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Oropharyngeal airway in children with


Class III malocclusion evaluated by cone-beam
computed tomography
Tomonori Iwasaki,a Haruaki Hayasaki,b Yoshihiko Takemoto,c Ryuzo Kanomi,d and Youichi Yamasakie
Kagoshima and Himeji, Japan

Introduction: Upper airway size is increasingly recognized as an important factor in malocclusion. However,
children with Class III malocclusion are somewhat neglected compared with those with a Class II skeletal pat-
tern. Therefore, the purpose of this study was to establish the characteristic shape of the oropharyngeal airway
(OA) in children with Class III malocclusion. Methods: The sample comprised 45 children (average age, 8.6 6
1.0 years) divided into 2 groups: 25 with Class I and 20 with Class III malocclusions. OA size of each group was
evaluated by cone-beam computed tomography. Cluster analysis, based on OA shape, redivided the subjects
into wide, square, and long types. The distributions of Class I and Class III subjects were compared among the
types. Results: The Class III group showed statistically larger OA area and width compared with the Class I
group. Area was positively correlated with Class III severity. The square type included 84% of the Class I mal-
occlusions but only 30% of the Class III malocclusions, indicating that the OA in Class III malocclusion tends to
be flat. Conclusions: The Class III malocclusion is associated with a large and flat OA compared with the Class
I malocclusion. (Am J Orthod Dentofacial Orthop 2009;136:318.e1-318.e9)

A
bnormal growth of the tissues of the upper air- the relationship between respiratory function and facial
way can make the airway narrower and prone morphology in orthodontics.4 Several articles have ana-
to obstructive sleep apnea (OSA).1 The impor- lyzed the morphology of the upper airway from lateral
tance of this obstruction in the development of many cephalograms.4,5 Class II patients have a narrower ante-
childhood problems is increasingly recognized.1-4 roposterior pharyngeal dimension, and this narrowing is
OSA in children is associated with excessive daytime specifically noted in the nasopharynx at the level of the
sleepiness, hyperactivity, attention deficit disorder, hard palate and in the oropharynx at the level of the tip
poor hearing, physical debilitation, and failure to of the soft palate and the mandible.5 Class II Division 1
thrive.3 Accordingly, much attention has been paid to malocclusion is associated with a narrower upper air-
way even without retrognathia.6 However, the relation-
a
Research associate, Developmental Medicine, Health Research Course, ship between facial morphology and the morphology of
Graduate School of Medical and Dental Sciences, Kagoshima University, the upper airway in children with Class III malocclusion
Kagoshima, Japan.
b
Assistant professor, Developmental Medicine, Health Research Course, has not been previously described.
Graduate School of Medical and Dental Sciences, Kagoshima University, Previous analyses5,6 established cephalometric
Kagoshima, Japan.
c
norms for the upper airway7 by using lateral cephalo-
Postgraduate student, Developmental Medicine, Health Research Course,
Graduate School of Medical and Dental Sciences, Kagoshima University, grams, based on the high reproducibility of its dimen-
Kagoshima, Japan. sions.8 Nevertheless, because the left-right length
d
Private practice, Himeji, Japan. (width) of the upper airway is not visible, its precise
e
Professor and chairman, Developmental Medicine, Health Research Course,
Graduate School of Medical and Dental Sciences, Kagoshima University, size cannot be estimated from a lateral cephalogram
Kagoshima, Japan. alone.
Supported in part by the Japanese Society for the Promotion of Science (nos. Accordingly, the purpose of this study was to carry
18791563, 19390532, 19592357, and 19592360).
The authors report no commercial, proprietary, or financial interest in the out a systematic evaluation of the oropharyngeal air-
products or companies described in this article. way (OA) in children with a Class III malocclusion
Reprint requests to: Tomonori Iwasaki, Field of Developmental Medicine, by using cone-beam computed tomography (CBCT)
Health Research Course, Graduate School of Medical and Dental Sciences,
Kagoshima University, 8-35-1, Sakuragaoka Kagoshima-City, Kagoshima, and 3-dimensional (3D) image reconstruction soft-
890-8544, Japan; e-mail, yamame@dentb.hal.kagoshima-u.ac.jp. ware. OA size (ie, cross-sectional area [CSA]), length,
Submitted, July 2008; revised and accepted, February 2009. and width in the horizontal plane of children with
0889-5406/$36.00
Copyright Ó 2009 by the American Association of Orthodontists. Class III malocclusion were measured and compared
doi:10.1016/j.ajodo.2009.02.017 with children with Class I malocclusion. The null
318.e1
318.e2 Iwasaki et al American Journal of Orthodontics and Dentofacial Orthopedics
September 2009

