Cervical vertebral column morphology in patients with obstructive sleep apnoea assessed using lateral cephalograms and cone beam CT. A comparative study

Abstract

Objectives:

Few studies have described morphological deviations in obstructive sleep apnoea (OSA) patients on two-dimensional (2D) lateral cephalograms, and the reliability of 2D radiographs has been discussed. The objective is to describe the morphology of the cervical vertebral column on cone beam CT (CBCT) in adult patients with OSA and to compare 2D lateral cephalograms with three-dimensional (3D) CBCT images.

Methods:

For all 57 OSA patients, the cervical vertebral column morphology was evaluated on lateral cephalograms and CBCT images and compared according to fusion anomalies and posterior arch deficiency.

Results:

The CBCT assessment showed that 21.1% had fusion anomalies of the cervical column, i.e. fusion between two cervical vertebrae (10.5%), block fusions (8.8%) or occipitalization (1.8%). Posterior arch deficiency occurred in 14% as partial cleft of C1 and in 3.5% in combination with block fusions. The agreement between the occurrence of morphological deviations in the cervical vertebral column between lateral cephalograms and CBCT images showed good agreement (κ = 0.64).

Conclusions:

Prevalence and pattern in the cervical column morphology have now been confirmed on CBCT. The occurrence of morphological deviations in the cervical vertebral column showed good agreement between lateral cephalograms and CBCT images. This indicates that 2D lateral cephalograms (already available after indication in connection with, e.g. treatment planning) are sufficient for identifying morphological deviations in the cervical vertebral column. For a more accurate diagnosis and location of the deviations, CBCT is required. New 3D methods will suggest a need for new detailed characterization and division of deviations in cervical vertebral column morphology.

Introduction

On lateral cephalograms, deviations in the morphology of the cervical vertebral column as regards fusion anomalies and posterior arch deficiency have been described in relation to craniofacial syndromes and cleft lip and palate. Deviations such as fusion anomalies have been observed in craniosynostosis syndromes, such as Pfeiffer’s disease, Crouzon’s disease and Apert’s syndrome.^1–5 Deviations of the cervical column morphology have also been observed in Saethre–Chotzen, Klippel–Feil, Turner and Down syndromes.^6–11 Malformations of the upper cervical vertebrae have been closely investigated in patients with cleft lip and/or palate.^11–17

Deviations in the morphology of the cervical vertebral column have been described in healthy subjects with neutral occlusion¹⁸ and in patients with severe skeletal malocclusion traits, such as deep bite, open bite, maxillary overjet and mandibular overjet.^19,20–22 Furthermore, associations have been found between deviations of the cervical vertebral column morphology, the craniofacial profile and posture of the head and neck.^18–22

To the knowledge of the authors, only two studies have described the morphology of the cervical vertebral column in patients with obstructive sleep apnoea (OSA) on two-dimensional (2D) lateral cephalograms.^23,24 The prevalence of morphological deviations was 43% and 46% in the two studies, and deviations occurred significantly more often in patients with OSA than in subjects with neutral occlusion and normal craniofacial morphology.²³ Morphological deviations in the OSA patients were described as fusions between two cervical vertebrae, block fusions, occipitalization, partial cleft of C1 or dehiscence of C3 and C4.^23,24 In addition, the craniofacial profile of OSA patients with block fusions in the cervical vertebrae and fusion of two vertebrae differed significantly from the craniofacial profile of other OSA patients.²⁴

The difficulty of reliably determining morphological deviations in the cervical vertebral column on a single lateral cephalogram has been discussed in the literature.^25–27 Studies have found that some fusions observed on 2D radiographs were more likely to be “pseudofusions”, and that a more valid method such as three-dimensional (3D) radiographs [CT or cone beam CT (CBCT)] is recommended.

Thus, the aims of the present study were: (1) to describe the morphology of the cervical vertebral column observed on CBCT in adult patients with OSA; and (2) to compare the cervical vertebral column morphology observed on 2D lateral cephalograms with that observed on 3D CBCTs.

Materials and methods

The OSA group comprised 20 females, aged 26–72 years (mean age 54.6 years), and 37 males, aged 33–76 years (mean age 49.7 years). The patients are the first 57 patients enrolled as part of a longitudinal sleep apnoea study at the Orthodontics Section, Department of Odontology, Copenhagen, Denmark, in the period October 2011–October 2012. The patients were diagnosed with OSA by sleep studies, using overnight polysomnography. The apnoea–hypopnoea index (AHI) ranged between 2 and 57 (mean 16.6). The study has been approved by the Ethical Committee for Copenhagen, Denmark (ref. no. H-3-2011-086) and the Danish Data Protection Agency (J. no. 2012-54-0041).

