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Introduction: The purpose of this article was to evaluate the pharyngeal space volume, and the size and shape
of the mandible and the hyoid bone, as well as their relationships, in patients with different facial types and skel-
etal classes. Furthermore, we estimated the volume of the pharyngeal space with a formula using only linear
measurements. Methods: A total of 161 i-CAT Next Generation (Imaging Sciences International, Hatfield,
Pa) cone-beam computed tomography images (80 men, 81 women; ages, 21-58 years; mean age, 27 years)
were retrospectively studied. Skeletal class and facial type were determined for each patient from multiplanar
reconstructions using the NemoCeph software (Nemotec, Madrid, Spain). Linear and angular measurements
were performed using 3D imaging software (version 3.4.3; Carestream Health, Rochester, NY), and
volumetric analysis of the pharyngeal space was carried out with ITK-SNAP (version 2.4.0; Cognitica,
Philadelphia, Pa) segmentation software. For the statistics, analysis of variance and the Tukey test with a
significance level of 0.05, Pearson correlation, and linear regression were used. Results: The pharyngeal space
volume, when correlated with mandible and hyoid bone linear and angular measurements, showed significant
correlations with skeletal class or facial type. The linear regression performed to estimate the volume of the
pharyngeal space showed an R of 0.92 and an adjusted R2 of 0.8362. Conclusions: There were significant cor-
relations between pharyngeal space volume, and the mandible and hyoid bone measurements, suggesting that
the stomatognathic system should be evaluated in an integral and nonindividualized way. Furthermore, it was
possible to develop a linear regression model, resulting in a useful formula for estimating the volume of the
pharyngeal space. (Am J Orthod Dentofacial Orthop 2018;153:825-33)
C
raniofacial growth and occlusion are influenced, have a profound influence on facial development by
among other things, by the respiratory function.1 the time a patient comes for orthodontic treatment.4,5
An impaired nasal respiratory function is associ- Combined orthodontic and orthognathic surgical
ated with airway inadequacy that can result in the habit treatment has become a common modality for the
of mouth breathing.2 This change in breathing pattern correction of facial deformities. An important aspect of
leads to lowering of the mandible and the tongue, and orthognathic surgery is the effect of skeletal movements
an extended head posture.3 Changes in normal airway in the surrounding structures.6 Maxillomandibular
function during the active facial growth period can advancement leads to anterior movements of the soft
palate, base of the tongue, hyoid bone, and anterior
pharyngeal tissues, resulting in increases in the volumes
a
Department of Oral Diagnosis, Piracicaba Dental School, State University of of the nasopharynx, oropharynx, and hypopharynx, and
Campinas, Piracicaba, S~ao Paulo, Brazil.
b
therefore increasing the posterior airway space.7
Department of Pediatric Dentistry, University of Washington, Seattle, Wash.
c
Department of Physiological Sciences, Piracicaba Dental School, State University Mandibular setback surgery can cause relative narrowing
of Campinas, Piracicaba, S~ao Paulo, Brazil. of the pharyngeal airway and a significant posterior
All authors have completed and submitted the ICMJE Form for Disclosure of movement of the hyoid bone.8,9
Potential Conflicts of Interest, and none were reported.