Fig 1. Three-dimensional image of a skull from CBCT. The standard coordinate system was estab-
lished by using orbitale and porion (blue lines). The OA was measured in a transverse plane that
passed through gonion (red line).

Fig 2. Measurements of the nasopharyngeal airway (NA) and the OA (OA): S, CSA; D, depth; and W,
width. The width of OA was measured at the narrowest part of the entire depth. Wmax was measured
at the greatest width of the OA.

hypothesis was that Class III and Class I children do clusion patients had a positive overjet of 2 to 4 mm,
not differ in upper airway size. a Class I deciduous or permanent canine relationship,
and a Class I permanent molar relationship; and (2)
Class III malocclusion patients had a negative overjet,
MATERIAL AND METHODS a Class III deciduous or permanent canine relationship,
A total of 45 patients, who visited Kanomi Or- and a Class III permanent molar relationship. The Class
thodontic & Pediatric Dental Clinic (Himeji-City, I and Class III groups included 13 boys and 12 girls
Hyogo-Prefecture, Japan) for orthodontic treatment, (average age, 8.8 6 1.0 years) and 12 boys and 8 girls
participated in this study. The subjects were divided (average age, 8.4 6 1.0 years), respectively. Because
into 2 groups according to occlusion: (1) Class I maloc- the volume of the airway is influenced by head posture,
American Journal of Orthodontics and Dentofacial Orthopedics Iwasaki et al 318.e3
Volume 136, Number 3

Fig 3. Volume measurement of the upper airway and intraoral airway space: A, upper airway volume
was measured between the hard palate and the base of the epiglottis; B, computer-generated
extraction of upper airway (left) and intraoral airway space (right).

Table I. Cephalometric measurements of the anteropos- A 3D coordinate system and 3D image were constructed
terior position of the maxilla and the mandible with a medical image analyzing system (ImagnosisVE,
Imagnosis, Kobe, Japan).
Class I group Class III group
(n 5 25) (n 5 20)
The origin of the 3D coordinate system was the
midpoint between the left and right porions. This origin
Mean SD Mean SD P and left and right orbitale defined the standard horizon-
Overjet (mm) 2.82 1.15 –2.28 0.99 \0.001* tal plane. A frontal plane was constructed through both
ANB ( ) 3.56 1.97 0.40 1.45 \0.001* orbitale points and perpendicular to the horizontal plane
AF-BF (mm) 5.60 2.60 1.00 3.04 \0.001* (Fig 1). The sagittal plane was constructed through both
Wits (mm) 1.23 1.78 4.85 1.56 \0.001* orbitale midpoints and perpendicular to the horizontal
APDI ( ) 79.90 3.50 87.60 4.51 \0.001*
and frontal planes.
AF-BF, The distance between perpendiculars drawn from A-point and From this cephalometric image, the anteroposterior
B-point onto the Frankfort horizontal plane; APDI, the facial angle 6 positions of both the maxilla and the mandible were eval-
the A-B plane angle and again 6 the Frankfort-palatal plane angle. uated with the ANB angle,10 AF-BF (the distance be-
*Statistically significant at P \0.01.
tween perpendiculars drawn from A-point and B-point
onto the Frankfort horizontal plane),11 Wits appraisal,12
the craniocervical inclinations of all subjects were ex- and APDI angle (the facial angle 6 the A-B plane angle
amined to ensure that their inclinations were between and again 6 the Frankfort-palatal plane angle).13
90 and 110 .9 The study was reviewed and approved In addition, the intraoral airway space and degree of
by the Ethics Committee of the Kagoshima University hyperplasia of the palatine tonsils were measured.
Graduate School of Medical and Dental Sciences, Ka- Airway cross-sectional measurements included
goshima, Japan. CSA, depth (anteroposterior direction), and width
Each subject was seated in a chair with his or her (left-right direction). The CSAs of the nasopharyngeal
Frankfort horizontal plane parallel to the floor. A and oropharyngeal airways were defined as shown in
CBCT device (CB MercuRay, Hitachi Medical, Tokyo, Figure 2. Three parameters for the size of the nasopha-
Japan) was set to maximum 120 kV, maximum 15 mA, ryngeal and oropharyngeal airways were determined
and exposure time of 9.6 seconds. The data were sent di- based on previous reports.14 The nasopharyngeal airway
rectly to a personal computer and stored in digital imag- cross-section was measured along a horizontal plane at
ing and communications in medicine format (DICOM). the airway’s narrowest part on the cephalometric image.
318.e4 Iwasaki et al American Journal of Orthodontics and Dentofacial Orthopedics
September 2009

