An evaluation and correlation of airway space of pharynx, mandibular morphology, and tongue volume in skeletal classes and facial patterns – A cone beam computed tomography study

INTRODUCTION

The pharynx is a critical structure in the human respiratory system that not only has a significant role in deglutition and respiration but also has a crucial role in the growth and development of bones of craniofacial regions.^[1,2] Any abnormalities in the soft tissue and craniofacial skeleton can change the pharyngeal airway system as a result of the posterior position of the mandible or maxillary retrognathism not only induces airway insufficiency and mouth breathing but also results in downward rotation of mandible, tongue, and extension of the head.^[3,4] Furthermore, an extended head position and lowered tongue posture increase the mandibular load due to stretching of facial musculature, resulting in upright incisors and narrow arches, and predominantly, such features are seen in hyperdivergent growth patterns.^[5,6]

According to “soft tissue stretching hypothesis”^[7,8] stated that alterations in the normal naso-respiratory processes due to stretching of soft tissues oro-pharyngeal area have an extreme impact on the craniofacial development, especially during the period of active growth when a patient approaches for orthodontic treatment.^[6,9,10]

Previous studies showed that growing individuals with Class II malocclusion had a constricted pharyngeal area, mainly of the oropharynx and hypopharynx, in comparison to Class I malocclusion.^[1-3,10] Furthermore, skeletal movements during orthognathic surgeries do have an effect on the surrounding structures, such as maxillo-mandibular advancement procedures that result in movement of the posterior of the tongue, soft palate, hyoid bone, and frontal pharyngeal structures anteriorly. Similarly, any mandibular setback surgeries are also associated with the narrowing of the pharyngeal space. ^[11,12]

Recent advancements in the field of technologies and healthcare systems, like the use of cone-beam computed tomography (CBCT), have overtaken the previous 2-D methods or procedures. These CBCT multiplanar reconstructions (MPRs) and 3D evaluations provide data that are more accurate and reduce radiation dose.^[13-15]

Considering the significance of determining the morphology of the pharyngeal airway in different facial skeletal patterns and its effect on treatment planning, this study was carried out to evaluate and correlate pharyngeal airway space, mandibular morphology, and tongue volume in individuals with various skeletal classes and facial patterns.

MATERIAL AND METHODS

Inclusion criteria

The individuals were selected based on the inclusion criteria, i.e., healthy individuals in an age range of 18–20 years before orthodontic treatment or orthognathic surgery. The samples were classified into 3 skeletal classes: Class I, Class II, and Class III (40/group). Each class was further subdivided into two subgroups (20/subgroup) as hyperdivergent and hypodivergent, respectively as shown in Flowchart 1 below.

Close

Flowchart 1:

Distribution of the samples.

Export to PPT

Procedure

CBCT volumes were captured (Kavo 3D Pro imaging system, Palodex group OY, Finland) at 120 kV, 10mA, field of view of 13 × 15 cm, voxel size of 0.4 mm, and scanning time of 40 s. The CBCT images were acquired with every individual seated in the upright position and with the eyeear plane parallel to the floor and the teeth of the patients in the maximal intercuspal position. The pre-treatment digital lateral cephalometric images were collected (CS IMAGING TECHNIQUE CS 8100 Rochester, NY USA). Digital Images (DICOM format) were exported to FACAD software (Version 3.10.1 Swedish Company, Ilexis AB Linkoping, SWEDEN) to classify into various classes and facial patterns.

