervical column morphology in relation to skeletal Class II malocclusion and horizontal maxillary overjet. Our aims in this study were (1) to describe the morphology of the cervical column in adult patients with skeletal horizontal maxillary overjet, (2) to compare the morphology of the cervical column in a group of adult patients with skeletal horizontal maxillary overjet (overjet group) with a control group with neutral occlusion and normal craniofacial morphology (control group), and (3) to analyze associations between the morphology of the cervical column and craniofacial dimensions in the total group (overjet and control groups).
MATERIAL AND METHODS

The overjet group consisted of 34 patients: 28 women (ages, 18-42 years; mean, 25.0) and 6 men (ages, 18-38 years; mean, 24.0). The inclusion criteria for the horizon188.e15

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Table I.

Craniofacial dimensions in the horizontal maxillary overjet and the control groups
Overjet (n 34) SD Controls (n Mean 21) SD Group P Sex P

Variable () Sagittal dimensions Ss-N-Pg Ss-N-Sm S-N-Ss S-N-Pg Vertical dimensions NL-ML NSL-NL NSL-ML Cranial base angle N-S-Ba Incisor relationship Overjet (mm) Overbite (mm)

Mean

7.04 7.98 81.14 75.09 30.45 8.49 38.93 132.44 10.03 1.97

2.39 1.83 3.85 4.04 3.46 3.46 9.64 5.52 2.95 3.83

1.58 2.14 81.64 80.12 22.32 7.41 29.71 130.99 2.82 2.30

1.92 1.59 2.97 3.41 3.13 3.02 4.81 4.61 0.73 0.96

* * NS * * NS * NS * NS

NS NS NS NS

NS

NS NS NS

*P .001; unpaired t test. P .05; women larger than men; unpaired t test. NS, not signicant; unpaired t test.

tal maxillary overjet group were (1) 18 to 42 years of age, (2) no history of orthodontic treatment during childhood, (3) skeletal horizontal maxillary overjet (sagittal jaw relationship larger than 1 SD as described by Bjrk7 and assessed by lateral radiographs of each patient), (4) at least 24 permanent teeth, (5) no craniofacial anomalies or systemic muscle or joint disorders, and (6) availability of a prole radiograph before surgical orthodontic treatment with the rst 5 cervical vertebrae visible. Thirty-four prole radiographs were systematically selected according to these inclusion criteria from patients registered since 1975 in the orthodontic surgical patient archive (378 records) at the Department of Orthodontics, School of Dentistry, University of Copenhagen in Denmark. The sagittal jaw relationships were between 4.5 and 12.67 (mean, 7.98), the horizontal overjets were 5.47 to 15.29 mm (mean, 10.03 mm), and the vertical jaw relationships were 15.00 to 43.10 (mean, 30.45) (Table I). The control group consisted of 21 subjects: 15 women (ages, 23-40 years; mean, 29.2) and 6 men (ages, 25-44 years; mean, 32.8). The subjects were students and staff members at the Aarhus School of Dentistry in Aarhus, Denmark. The selection criteria were (1) neutral occlusion or minor malocclusion not requiring orthodontic treatment according to the Danish screening procedure for malocclusion entailing health risks,8,9 (2) no previous history of orthodontic treatment, (3) sagittal and vertical jaw relationship within 1 SD as described by Bjrk7 and assessed by lateral radiographs of each subject, (4) at least 24 permanent teeth, (5) no craniofacial anomalies or systemic muscle