Address correspondence to: Yuri Nejaim, Av. Limeira, 901, Arei~ao, Piracicaba, SP, The hyoid bone is connected to the pharynx,
Brazil, 13414-903; e-mail, ynejaim@hotmail.com. mandible, and cranium by muscles and ligaments. The
Submitted, January 2017; revised and accepted, September 2017. hyoid bone and its connecting muscles are also part of
0889-5406/$36.00
Ó 2018 by the American Association of Orthodontists. All rights reserved. the oropharyngeal complex. Without the hyoid bone,
https://doi.org/10.1016/j.ajodo.2017.09.018 our facility for maintaining an airway, swallowing,
825
826 Nejaim et al
Table I. Measurements
Measurement Description Reconstruction Figure
Pharyngeal space dimensions:
Anterior nasal spine-posterior nasal Line from the most anterior to the most posterior point of hard palate Sagittal 1A
spine distance
Shortest distance Horizontal line on the greatest constriction of pharyngeal space Sagittal 1B
C1- latero-lateral distance Horizontal line on the greatest latero-lateral dimension of pharyngeal space Axial 2A
oriented at the level of the most inferior point of C1
C1-anteroposterior distance Vertical line on the greatest anterior-posterior dimension of pharyngeal Axial 2A
space oriented at the level of the most inferior point of C1
C2-latero-lateral distance Horizontal line on the greatest latero-lateral dimension of pharyngeal space Axial 2B
oriented at the level of the most inferior point of C2
C2-anteroposterior distance Vertical line on the greatest anteroposterior dimension of pharyngeal space Axial 2B
oriented at the level of the most inferior point of C2
C3-latero-lateral distance Horizontal line on the greatest latero-lateral dimension of pharyngeal space Axial 2C
oriented at the level of the most inferior point of C3
C3-anteroposterior distance Vertical line on the greatest anteroposterior dimension of pharyngeal space Axial 2C
oriented at the level of the most inferior point of C3
Epiglottis-latero-lateral distance Horizontal line on the greatest latero-lateral dimension of pharyngeal space Axial 2D
oriented at the level of the most concave point of epiglottis base
Epiglottis-anteroposterior distance Vertical line on the greatest anteroposterior dimension of pharyngeal space Axial 2D
oriented at the level of the most concave point of epiglottis base
Mandible dimensions:
Anterior-posterior angle of mandible Angle between the most posterior point of the mandibular condyle, the Sagittal (MIP) 1C
gonion point and the most inferior border of the mandible body
Transverse angle of mandible Angle between the most anterior point of the mandibular symphysis and the Axial 3A
gonion point on right and left sides of the mandible
Latero-lateral distance of mandible Line between the right and left gonion points Axial 3B
Anteroposterior distance of mandible Perpendicular line from the most anterior point on the lingual surface of the Axial 3C
symphysis to a line between the right and left gonion points
Hyoid bone dimensions:
Transverse angle of hyoid bone Angle between the projections of the lines crossing the lesser and greater Axial 4A
horns of right and left sides of hyoid bone
Latero-lateral distance of hyoid bone Line between the right and left greater horns Axial 4B
Anteroposterior distance of hyoid bone Perpendicular line from the most anterior point in the concavity of the body Axial 4C
of the hyoid bone to a line between the right and left greater horns
preventing regurgitation, and maintaining the upright The aim of this study was to correlate the volume of
postural position of the head could not be controlled the pharyngeal space, the size and shape of mandible
as carefully.10 and the hyoid bone in patients with different facial types
The use of 3-dimensional (3D) imaging in dentistry, and skeletal classes. Furthermore, we estimated the vol-
more specifically cone-beam computed tomography ume of the pharyngeal space with a formula using only
(CBCT), has increased considerably in the last years, linear measurements.
making possible the evaluation of anatomic structures
and analysis of pharyngeal space morphology.11 Because MATERIAL AND METHODS
of its high spatial resolution, adequate contrast between This study was approved by the research ethics com-
the soft tissues and empty space, and the relatively low mittee of Piracicaba Dental School, State University of
radiation dose compared with multislice computed to- Campinas, in Brazil with protocol number 092/2014.
mography, CBCT is an important tool in the study of This retrospective study was performed on a batch of
craniofacial development.12,13 previously taken CBCT volumes (i-CAT Next Generation;
Due to the close relationship between the pharynx, Imaging Sciences International, Hatfield, Pa) at 120 kV,
mandible, and hyoid bone and the fact that orthodontic 5 mA, 23 3 17-cm field of view, 0.4-mm voxel, and 40-
or orthognathic interventions may affect the pharyngeal second scanning time, with indication for orthodontic
space,14 information regarding the influence of skeletal treatment or orthognathic surgery planning. The CBCT
classes and facial types on these structures would improve examinations were made with each subject sitting up-
the diagnosis and treatment of orthodontic patients. right, and with the Frankfort horizontal plane parallel