The skeletal class was determined based on ANB, SNA, and SNB angle, while the facial pattern was differentiated as hypodivergent and hyperdivergent groups by calculating the VERT index of Rickets.^[17]

The CBCT DICOM files were transferred to on-demand 3D software (version 1.0.10.746; CybeMed, Seoul, South Korea) for conversion to volumetric 3D MPR. For pharyngeal airway analysis, the reference line vertically was placed in the median sagittal plane, and the horizontal reference line was placed from the anterior nasal spine (ANS) to the posterior nasal spine (PNS) to reconstruct in axial and sagittal planes. Considering the mandible, the horizontal reference line was placed tangent to the lower border of the mandible for reconstruction in the sagittal plane and then extended to the genial tubercle in the superior direction [Figure 1a-d].^[1]

Close

Figure 1:

Parameters for pharyngeal airway analysis (a) Determine the reference planes sagitally, as the distance from anterior nasal spine to posterior nasal spine as CV1 plane. Cv1 to CV2 as Oropharynx and CV2 to Cv4 as Hypopharynx; (b) Constricted distance; (c) largest transverse width and anteroposterior length determines the anatomic characteristics of the upper airway and cross-section area on axial plane. Largest transverse width, anteroposterior length; (d) Gonial angle of mandible.

Export to PPT

The analysis of the pharyngeal space volume (PSV) was accomplished from a 3D model. From the reconstructed 3D model, PVS was measured in mm³. PSV was evaluated by exporting the CBCT DICOM files to the ITK-SNAP software (version 3.8.0; Cognitica, Philadelphia, Pa; www.itksnap.org). From the MPR of images, the 3D models of the volume of the oropharynx and hypopharynx were reconstructed by utilizing the semi-automated segmented mode of the ITK-SNAP software.

The PSV in this research relates to the fusion between the oropharynx and the hypopharynx. Thus, we established the anatomic borderline according to Park et al.,^[1,18] i.e., superiorly by taking a reference line at the right angle to midsagittal plane traced from the posterior-most point of the palatal plane (ANS-PNS) to the inferior most point of the C1 (first cervical vertebra) as CV1 plane and the anterior-inferior most point of the C2 (2^nd cervical vertebra) as CV2 plane, similarly, CV3 plane and CV4 plane.^[1] Based on these reference planes, the upper airway is divided into the oropharynx (between the CV1 and CV2 planes) and the hypopharynx (between the CV2 and CV4 planes) [Figure 1a]. Assessments of the anatomical parameters of the upper airway were measured as the largest transverse width, anteroposterior length, and cross-sectional area on the axial plane as shown in [Figures 1c, 2 and 3]. Parametres for measurement of mandibular morphology was shown in [Figure 4].

Close

Figure 2:

Parameters for pharyngeal airway analysis at the level of cervical vertebrae and epiglottis (a) interspace at C1, interspace at C1 anterioposteriorly, (b) interspace at C2 and interspace at C2 anterioposterioly, (c) interspace at C3 and Interspace at C3 anterioposteriorly, (d) Interspace at epiglottis and Interspace at epiglottis anterioposteriorly

Export to PPT

Close

Figure 3:

Segmentation of pharyngeal space described in the red text represents the 3D volume of union between the oropharynx and the hypopharynx.

Export to PPT

Close

Figure 4:

Parameters for mandibular morphology analysis (a) Inter-distance of mandible; (b) anterior-posterior distance of mandible; (c) Transverse angle of mandible.

Export to PPT

Boundaries to measure tongue volume were identified as the cementoenamel junction of posterior teeth (first molar and premolars) parallel to the X-axis plane both sagittally and axially, defining the ventral aspect of the tongue for segmentation. A plane at the right angle from the PNS in the axial orientation is defined to form the posterior aspect of the tongue for segmentation on the axial view. The occlusal plane was defined from the central cusps of the lower first molar to the incisal edge of the incisors for volume analysis, as shown in [Figure 5].

Close

Figure 5:

Segmentation of the tongue described in red text represents the 3D volume of tongue.

Export to PPT

As the tongue is a soft tissue, for each patient, Hounsfield values (−650–200 HU) were set to calculate the maximum amount of voxel. According to the Hounsfield values chosen initially, the above-defined borders for the tongue were then added to form a three-dimensional mask of the volume of the tongue.

Volumetric analysis of the tongue was determined by utilizing the voxel volume from the scan and the number of voxels taken for a specific mask. To rule out inter-investigator variance, the same investigator determined all the parameters 2 times with a 1-week interval. To determine the reproducibility of the measured parameters, the intra-class correlation coefficient was calculated.^[19]

The parameters analyzed are represented in [Tables 1 and 2].