Table II. Mean measurements of the upper airway


Class I group (n 5 25) Class III group (n 5 20)

Mean SD Mean SD P

Nasopharyngeal airway
CSA (mm2) 181.12 64.57 182.77 64.89 0.993
Depth (mm) 8.27 2.65 9.57 3.64 0.173
Width (mm) 26.80 3.84 25.79 3.36 0.360
Oropharyngeal airway
CSA (mm2) 119.18 48.09 168.56 54.40 0.002†
Depth (mm) 10.68 2.52 13.58 3.16 0.001†
Width (mm) 14.97 3.98 18.40 4.47 0.021*
Width difference 3.33 2.17 6.09 3.72 0.008†
Upper airway volume (mm3) 6260.15 3010.03 7326.89 2593.40 0.295
Intraoral airway (mm3) 702.02 1289.18 2101.51 2148.17 0.016*

*Statistically significant at P \0.05; †Statistically significant at P \0.01.

Table III. Correlations among the OA measurements of Table IV. Correlations between the anteroposterior posi-
the Class I and Class III groups tion of the maxilla and the mandible and the OA mea-
surements of the Class III group (n 5 20)
Depth (P) Width (P)
ANB (P) AF-BF (P) Wits (P) APDI (P)
Class I group CSA 0.471 (0.018)* 0.570 (0.003)†
(n 5 25) Depth — –0.234 (.261) CSA –0.529 –0.515 0.173 0.584
Class III group CSA 0.219 (0.355) 0.536 (0.015)* (0.016)* (0.020)* (0.465) (0.007)†
(n 5 20) Depth — –0.406 (0.076) Depth –0.253 –0.26 0.085 0.343
† (0.281) (0.269) (0.722) (0.139)
*Statistically significant at P \0.05; Statistically significant at
Width –0.017 0.03 0.095 0.009
P \0.01.
(0.944) (0.900) (0.691) (0.970)