June 2018 Vol 153 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics
Nejaim et al 827
to the ground and the patient's teeth occluding in Linear and angular measurements were performed
maximum intercuspation. using the CS 3D Imaging software (version 3.4.3; Care-
A total of 161 CBCT volumes from 80 men and 81 stream Health, Rochester, NY). The linear ones were
women, aged between 21 and 58 years (mean age, anterior nasal spine-posterior nasal spine distance
27 years), were included in this study. Patients younger (ANS-PNS distance), shortest distance of the pharyngeal
than 21 years (due to incomplete development of their space (shortest distance), anteroposterior distance of the
craniofacial structures), patients who had orthognathic pharyngeal space-C1 (APC1), latero-lateral distance of
surgery, and those with pathologies in the region of the the pharyngeal space-C1 (LLC1), anteroposterior dis-
head and neck or syndromes were excluded from the study. tance of the pharyngeal space-C2 (APC2), latero-lateral
Skeletal class (Classes I, II, and III) and facial type distance of the pharyngeal space-C2 (LLC2), anteropos-
(brachycephalic, mesocephalic, and dolichocephalic) terior distance of the pharyngeal space-C3 (APC3),
were determined by an orthodontist with 13 years of latero-lateral distance of the pharyngeal space-C3
experience for each patient from multiplanar recon- (LLC3), anteroposterior distance of the pharyngeal
structions (lateral cephalometric) derived from the space-base of epiglottis (AP epiglottis), latero-lateral
CBCT images with the NemoCeph software (Nemotec, distance of the pharyngeal space-base of epiglottis (LL
Madrid, Spain). epiglottis), latero-lateral distance of mandible (LL
To determine the skeletal classes, classified as Class I, mandible), anteroposterior distance of mandible (AP
Class II, or Class III, we used the SNA, SNB, and ANB angle mandible), latero-lateral distance of hyoid bone (LL hy-
measures from the cephalometric analysis of Steiner.15 All oid bone), and anteroposterior distance of hyoid bone
patients selected as Class II had a greater value of SNA (AP hyoid bone). The angular measurements were ante-
angle (accentuated development of the maxilla), whereas roposterior angle of mandible (AP angle of mandible),
all Class III patients had an increased SNB angle (accentu- transverse angle of mandible (TA mandible), and trans-
ated development of the mandible). The measurement of verse angle of hyoid bone (TA hyoid bone). The measure-
Jarabak and Fizzell16 for line connecting point A to the ments are listed in Table I and Figures 1-4.
occlusal plane and line connecting point B to the occlusal To perform the linear measurements, all CBCT exam-
plane was used to confirm the skeletal class classification. inations were oriented according to the structures to be
With regard to facial type, differentiation into vertical measured. For pharyngeal space, the vertical reference
groups (brachyfacial, mesofacial, dolichofacial) was line was positioned in the median sagittal plane, and
determined by the VERT index (arithmetic average of 5 the horizontal line was positioned from the anterior
cephalometric measurements, angle of the facial axis, nasal spine to the posterior nasal spine in the axial and
facial depth, mandibular plane angle, lower facial sagittal reconstructions. For the mandible, the horizon-
height, and mandibular arch) as calculated in the ceph- tal line was tangentially positioned on the lower edge of
alometric analysis of Ricketts.17 With regard to the VERT the mandible in the sagittal reconstruction and then
index, a negative value corresponded to a dolichofacial moved superiorly to the genial tubercle. For the hyoid
type and a positive value to a brachyfacial type; if the bone, the software orientation line was positioned, in
value was zero, the patient was classified as mesofacial. the sagittal reconstruction, on the long axis of this bone.
American Journal of Orthodontics and Dentofacial Orthopedics June 2018 Vol 153 Issue 6
828 Nejaim et al
Fig 2. A, LLC1 and APC1; B, LLC2 and APC2; C, LLC3 and APC3; D, LL epiglottis and AP epiglottis.
The analysis of the pharyngeal space volume (PS vol- the lowest point of the first cervical vertebra, and an
ume) was carried out from the 3D model. The recon- inferior reference line traced on the most inferior point
struction of the 3D model was established with the of the fourth cervical vertebra perpendicular to the
semiautomatic segmentation mode of the software medial sagittal plane (Fig 5).
Insight ITK-SNAP (version 2.4.0; Cognitica, Philadel- One calibrated examiner (Y.N.) performed all soft-
phia, Pa), which measured the volume of the structure ware operations and measurements in a subdued and
in cubic millimeters. The volume measured in this study quiet room. The examiner executed all 18 measures 10
corresponded to the union between oropharynx and hy- times, with a 1-day interval, to assess the reproducibility
popharynx. For this, we followed the anatomic delimita- of the method. The intraclass correlation coefficient was
tions described by Park et al18 establishing a superior determined to assess the investigator's reproducibility on
reference line traced from the posterior nasal spine to the measurements.