Table 1: Parameters for pharyngeal airway analysis.

Parameters	Definition of Parameters	Reconstructed plane
Pharyngeal space dimensions
ANS to PNS distance [Figure 1a]	Linear distance from the anterior most to posterior most point on the palatal plane.	Sagittal
Constricted distance [Figure 2b]	Linear distance from the narrowest area of pharyngeal space horizontally	Sagittal
Intrerspace at C1 (lateral to lateral [LLC1]) [Figure 2a]	Linear distance horizontally from the greatest lateral to lateral measurement of pharyngeal space situated at the lowermost point at C1	Axial
Interspace at C1 anterioposteriorly (APC1)[Figure 2a]	Linear distance vertically from the greatest measurement anterioposteriorly of pharyngeal space situated at the lowermost point at C1	Axial
Interspace at C2 (lateral to lateral [LLC2]) [Figure 2b]	Linear distance in horizontal direction from the greatest laterallateral measurement of pharyngeal space situated at the lowermost point at C2	Axial
Interspace at C2 anterioposteriorly (APC2) [Figure 2b]	Linear distance vertically from the greatest measurement anterioposteriorly of pharyngeal space situated at the lowermost point at C2	Axial
Interspace at C3 (lateral to lateral [LLC3]) [Figure 2c]	Linear distance horizontally from the greatest lateral to lateral measurement of pharyngeal space situated at the lowermost point at C3	Axial
Interspace at C3 anterioposteriorly [APC3][Figure 2c]	Linear distance vertically from the greatest measurement anterioposteriorly of pharyngeal space situated at the lowermost point at C3	Axial
Interspace at epiglottis (lateral to lateral [Epiglotiss-LL]) [Figure 2d]	Linear distance horizontally from the greatest lateral to lateral measurement of pharyngeal space situated at the point of maximum concavity of the stalk of the epiglottis.	Axial
Interspace at epiglottisanterioposteriorly (Epiglottis-AP) [Figure 2d]	Linear distance vertically from the greatest measurement anterioposteriorly of pharyngeal space situated at the point of maximum concavity of stalk of the epiglottis.	Axial

ANS: Anterior nasal spine, PNS: Posterior nasal spine

Table 2: Parameters for mandibular morphology and tongue volume analysis.

Gonial angle [Figure 1d]	Angular measurement between the line from condylion to gonion and the line tangent to lower border of the mandible.	Sagittal
Interdistance of mandible (LL) [Figure 4a]	Linear distance from the point of one gonion to the point of contralateral gonion.	Axial
Sagittal distance of mandible (AP) [Figure 4b]	Vertical line from the anterior most point on the lingual aspect of the mandibular symphysis to a line between both sides of the gonion points	Axial
Transverse mandibular angle. [Figure 4c]	Angular measurement between the anterior most point on the mental protuberance and the gonion point on both sides of the mandible.	Axial
Tongue volume (mm3) [Figure 5]	Segmentation of the tongue on the ventral aspect: e cervical margin of mandibular posterior teeth will be rotated on the sagittal view in such a manner that the above plane will be parallel to the xaxis plane Segmentation of the tongue on the axial aspect: A right angle plane declining from the PNS in the axial direction will be considered to form the base of the tongue

PNS: Posterior nasal spine

RESULTS

The intra-examiner intraclass correlation showed values between 0.76 and 0.97 for the angular measurements. The distribution of skeletal Classes is shown in [Table 3]. There were statistically significant differences in all the measured variables (P < 0.001) except for the gonial angle of the mandible, which showed statistically insignificant with P = 0.675.

The distribution of variables in different facial types, which showed highly significant differences (P < 0.001) while tongue volume showed a statistically significant difference at P < 0.05 whereas ANS-PNS, C1-LL distance, C1-AP distance, LL distance of mandible, and AP distance of mandible showed no statistically significant differences (P < 0.05) with P = 0.223, 0.067, 0.123, 0.475, and 0.37, respectively is showed in [Table 4].