Lateral cephalograms and cone beam CTs

The lateral cephalograms and CBCTs were taken with the teeth in occlusion and in the standardized head posture in the self-balance position as described by Siersbaek-Nielsen and Solow.²⁸ The radiographs were taken at the Radiology Section, Department of Odontology, Copenhagen, Denmark.

The lateral cephalograms were taken with a Philips MEDIO 30 CP X-ray tube (Philips, Eindhoven, Netherlands) in a cephalostat with a receptor-to-focus distance of 180 cm and a receptor-to-median plane distance of 10 cm. An aluminium wedge was placed at the collimator of the X-ray tube. The exposure parameters were 70 kV, 4 mAs and 12 ms. No correction was made for the constant linear enlargement of 5.6%. The profile radiographs were taken with a photostimulable phosphor plate system, Digora PCT (Soredex, Tuusula, Finland).

The CBCTs were taken in a NewTom VGi unit (QR srl, Verona, Italy). The settings were as follows: standard scan mode with an imaging volume of 15 × 15 cm², exposure time of 18 s and axial thickness of 0.3 mm. The 3D images of the cervical vertebrae were analysed for morphological deviations in the cervical vertebral column using the NewTom NNT software (QR srl, Verona, Italy).

Morphology of the cervical vertebrae

The visual assessment of the cervical column included the first five cervical vertebral units, normally seen on a standardized lateral skull radiograph. Characteristics of the cervical column were described according to Sandham²⁹ and divided into either fusion anomalies or posterior arch deficiency. Accordingly, no differentiations were made between congenital and degenerative morphological changes. If any doubt occurred regarding the category, the region under consideration was registered as having normal morphology.

Fusion anomalies are defined as fusion, block fusion and occipitalization. Fusion is defined as fusion of one unit with another at the articulation facets, neural arch or transverse processes. Occipitalization is defined as assimilation, either partially or completely, of the atlas (C1) with the occipital bone. The definition of block fusion was modified according to Sonnesen and Kjaer¹⁹ and defined as fusion of more than two units at the vertebral bodies, articulation facets, neural arch or transverse processes.

Posterior arch deficiency includes partial cleft and dehiscence.²⁹ Partial cleft is defined as the failure to fuse the posterior part of the neural arch. Dehiscence is defined as the failure to develop a part of the vertebral unit.

One author (LS) described the morphological deviations on the lateral cephalograms and another author (KEJ) described the CBCT images in a blinded fashion. Both authors have extensive experience in describing the morphology of the cervical vertebral column on cephalograms and CBCT images, respectively.

Statistical methods

For the occurrence of morphological deviations of the cervical column, differences between gender and between lateral cephalograms and CBCT images were assessed using Fisher’s exact test and Mann–Whitney U test. The effect of age and AHI was tested by logistic regression analysis. The interobserver agreement between lateral cephalograms and CBCT images were assessed using the kappa coefficient (κ).³⁰ The results from the tests were considered to be significant at p < 0.05. The statistical analyses were performed using SPSS^® v. 20.00 (SPSS Inc., Chicago, IL).

Results

Reliability

The reliability of the visual assessment on the CBCT images was determined by interobserver examination between two authors (LS and KEJ) and showed “very good” agreement (κ = 0.92), as assessed using the kappa coefficient.³⁰ The interobserver agreement on the lateral cephalograms has previously been reported (κ = 0.82).¹⁹

Cone beam CT

Assessment of 3D CBCT showed that 31.6% had morphological deviations of the cervical vertebral column, such as fusion anomalies or posterior arch deficiency (Table 1). Fusion anomalies occurred in 21.1% as fusions either between C2 and C3 or C3 and C4 (10.5%; Figure 1) or as block fusions (8.8%) between C2, C3 and C4 or between C3, C4 and C5 (Figure 2). Occipitalization occurred in 1.8% on one side. The fusions were located between the vertebral bodies or between the articulatory facets, either unilaterally or bilaterally. Posterior arch deficiency occurred in 14%, always as partial cleft of C1, and in 3.5% in combination with block fusions (Figure 2).