AF-BF, The distance between perpendiculars drawn from A-point and


The OA cross-section was measured along a horizontal B-point onto the Frankfort horizontal plane; APDI, the facial angle 6
the A-B plane angle and again 6 the Frankfort-palatal plane angle.
plane passing through the midpoint of bilateral gonion. *Statistically significant at P \0.05; †Statistically significant at
Volume-rendering software (INTAGE Volume Edi- P \0.01.
tor, KGT, Tokyo, Japan) was used to create 3D images
and evaluate the volumes of the upper airway and intrao-
ral airway space. The volume data were in a 512 3 512 correlation coefficients were calculated to evaluate
matrix with a voxel size of 0.377 mm. A Hounsfield unit the relationships among CSA, depth, and width of
range of –1024 to –300 was interpreted to be air. The the OA, and correlations between the size of the OA
upper airway volumes from nasal plane to the base of and the anteroposterior position of the maxilla and
epiglottis plane and the intraoral airway space were the mandible in the Class III group. A cluster analysis
measured15 (Fig 3). (group average method) was carried out based on the
The difference between the greatest width and the shape of the OA after the size parameters of the air-
narrowest width of the OA was examined to evaluate way were standardized from 0 to 1. According to the
changes in airway form produced by hyperplasia of resulting dendrogram, the subjects could be divided
the palatine tonsils (Fig 2). into 3 types of shapes. The Scheffé test was performed
among the 3 groups for the anteroposterior position of
the maxilla and the mandible and the size of OA. In
Statistical analysis addition, the Fisher exact test clarified the distribution
T tests were used to compare (1) the anteroposte- of shape types in the 2 malocclusion groups. P \0.05
rior position of the maxilla and the mandible; (2) the was considered statistically significant.
size of the upper airway (volume, CSA, width, depth); The reliability of the measurements (intraoperator
(3) intraoral airway space, and (4) degree of repeatability) was assessed first by repeated tracings
hyperplasia of the palatine tonsils between the Class (landmark identification) and then by digitization of
I and Class III groups. The Pearson product-moment the same lateral cephalograms. To assess the error in
American Journal of Orthodontics and Dentofacial Orthopedics Iwasaki et al 318.e5
Volume 136, Number 3

Fig 4. Dendrogram of the 3 airway shapes obtained by cluster analysis.

Fig 5. Examples of 3 airway-shape types. W, Width; D, depth. In the wide type, W . D; in the square
type, W 5 D; in the long type, W \ D.

landmark identification, 10 randomly selected lateral for CSA, 0.34 mm for depth, and 0.53 mm for width
cephalograms from the 45 were traced and digitized of the nasopharyngeal airway. For the OA, the errors
twice by the same operator (T.I.) a week later. A paired were 1.69 mm2 for CSA, 0.15 mm for depth, and 0.54
t test detected no statistically significant differences. mm for width. The error for airway volume was
Correlations between the first and second measurements 162.48 mm3. According to all repeated analyses, the
ranged from 0.975 to 0.999 (P \0.001, df 5 8). Calcu- method error was considered negligible.
lations were also performed independently for each dig-
itization, the differences between paired linear
measurements were calculated, and error according to RESULTS
Dahlberg’s method16 (double determination method) The cephalometric anteroposterior position of the
was computed. The resulting errors were 1.37 mm2 maxilla and mandible, and the OA measurements of
318.e6 Iwasaki et al American Journal of Orthodontics and Dentofacial Orthopedics
September 2009

Table V. Subject distributions based on airway shape between the square and long types. The wide type had
the largest CSA (198.58 mm2), and the long type’s
Wide type Square type Long type
CSA was only 67% (132.75 mm2), whereas the square
Class I group (n 5 25) 3 21 1 type’s CSA was just 53% (105.70 mm2) of the wide
Class III group (n 5 20) 11 6 3 type. The anteroposterior position of the maxilla and
Total 14 27 4 the mandible were significantly different only between
Fisher exact test: df 5 2; chi-square 5 14.18; P \0.01. the wide and square types.