As shown in [Table 5], a significant correlation was found between the PSV and the measured variables. In both facial types, the correlation between the parameter’s airway volume and ANS-PNS shows a negative correlation and is statistically significant for P < 0.001 for the hypodivergent pattern (−0.456).

In class III hypodivergent, the correlation between the airway volume and shortest distance (0.726, 0.585, respectively) shows a very good positive correlation and is significant with a P < 0.001. Correlation between the airway volume and transverse angle of the mandible shows excellent negative correlation (−0.409, −0.771, −0.605, −0.706, −0.542, respectively) for class II and class III skeletal classes and both facial types and is statistically significant for P < 0.001.

The correlation between the parameters airway volume and tongue volume (0.921, 0.931, 0.984, and 0.964, respectively) shows an excellent positive correlation and is significant with a P < 0.001 for class II and class III skeletal pattern and in both facial types.

The results of the intergroup comparison of skeletal classes with hypodivergent growth pattern are shown in [Table 6], and all variables showed statistically significant differences (P < 0.001), the following variables showed significantly higher values for the shortest/constricted distance (8.420 ± 0.5307), C1-LL (28.130 ± 0.7935), C1-AP (10.960 ± 1.5581), C2-LL (27.980 ± 1.9509), C2-AP (10.960 ± 2.0423), C3-LL (30.450 ± 1.0566), C3-AP (11.080 ± 1.7392), epiglottis-LL (35.550 ± 3.0050), epiglottis-AP (12.390 ± 1.5), airway volume (12310.140 ± 858.6), gonial angle (118.0 ± 2.15), inter-distance of the mandible (84.320 ± 0.69), and tongue volume (51271.300 ± 1104.7) in Class III in comparison with class I and class II.

ANS-PNS (47.8 ± 1.7205) and transverse mandibular angle (62.300 ± 0.7211) showed significantly higher values in Class II compared to Class I and Class III in the hypodivergent growth pattern. Interdistance of the mandible (87.680 ± 0.92) showed significantly higher values for class I compared to class II and class III hypodivergent patterns.

As shown in [Table 7], comparison of skeletal classes with hyperdivergent growth pattern showed statistically higher values for shortest distance, C1-LL, C1-AP, C2-LL, C2-AP, C3-LL, C3-AP, epiglottis-LL, epiglottis-AP, airway volume, and tongue volume in class III compared to class I and class II. ANS-PNS, transverse mandibular angle, and AP mandibular distance showed significantly higher values in class II in comparison with class I and class III. AP-mandible distance showed significantly higher values for class I in comparison with class III and class II.

DISCUSSION

The influence of respiration on the growth of craniofacial structure and its significance in treatment planning has been a controversial topic in the field of orthodontics.^[2,7,20] Previous studies have stated that abnormal development of the maxilla-mandibular structures can result in modification of the pharyngeal airway volume, which could lead to changes in soft and hard tissue structures like hyoid bone.^[21-23]

Previous study has reported that pharyngeal tissues exhibit growth till the age of 13 years.^[10] Most of the longitudinal studies have reported that the muscular palate increases in height and depth between 20 and 50 years. ^[10,24] Many investigators have utilized lateral cephalometric analysis to evaluate the pharyngeal airway space, identifying the definite hard and soft-tissue landmarks. A major disadvantage is that it lacks accurate description and characteristics of pharyngeal airway space. In this study, we used 3D CBCT imaging technology, which helped us to understand and visualize the 3D airway volume in a better way.^[25] Previous studies have reported adaptations in the PSV, such as extended or forwarded head posture, skeletal classes, and facial patterns^[26-28], while few authors have assessed the pharyngeal volume in different skeletal classes, although the consequence was questionable.^[6,14,29] Kormaz et al.^[30] reported no significant difference in cranio-cervical angulation among obese and non-obese subjects without OSA, which might probably influence the head posture, according to body mass index (BMI). From this, we can conclude that there is no significant effect of BMI on the pharyngeal airway.