or joint disorders, and (6) availability of a prole radiograph with the rst 5 cervical vertebrae visible. The sagittal jaw relationships ranged from 0.60 and 5.40 (mean, 2.15), the horizontal overjets were 1.50 to 4.70 mm (mean, 2.82 mm), and the vertical jaw relationships were between 18.00 and 28.20 (mean, 22.32) (Table I). The differences in mean values for the craniofacial dimensions between the 2 groups and the sexes are shown in Table I. The morphology of the cervical column was assessed from visual inspection of the rst 5 cervical vertebrae (C1-C5) as they are normally seen on a standardized lateral skull radiograph. Characteristics of the cervical column were classied according to the method of Sandham2 and divided into 2 categories: posterior arch deciency and fusion anomalies. Posterior arch deciency consisted of partial cleft and dehiscence. Fusion anomalies were registered in subjects with fusions of 2 cervical bodies, block fusion when more than 2 bodies were fused, and occipitalization of C1 and the occipital bone. Only anomalies that were veried on the later prole radiographs after surgery were considered anomalies of the cervical column.
Craniofacial dimensions

For the control group, the prole radiographs were taken with the teeth in occlusion and standardized head posturethe mirror positionas described by Siersbk-Nielsen and Solow.10 The radiographs were taken at the Department of Oral Radiology, Aarhus School of

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nial base, and vertical and sagittal craniofacial dimensions was assessed by remeasurement of 20 lateral radiographs selected at random from the previously recorded radiographs. The radiographs were digitized again, and the differences between the 2 sets of recordings were calculated. No signicant differences between the 2 sets of recordings were found by paired t test. The method errors calculated by Dahlbergs formula13 ranged from 0.09 to 0.69, and the Houston reliability coefcients were from 0.99 to 1.00.14 The reliability was within the same range as for traditional lm-based radiographs.15
Statistical analysis

Fig 1. Reference points and lines according to the method of Solow and Tallgren.28

Dentistry, in a Bucky Conds cephalometer (Petersen and Schmidt, Copenhagen, Denmark) with a lm-tofocus distance of 180 cm and a lm-to-median plane distance of 10 cm. No correction was made for the constant linear enlargement of 5.6%. A plumb line was suspended from the ceiling to mark the true vertical line on the radiographs. The digital radiography system was photostimulable phosphor plate, Digora (Soredex, Helsinki, Finland), placed in a traditional 24 30-cm cassette without intensifying screen. The reference points were marked and digitized in PorDias for Windows (version 6; Institute for Orthodontic Computer Science, Middelfart, Denmark) (Fig 1), and 9 variables representing the cranial base angle and the vertical and sagittal craniofacial dimensions were calculated. For the horizontal maxillary overjet group, the 34 prole radiographs were taken in a cephalostat with a lm-to-focus distance of 180 cm and a lm-to-median plane distance of 10 cm. No correction was made for the constant linear enlargement of 5.6%.11 The variables are listed in Table I. The reliability of the visual assessment of the morphological characteristics of the cervical vertebrae was determined by interobserver examinations between the authors. The interobserver examinations showed very good agreement (0.82) as assessed by the kappa coefcient.12 The reliability of the variables describing the cra-

The normality of the distributions was assessed by the parameters of skewness and kurtosis and by the Shapiro-Wilks W test. The cephalometric measurements were normally distributed except for overjet. For the craniofacial dimensions, the effect of age was assessed by linear regression analysis and, for morphological characteristics of the cervical column, by logistic regression analysis. Differences in the means of the craniofacial dimensions between sexes and groups were assessed with the unpaired t test. Differences in the occurrence of morphological characteristics of the cervical column between sexes and groups were assessed with the Fisher exact test. Associations between the morphology of the cervical column and each craniofacial dimension were expressed in terms of Nagalkerke16 logistic regression correlation coefcients (R2) and tested for the possible effects of age and sex by multiple logistic regression analyses. A multiple logistic regression analysis with stepwise backward elimination was then performed to determine the relationship between the morphology of the cervical column as the dependent variable and the variables that were signicantly correlated with the morphology of the cervical column as the independent variables. The multiple correlation coefcients (R2) (R R2) in the logistic regression analysis were calculated according to the method of Nagelkerke.16 In all logistic regression models, the linearity of the effect was tested with the HosmerLemeshow goodness-of-t test. The results were considered signicant at P .05. The statistical analyses were performed with SPSS software (version 13.00; SPSS, Chicago, Ill).
RESULTS

In the overjet group, 52.9% had fusion of the cervical column, and 5.9% had posterior arch deciency (Table II). The fusion always occurred between C2 and C3, and posterior arch deciency always occurred in combination with fusion (Fig 2). No statis-

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Table II.