the Class I and the Class III groups are compared in DISCUSSION
Table I. The mandible of the Class III group was located
more anteriorly than in the Class I group. The main purpose of this study was to establish the
characteristics of the OA in children with Class III mal-
The size of the nasopharyngeal airway and the upper
occlusion with CBCT. Upper airway shape has been of
airway volume of the Class III group did not differ sig-
interest for more than 30 years because of its connection
nificantly from those of the Class I group (Table II).
with OSA in young children, and studies have included
However, the size of the OA of the Class III group
clinical observations,17 anatomy,18 flow mechanics,19
was significantly larger than that of the Class I group.
and ventilation control.20 That children with OSA
The CSA of the Class I group (119.18 mm2) was 71%
have narrower pharyngeal airways compared with con-
that of the Class III group (168.56 mm2). The intraoral
trol children during wakefulness21 and sedation22 has
airway space of the Class III group (2101.52 mm3) was
been shown by cephalometry,23 acoustic reflection,21
significantly larger than that of the Class I group (702.03
endoscopy,24 and magnetic resonance imaging.25-27
mm3), indicating a lower tongue position; the difference
Aboudara et al28 found much larger interindividual
between the maximum and minimum oropharyngeal
variations of the volume and area of the upper airway in
widths was significantly greater in the Class III group
cephalograms than with computed tomography (CT).
(6.09 mm) than in the Class I group (3.33 mm), indicat-
CBCT can better assess the cross-sectional dimensions
ing greater hyperplasia of the palatine tonsils.
of the airway space than conventional 2-dimensional radi-
The 2 groups also differed in how the OA measure- ography. The drawing of airway circumferences and cal-
ments were correlated. The oropharyngeal CSA was culation of cross-sectional areas by computer also greatly
significantly correlated with both depth and width in reduces operator-dependent bias.
the Class I group (Table III) but with width only in the Because of the relatively small sample in this study,
Class III group. boys and girls were analyzed together. Abu Allhaija
Table IV shows the correlations between the antero- et al29 found no sex differences in pharyngeal dimen-
posterior positions of the maxilla and mandible with 3 sions between 45 girls and 45 boys (Class I, Class II,
measurements of the OA in the Class III group. Depth and Class III groups of 15 patients each; ages, 14-17
and width did not show significant correlations with years), and their findings agree with other reports that
cephalometric parameters; however, the CSA had mod- suggest no sex differences in the pharyngeal dimensions
erate correlations with all but the Wits appraisal. ANB of prepubertal children.30-33
and AF-BF were negatively correlated to CSA, and The CSA of the upper airway has been measured in
APDI showed the only significant positive correlation. children with respiratory obstruction with 3D CT.29-34
The subjects were divided into 3 groups—wide, However, norms for the upper airway in healthy children
square, and long—according to the shape of their OAs have not been previously reported. After evaluating up-
by the cluster analysis (Figs 4 and 5). This number of per airway volume and CSAs of the nasopharyngeal and
groups was determined by considering the number of sub- oropharyngeal airways, we found that the oropharyngeal
jects. Based on this analysis, 21 of 25 (84%) of the Class I CSA is a characteristic of Class III children (Table II).
subjects were the square type, and 11 of 20 (55%) of Class Thus, about the oropharyngeal airway which was a char-
III subjects were the wide type (Table V). This distribu- acteristic of Class III, size and form of the CSA were
tion of the subjects was statistically significant according examined.
to the Fisher exact test (P \0.01). Peh et al35 used CT to compare the CSAs of adult
When the cephalometric parameters were compared OSA patients in the supine position with matched con-
among the 3 shape types, significant differences were trols. They found that the size of the OA of the Class I
found, especially between the wide and square types group was smaller (119.18 6 48.09 mm2, n 5 25) than
(Table VI). The group differences of the 3 size dimen- that of normal adults (173.0 6 97.6 mm2, n 5 25),
sions were significant except for CSA and width who were closer to the Class III group (168.56 6 54.4
American Journal of Orthodontics and Dentofacial Orthopedics Iwasaki et al 318.e7
Volume 136, Number 3

Table VI.Comparison of anteroposterior positions of the maxilla and the mandible, and the OA size parameters of the 3
shape types
Post-hoc

Wide Square Long Scheffé test


(n 5 14) (n 5 27) (n 5 4) ANOVA
Mean (SD) Mean (SD) Mean (SD) P Wide vs square Long Square vs long