June 2018 Vol 153 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics
Nejaim et al 829
Fig 5. A, Segmentation of the pharyngeal space using the reference points described in the text (red);
B, 3D volume of the union between oropharynx and hypopharynx.
American Journal of Orthodontics and Dentofacial Orthopedics June 2018 Vol 153 Issue 6
830 Nejaim et al
June 2018 Vol 153 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics
Nejaim et al 831
sizes, ethnicities, examination modalities (2-dimensional apnea in previous studies. These have found that the
or 3D), and software programs used. smaller the measurement, the more severe the obstruc-
Linear and angular measurements have been per- tive sleep apnea.24-26 In our study, we measured the
formed in the mandible, hyoid bone, and pharyngeal distance of greatest constriction in the pharyngeal
space to classify different degrees of obstructive sleep space. The results showed that these measurements
American Journal of Orthodontics and Dentofacial Orthopedics June 2018 Vol 153 Issue 6
832 Nejaim et al
Table V. Correlations (Pearson, rP) between PS volume and all other variables, segmented in groups (facial types or
occlusal classes) or not (total)
PS volume Total Brachyfacial Dolichofacial Mesofacial Class I Class II Class III
Transverse angle of 0.1604 0.1872 0.1962 0.0921 0.0746 0.2432 0.1051
hyoid bone (P 5 0.0421) (P 5 0.1207) (P 5 0.2378) (P 5 0.5121) (P 5 0.571) (P 5 0.0612) (P 5 0.5133)
AP hyoid bone 0.3229 0.3755 0.2397 0.2754 0.2097 0.2804 0.4316
(P \0.0001)* (P 5 0.0014)* (P 5 0.1472) (P 5 0.0459) (P 5 0.1079) (P 5 0.03)* (P 5 0.0048)*
LL hyoid bone 0.0369 0.1221 0.0422 0.0945 0.0834 0.0615 0.0451
(P 5 0.6419) (P 5 0.3138) (P 5 0.8012) (P 5 0.5011) (P 5 0.5264) (P 5 0.6406) (P 5 0.7796)
Transverse angle of 0.1398 0.1894 0.2298 0.0262 0.024 0.2253 0.013
mandible (P 5 0.077) (P 5 0.1163) (P 5 0.1652) (P 5 0.8522) (P 5 0.8556) (P 5 0.0835) (P 5 0.9355)
AP mandible 0.2907 0.339 0.3534 0.1191 0.0124 0.4292 0.0979
(P 5 0.0002)* (P 5 0.0041)* (P 5 0.0295)* (P 5 0.3955) (P 5 0.9252) (P 5 0.0006)* (P 5 0.5425)
LL mandible 0.2594 0.3328 0.0652 0.2274 0.217 0.2288 0.1102
(P 5 0.0009)* (P 5 0.0049)* (P 5 0.6974) (P 5 0.1016) (P 5 0.0958) (P 5 0.0787) (P 5 0.4926)
AP angle of mandible 0.0868 0.1177 0.0059 0.0771 0.1524 0.0687 0.1736
(P 5 0.2736) (P 5 0.332) (P 5 0.972) (P 5 0.5832) (P 5 0.245) (P 5 0.6019) (P 5 0.2776)
APC1 0.3404 0.2557 0.4575 0.3892 0.4055 0.3496 0.1686
(P \0.0001)* (P 5 0.0326) (P 5 0.0039)* (P 5 0.004)* (P 5 0.0013)* (P 5 0.0062)* (P 5 0.292)
APC2 0.6123 0.6222 0.624 0.5574 0.6357 0.722 0.4405
(P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P 5 0.0039)*
APC3 0.6696 0.7733 0.5362 0.5971 0.612 0.7019 0.6708
(P \0.0001)* (P \0.0001)* (P 5 0.0005)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)*
AP epiglottis 0.5244 0.6182 0.3946 0.3808 0.4381 0.6279 0.467
(P \0.0001)* (P \0.0001)* (P 5 0.0142)* (P 5 0.0049)* (P 5 0.0005)* (P \0.0001)* (P 5 0.0021)*
LLC1 0.5641 0.6274 0.5416 0.604 0.5547 0.6069 0.495
(P \0.0001)* (P \0.0001)* (P 5 0.0004)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P 5 0.001)*
LLC2 0.6727 0.7286 0.5015 0.72 0.6201 0.6589 0.7177
(P \0.0001)* (P \0.0001)* (P 5 0.0013)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)*
LLC3 0.5747 0.6066 0.5235 0.5777 0.4022 0.6273 0.6467