Prevalence of morphological characteristics of cervical column in patients with horizontal maxillary overjet (overjet group) and subjects with neutral occlusion and normal craniofacial morphology (control group)
Overjet group Control group n 18 3 1 1 % 85.7 14.3 4.8 4.8 P * * NS NS

Table III. Signicant correlations (R) between morphology of cervical column and mandibulary prognathism (S-N-Pg), inclination of the maxilla (NSL-NL), cranial base angle (N-S-Ba) and overjet in the total group (n 55) Fusion S-N-Pg NSL-NL N-S-Ba Overjet .36* NS .36* .35* Posterior arch deciency NS .54* .65* NS More than 1 deviation NS .54* .65* NS

Variable Normal Fusion anomalies Posterior arch deciency More than 1 deviation

n 16 18 2 2

% 47.1 52.9 5.9 5.9

*P 0.1; Fisher exact test. NS, not signicant; Fisher exact text.

*P .05; logistic regression. NS, not signicant; logistic regression.

logical characteristics of the cervical column (women, 13.3%; men, 16.7%). The comparison of the overjet group and the control group showed that the morphological deviations of the cervical column occurred signicantly more often in the overjet group (P .01, Table II).
Craniofacial dimensions related to the cervical column morphology

Fig 2. Morphological characteristics of the cervical column in patients with skeletal horizontal overjet illustrated by radiographs and graphic drawings: 1, fusion of C2 and C3 (fusion anomalies); 2, partial cleft of the posterior portion of the neural arch of atlas (posterior arch deciency).

In the total group, the correlation analysis showed that mandibular retrognathia (S-N-Pg, P .05), large cranial base angle (N-S-Ba, P .05), and large horizontal overjet (P .05) were signicantly correlated with fusion of the cervical column. These associations were not due to the effect of age or sex. Posterior arch deciency was signicantly positively correlated with maxillary inclination (NSL-NL, P .05) and cranial base angle (N-S-Ba, P .05). The signicant regression coefcients (R) were low to moderate, with numerical values from 0.35 to 0.65 (Table III). The multiple logistic regression analysis showed that the most important factors for fusion of the cervical column were cranial base angle (P .05) and horizontal overjet (P .05) (R2 0.22, R 0.47). Multiple logistic regression analysis for posterior arch deciency was not included in the analyses because of its low prevalence.
DISCUSSION

tical sex differences were found in the occurrence of morphological characteristics of the cervical column (women, 46.4%; men, 83.0%) even though the sex difference was large. As previously reported, in the control group, 14.3% had fusion of the cervical column, and 4.8% had fusion and posterior arch deciency (Table II).1 The fusion always occurred between C2 and C3. No statistical sex differences were found in the occurrence of morpho-

The morphological deviations of the cervical column, which have not previously been described on lateral radiographs or by either computed tomography scan or magnetic resonance imaging, occurred signicantly more often in the overjet group (52.9%) compared not only with the control group but also with a group of patients with skeletal deepbite (41.%),5 whereas the prevalences were greater in patients with