Table 1.

Prevalence of morphological deviations of the cervical vertebral column in patients with obstructive sleep apnoea assessed using lateral cephalograms (2D) and cone beam CT images (3D)

	2D	3D
Variables	n (%)	n (%)	p
Normal	38 (66.7)	39 (68.4)	NS
Fusion anomalies	13 (22.8)	12 (21.1)	NS
Fusion	9 (15.8)	6 (10.5)	NS
Block fusion	4 (7.0)	5 (8.8)	NS
Occipitalization	0 (0.0)	1 (1.8)	NS
Posterior arch deficiency	7 (12.3)	8 (14.0)	NS
Partial cleft	7 (12.3)	8 (14.0)	NS
Dehiscence	0 (0.0)	0 (0.0)	NS
More than one deviation	1 (1.8)	2 (3.5)	NS

2D, two-dimensional; 3D, three-dimensional; NS, not significant.

Figure 1.

Cervical vertebral column morphology in the same patient seen on a lateral cephalogram (a) and on cone beam CT images (b–e) marked by arrows. (a) Fusion between C2 and C3 at the vertebral bodies and at the articulatory facets, (b) in the right sagittal view, (c) in the coronal view, (d) in the left sagittal view and (e) in the midsagittal view

Figure 2.

Cervical vertebral column morphology in the same patient seen on a lateral cephalogram (a) and on cone beam CT images (b–f) marked by arrows. (a) Partial cleft of C1 and block fusion between C2, C3 and C4. (b) Block fusion between C2, C3 and C4 in the right sagittal view, (c) on both sides in the coronal view, (d) in the left sagittal view, (e) partial cleft of C1 in the axial view and (f) in the coronal view

No statistical effect of age was found in the occurrence of morphological deviations of the cervical column in females, but in males the occurrence of morphological deviations increased significantly with age (p = 0.024). No statistical effect of AHI or gender was found in the occurrence of morphological deviations of the cervical column (females 35% and males 29.7%).

Lateral cephalograms

The assessment of 2D lateral cephalograms showed deviations of the cervical vertebral column morphology in 33.3%, i.e. fusion anomalies or posterior arch deficiency (Table 1). Fusion anomalies occurred in 22.8% as fusions between C2 and C3 (15.8%; Figure 1) or as block fusions between C2, C3 and C4 (7.0%; Figure 2). Posterior arch deficiency occurred in 12.3%, always as partial cleft of C1, and in 1.8% in combination with block fusion (Figure 2).

No statistical effect of age, AHI or gender was found in the occurrence of morphological deviations of the cervical column (females 35% and males 32.4%).

Comparison of lateral cephalograms and CBCT images

No statistically significant differences in the occurrence of morphological deviations of the cervical column were found between lateral cephalograms and CBCT images. The agreement between the occurrence of cervical vertebral column morphological deviations seen on lateral cephalograms and CBCT images was good (κ = 0.64). Disagreements were observed in nine patients. In five patients, the morphological deviations seen on the lateral cephalograms were not verified by the CBCT images, i.e. four patients with fusions between C2 and C3 (Figure 3) and one patient with partial cleft of C1 (Figure 4). In four patients, the morphological deviations seen on the CBCT images were not seen on the lateral cephalograms, i.e. two patients with fusion between the articulatory facets in only one side (Figure 5), one patient with partial cleft of C1 and one patient with occipitalization in one side.

Figure 3.

Cervical vertebral column morphology in the same patient seen on a lateral cephalogram (a) and on cone beam CT images (b–d) marked by arrows. (a) Fusion between C2 and C3 at the articulatory facets, (b) no fusion between C2 and C3 in the sagittal right view, (c) in the coronal view and (d) in the sagittal left view

Figure 4.

Cervical vertebral column morphology in the same patient seen on a lateral cephalogram (a) and on cone beam CT images (b–d) marked by arrows. (a) Partial cleft of C1, (b) no partial cleft of C1 in the axial view, (c) in the coronal view and (d) in the right sagittal view

Figure 5.