According to Jayaratne and Zwahlen,^[31] there was a significantly larger oropharyngeal volumes in skeletal class III subjects in comparison with skeletal class II subjects, which was in concordance with our research. We consider that these differences among the studies might be due to discrete methodologies, which include variable sample sizes, ethnic groups, examination procedure (2-D or 3D technique), and use of different software programs.

A study by Chianchitlert et al.,^[32] reported that subjects with retrognathic mandible exhibited a narrow pharyngeal airway space compared to individuals with normal sagittal skeletal pattern. While small and backwardly rotated mandible probably influences the tongue and the muscular palate in the posterior-inferior direction, which leads to encroach of the muscles of the pharynx in the gonial angle area with a resultant reduction in pharyngeal airway space.^[25,33] Above findings were in agreement with our study, as class II hyperdivergent subjects showed a significant negative correlation between PSV and mandibular morphological parameters . Furthermore, a study by Syal et al.^[10] stated that the position of the mandible in relationship with the cranial base has an influence on the oropharyngeal area.

Diwakar et al.^[34] claimed that there was a direct relationship between the mandibular length and, the oropharyngeal airway and the total pharyngeal airway space. These discovered a relationship between mandibular length and airway size. The present study has exhibited that class III subjects showed higher pharyngeal volume and tongue volume, followed by class I and class II subjects. Since skeletal class III subjects showed more forwardly placed mandible and tongue, thereby increasing the linear dimension between posterior aspects of the tongue and the pharyngeal posterior wall, leading to enlarged pharyngeal volume and tongue volume in class III skeletal malocclusion than compared to skeletal class I and II malocclusion.^[35] This was in agreement with studies by Kale and Buyukcavus,^[6] Laranjo and Pinho,^[36] and Habumugisha et al.^[37] They reported that retrognathic class II subjects had reduced nasal pharyngeal and adenoidal tissue.

The current study shows a substantial correlation between the pharyngeal airway capacity and craniofacial characteristics, demonstrating the relationship between form and function. In relation to facial types, a highly significant difference was established in the hyperdivergent growth pattern and hypodivergent growth pattern. Among all the groups and subgroups, the Class III hypodivergent growth pattern showed larger pharyngeal volume and smaller pharyngeal volume was found in the Class II hyperdivergent growth pattern. According to a study done by Opdebeeck et al.,^[38] the individuals with a long face have a narrower airway volume due to the reduced cross-section of the hyoid bone and backward positioning of the pharynx nearer to the cervical spine.

Another study by Kale and Buyukcavus^[6] stated that subjects with hyperdivergent pattern with Class I and Class II malocclusion had a reduced oropharyngeal airway than subject with normodivergent pattern with Class I and Class II malocclusion. Previous studies have classified variable grades of OSA by assessing linear and angular measurements in the lower jaw, hyoid bone, and pharyngeal space, and they reported that the severity of OSA is more with smaller measurements.^[29,39,40] In our research, we measured the pharyngeal space at the area of greatest constriction. The results exhibited that these measurements were lower in Class II hyperdivergent subjects.

Further, to enable the evaluation of PSV by experts without access to or knowledge of segmentation tools, a linear regression equation has been formulated using only linear measurements for the estimation of PVS. The above formula exhibited that our equation is probably helpful for airway volume assessment.

Therefore, we believe that our research has emphasized the significance of the inter-relation and compensation of morphological patterns of the mandible, tongue, and pharyngeal airway volume, and information regarding this will help in orthodontic diagnosis and treatment planning, especially for timely dentofacial orthopedic treatment interventions and need for referral to ENT specialist.

CONCLUSION

• Within the scope of the study, it is stated that there is a direct relationship between pharyngeal space, mandibular morphology, and tongue volume.

• Among all the subgroups, Class III hypodivergent showed the highest pharyngeal airway volume and tongue volume, and the least was found in Class II hyperdivergent subjects, showing the influence on pharyngeal space, mandibular morphology, and tongue position.

• Thus, recommending thorough analysis of oropharyngeal structures in a non-individualized way for orthodontic diagnosis and treatment plan to obtain stable treatment outcomes.