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skeletal mandibular overjet (61.4%)6 and patients with condylar hypoplasia (72.7%).1 Because the prevalence of morphological cervical column deviations differs in groups with skeletal craniofacial morphology deviations and malocclusion traits, the pattern of cervical column morphology was the same as seen in the controls and a group of patients with skeletal deepbite.5 In these groups, the fusions always occurred between C2 and C3. The pattern in patients with skeletal mandibular overjet and patients with condylar hypoplasia was different. In the patients with condylar hypoplasia, 9% of the fusions occurred between C3 and C4,1 and, in the mandibular overjet group, 3.5% of the fusions were block fusions.6 As a conclusion from this comparison, the cervical column differs phenotypically in the various skeletal malocclusion traits. Body fusions occurred in the deepbite, control, and horizontal maxillary overjet groups at the same cervical region but with different prevalences, whereas, in patients with mandibular overjet, the malformations are located in the same region, but block fusion occurs. It is not known why these malformations occur in the cervical column and why they occur with different frequencies. Also, the different patterns in groups of patients with varied skeletal craniofacial morphologies and malocclusion traits are inexplicable. In the prenatal period, the vertebral bodies were formed around the notochord, and thus the notochord might be responsible for their location and morphology.17-20 Previous studies also found that different genes act in different regions,21-24 and this might be the focus of future studies on the pathogenesis.
Associations

cervical vertebrae, especially the vertebral bodies, but also the basilar part of the occipital bone, which is the posterior part of the cranial base angle,17-20,25-27 it is understandable, as seen in this study, that the cranial base angle is associated with malformations in the cervical vertebrae. The mesoderm forming the vertebral arches and the remaining parts of the occipital bone is also formed from notochordal inductions. In this study, we found an association between posterior arch deciency as partial cleft of the vertebral arches and the cranial base angle and the maxillary inclination. Because the maxilla is attached to the inferior cranial base,7 it could be presumed that also the inclination of the anterior part of the cranial base deviates in horizontal skeletal overjets. Future molecular genetic studies and prenatal insight into normal and pathologic associations between development in the cranial base, the jaws, and the cervical region might be essential to subdivide maxillary overjets and thereby explain the etiology of skeletal deviations in the craniofacial prole. The clinical application of this phenotypic differentiation of maxillary overjets is a more accurate diagnosis that might help to determine the correct treatment for these patients.
CONCLUSIONS

In this study, mandibular retrognathia, cranial base angle, and horizontal overjet were correlated with fusion of the cervical column. This means that patients with skeletal horizontal overjet are most likely to have fusion anomalies if the horizontal overjet is caused by mandibular retrognathia and a large cranial base angle and not by maxillary prognathia. This agrees with a previous study that found that patients with skeletal mandibular overjet were more likely to have fusion anomalies if the mandibular overjet was caused by maxillary retrognathia and not by mandibular prognathia.6 This could indicate that fusions of the cervical column are more likely to be associated with retrognathia of the jaws in general instead of prognathia of the jaws. We found that the craniofacial parameters most important for the fusions of the cervical vertebral bodies were cranial base angle and horizontal overjet. Because the notochord determines the development of not only the

In the overjet group, 52.9% had fusion of the cervical column, and 5.9% had posterior arch deciency. The morphological deviations of the cervical column occurred signicantly more often in the overjet group than in the control group, whereas the pattern of morphological deviations of the cervical column was the same in both groups. Associations were found between fusions of the cervical column and mandibular retrognathia, large cranial base angle, and large horizontal overjet, and between posterior arch deciency and large maxillary inclination and cranial base angle. The craniofacial parameters most important for the fusions were cranial base angle and horizontal overjet. Our ndings differ from previous studies on prole radiographs of skeletal mandibular overjet and skeletal deepbite and subjects with condylar hypoplasia. Molecular genetic studies and prenatal insight into normal and pathologic associations between development in the cranial base, the jaws, and the cervical region might be necessary to explain the etiology of skeletal deviations in the craniofacial prole. We thank the students and staff at the Aarhus School of Dentistry, Aarhus University; Jan Hesselberg Madsen, specialist in orthodontics, coordinator of the

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treatment of orthodontic surgical patients at the Department of Orthodontics, University of Copenhagen; and Maria Kvetny for linguistic support and manuscript preparation.
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