ANB ( ) 0.72 (1.94) 3.22 (2.08) 1.25 (2.50) 0.002* \0.05† 0.9 0.221
AF-BF (mm) 1.46 (2.76) 5.26 (3.20) 1.30 (4.11) 0.001* \0.05† 0.995 0.074
Wits (mm) 4.23 (1.80) 1.76 (2.23) 4.02 (3.41) 0.003* \0.05† 0.986 0.174
APDI ( ) 86.84 (5.18) 80.60 (4.09) 86.25 (6.29) 0.006* \0.05† 0.975 0.094
CSA (mm2) 198.58 (44.68) 105.70 (30.68) 132.75 (24.52) \0.001* \0.05† \0.05† 0.385
Depth (mm) 13.07 (1.52) 10.12 (1.87) 19.12 (1.53) \0.001* \0.05† \0.05† \0.05†
Width (mm) 16.64 (4.21) 10.49 (4.06) 7.22 (2.37) \0.001* \0.05† \0.05† 0.328

AF-BF, The distance between perpendiculars drawn from A-point and B-point onto the Frankfort horizontal plane; APDI, the facial angle 6 the A-B
plane angle and again 6 the Frankfort-palatal plane angle.
*Statistically significant at P \0.01; †Statistically significant at P \0.05.

Fig 6. Examples of tongue position against the palate and OA: A, the wide type has a flat shape and
a lower position of the tongue, resulting in reduced OA; B, the long type has hypertrophic palatine
tonsils. The tongue is positioned more anteriorly to maintain OA.

mm2, n 5 20).30 Ciscar et al2 stated that the maximum is almost the same as the 15 mm reported by McNa-
and minimum velopharyngeal area in healthy adults mara.36 All measurements of the OA were significantly
(n 5 8; ages, 30-50 years) are 121.9 6 7.9 and 103.2 6 larger in our Class III group than in our Class I group.
10.0 mm2, respectively, based on magnetic resonance Although the negative and moderate correlation be-
imaging. They also reported maximum and minimum tween depth and width (Table III) in the Class III group
depths and widths of the same healthy subjects (8.7 6 was not significant (r 5 –0.406, P 5 0.076), the results
3.2 to 4.9 6 3.4 mm, and 16.4 6 2.3 to 13.9 6 2.6 still suggest a flat OA shape. In both groups, CSA was
mm, respectively). Their results were relatively small statistically correlated with airway width, making it
compared with ours because of differences in age, posi- a more important contributor to CSA than depth. CSA
tion, and projected planes. The depths of our Class III tends to be larger in proportion to the severity of the
group were 13.58 mm before enlargement and 14.98 Class III malocclusion (Table IV). Lopatiene and Babar-
mm after enlargement to match a cephalogram, which skas37 reported that nasal resistance was correlated to
318.e8 Iwasaki et al American Journal of Orthodontics and Dentofacial Orthopedics
September 2009

overjet (P 5 0.042), open bite (P 5 0.033), and maxil- Our data indicate that Class III patients have larger
lary crowding (P 5 0.037) of Class II patients aged 7 to OAs, with less possibility of OSA, even though the
15 years. Accordingly, Class III children might have shape is not square (ie, flat in an anteroposterior or
less obstruction of the upper airway. left-right direction).
Variation of OA measurements were relatively large
in this study (Table II), but all subjects could be divided CONCLUSIONS
into 3 groups based on airway shape. According to this
division, 84% of the Class I subjects but only 30% of the Children with Class III malocclusion had signifi-
Class III subjects were of the square type. In other cantly larger OAs compared with those with Class I
words, 70% of the Class III subjects were either of the malocclusion. Although 84% of children with Class I
wide or the long type, with a flattened OA along either malocclusion had a square OA, 70% of the children
the anteroposterior axis (55% of the Class III subjects) with Class III malocclusion had a relatively flat shape,
or the left-right axis (15% of the Class III subjects) either left-right (55% wide type) or anteroposterior
(Table V). The most interesting finding was the smallest (15% long type).
CSA in the square type (Table VI). These results suggest
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