(P \0.0001)* (P \0.0001)* (P 5 0.0007)* (P \0.0001)* (P 5 0.0014)* (P \0.0001)* (P \0.0001)*
LL epiglottis 0.3004 0.2929 0.295 0.3377 0.2034 0.2854 0.3394
(P 5 0.0001)* (P 5 0.0139)* (P 5 0.0722) (P 5 0.0134)* (P 5 0.119) (P 5 0.0271)* (P 5 0.0299)*
ANS PNS distance 0.128 0.1585 0.1553 0.0349 0.1964 0.0167 0.2208
(P 5 0.1056) (P 5 0.1899) (P 5 0.3518) (P 5 0.8042) (P 5 0.1327) (P 5 0.8992) (P 5 0.1654)
Shortest distance 0.6615 0.6358 0.6746 0.6727 0.7258 0.7632 0.4089
(P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P \0.0001)* (P 5 0.0079)*
Table VI. The best (analysis of variance, F 5 82.7; P \0.0001) linear regression (stepwise) model for PS volume
Nonstandardized coefficient (B) SD Standardized coefficient (beta) t Significance VIF
Constant 2533.1 371.2 6.8 \0.0001
LLC2 27.1 4.1 0.30 6.6 \0.0001 2.0043
Shortest distance 52 9.8 0.25 5.3 \0.0001 2.1900
APC3 46.3 6.9 0.30 6.7 \0.0001 1.9403
LL mandible 11.2 4.2 0.10 2.7 0.0088 1.4238
LLC1 13.3 4.1 0.15 3.3 0.0013 1.9209
AP hyoid bone 23.1 5.8 0.15 4 0.0001 1.3197
LL epiglottis 15.8 5.9 0.10 2.7 0.0083 1.4981
APC1 25.1 7.3 0.15 3.4 0.0008 1.7510
ANS-PNS distance 11.3 5.6 0.08 2 0.0428 1.3168
LLC3 11.9 5.9 0.09 2 0.0436 1.8444
June 2018 Vol 153 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics
Nejaim et al 833
were smaller in Class II mesofacial and dolichofacial tomography and cephalometry after mandibular setback surgery.
patients. Am J Orthod Dentofacial Orthop 2010;138:292-9.
10. Sheng CM, Lin LH, Su Y, Tsai HH. Developmental changes in
To provide the assessment of pharyngeal space vol-
pharyngeal airway depth and hyoid bone position from childhood
ume by professionals who do not have access to or expe- to young adulthood. Angle Orthod 2009;79:484-90.
rience in segmentation software programs, we have 11. Di Carlo G, Polimeni A, Melsen B, Cattaneo PM. The relationship
created a formula through linear regression analysis us- between upper airways and craniofacial morphology studied in
ing only linear measurements. This formula showed that 3D. A CBCT study. Orthod Craniofac Res 2015;18:1-11.
12. Chen H, Aarab G, Parsa A, De Lange J, Van Der Stelt PF,
our model can be useful to estimate the volume of the
Lobbezoo F. Reliability of three-dimensional measurements
pharyngeal space. As far as we know, no other studies of the upper airway on cone beam computed tomography im-
in the literature have developed a formula with this goal. ages. Oral Surg Oral Med Oral Pathol Oral Radiol 2016;122:
104-10.
CONCLUSIONS 13. Abramson ZR, Susarla S, Tagoni JR, Kaban L. Three-dimensional
computed tomographic analysis of airway anatomy. J Oral Maxil-
It was concluded that there are significant correla- lofac Surg 2010;68:363-71.
tions between the volume of pharyngeal space and the 14. Yang Q, Wang CH, Fan C, Chen J. A changes in hyoid bone position
mandible and hyoid bone measurements, suggesting after orthodontic treatment of patients with mandibular deviation.
West Indian Med J 2013;62:239-43.
that the stomatognathic system should be evaluated in
15. Steiner CC. Cephalometrics for you and me. Am J Orthod 1953;39:
an integral and nonindividualized way. Furthermore, it 729-55.
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precision, resulting in a useful formula for estimating edgewise appliances. 2nd ed. St Louis: Mosby; 1972.
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