Cervical vertebral column morphology in the same patient seen on a lateral cephalogram (a) and on cone beam CT images (b–d) marked by arrows. (a) No morphological deviations, (b) fusion between C3 and C4 at the articulatory facets in the right sagittal view, (c) in the coronal view and (d) no fusion between C3 and C4 in the left sagittal view

Discussion

This is the first time that morphological deviations in the cervical vertebral column regarding fusion anomalies and/or posterior deficiencies in patients with OSA have been described on CBCT. The cervical column morphology in adult patients with OSA has previously been examined on 2D lateral cephalograms.²³ It was found that fusion between two cervical vertebrae occurred in 26%, block fusions in 12%, occipitalization in 14%, partial cleft of C1 in 2.2% and dehiscence in 3.3%. In the present study, on 2D cephalograms and CBCT images, the prevalence was lower except from the occurrence of partial cleft, which was six times higher. Nevertheless, the pattern of morphological deviations in the cervical column was confirmed on CBCT, except that no dehiscence was found in the present study. The differences in prevalence between the two studies could be owing to the differences in AHI between the two OSA groups or to the false-positive findings on the lateral cephalograms in the previous study. In that study,²³ the AHI ranged between 5.1 and 111.7 (mean 36), and in the present study the AHI ranged between 2 and 57 (mean 16.6). In both studies, the AHI was higher in OSA patients with morphological deviations of the spine compared with OSA patients without morphological deviations, but the differences were not statistically significant. With regard to the reliability in the previous study, the interobserver evaluation showed very good agreement (κ = 0.82).²³

The reliability of C2 and C3 facet joint fusion has been discussed previously in the literature. Studies have found that some fusions observed on 2D radiographs were more likely to be pseudofusions.^25–27 Oblique orientation of the cervical facet joints relative to the X-ray beam, flexion or extension of the spine and other morphological variations could result in superposition of structures and an analogous appearance of fusion. These studies have recommended a more valid method such as 3D radiographs (CT or CBCT) for assessing fusions. In the present study, no statistically significant differences in the occurrence of morphological deviations of the cervical column were found between lateral cephalograms and CBCT images, and the agreement was κ = 0.64. This indicates that there is good agreement between the findings on the lateral cephalograms and the CBCT images. The few disagreements between lateral cephalograms and CBCT images included diagnosis of fusion between two cervical vertebrae, occipitalization and partial cleft. Furthermore, if fusion only occurred between the articulatory facets on one side, the fusion was not visible on the lateral cephalograms. The results indicate that 2D lateral cephalograms are sufficient for identifying morphological deviations of the cervical vertebral column. Meanwhile, diagnosis of morphological deviations of the cervical vertebral column cannot be the only indication for obtaining lateral cephalograms. For a more accurate diagnosis and location of morphological deviations in the cervical vertebral column, a CBCT is required. The current characterization and division of deviations in cervical vertebral column morphology is based on 2D studies from the 1980s. The new 3D methods will suggest a need for new detailed characterization and division of deviations in cervical vertebral column morphology.

The interesting deviations in prevalence and pattern in the cervical column morphology now confirmed on CBCT may prove to be a factor in the pathogenetic background for sleep apnoea and thereby contribute to the diagnosis, subdivision and treatment of patients with OSA.

So far, the complex aetiology of OSA is still not fully understood, but a number of studies have contributed to phenotypic differentiations between types of sleep apnoea. It is well known that older males with an enlarged body mass index are at risk of developing OSA.^31–33 In studies performed on 2D lateral cephalograms, specific types of craniofacial morphology and head posture, such as reduced posterior airway space, abnormally long soft palate, a low position of the hyoid bone and an extended head posture,^34–43 are also considered predisposing factors. In a previous study, an association was found between the posture of the head and neck and fusions of the upper cervical vertebrae.¹⁸ Furthermore, a recent study has shown that the craniofacial profile of OSA patients with block fusions in the cervical vertebrae and fusion of two vertebrae differed significantly from the craniofacial profile of other OSA patients.²⁴ Only one 3D CT study has described the cervical spine morphology in terms of anterior cervical osteophytes.⁴⁴ The study described two cases with degenerative disc disease with large anterior osteophytes and found that the posterior airway space was compromised at the level of the occurrences of the osteophytes.

In the present study, morphological deviation of the cervical vertebral column in patients with OSA has been confirmed on CBCT. The findings indicate that the morphological deviations of the cervical vertebrae could be a factor in the phenotypic differentiation between patients with OSA and thereby contribute to the diagnosis, subdivision and treatment of patients with OSA. Furthermore, 2D lateral cephalograms seem to be sufficient for screening of morphological deviations in the cervical vertebral column, but CBCT is required for an accurate diagnosis and location of the morphological deviations of the upper spine.