Developmental Changes in Pharyngeal Airway Depth and Hyoid Bone
Position from Childhood to Young Adulthood
Chang-Min Shenga; Li-Hsiang Linb; Yu Suc; Hung-Huey Tsaid
ABSTRACT
Objective: (1) To test the hypothesis that there are no developmental changes in the pharyngeal
airway depth and hyoid bone position from childhood to adulthood in normal Taiwanese persons, (2) to identify any sexual dimorphism, and (3) to find the predictive value of selective variables for the hyoid bone position.
Materials and Methods: Lateral cephalometric radiographs of 239 normal Taiwanese (132
fe-males and 107 fe-males; aged 7–27 years) were separated into three stages according to dental age. Twenty-three linear and 20 angular measurements were made in all subjects. Sexual di-morphism was analyzed by Student’s t-test. Analysis of variance was used to compare the three stages in both genders. A stepwise regression analysis was carried out to predict the hyoid bone position. The level of significance for all analyses was set at P⬍ .05.
Results: The pharyngeal airway depth increased from the mixed dentition stage to the permanent
dentition stage in both genders. There was sexual dimorphism in the lower pharyngeal airway depth. The hyoid bone position showed an obvious difference in the permanent dentition stages between genders. The vertical position of the hyoid bone was associated with the mandibular morphology and position, but the relationship in males was reversed compared with that in fe-males.
Conclusions: The hypothesis was rejected. There are developmental changes in the pharyngeal
airway depth and hyoid position from childhood to young adulthood. Sexual dimorphism appeared in the lower pharyngeal airway and the direction of change in the vertical position of the hyoid bone. (Angle Orthod. 2009;79:484–490.)
KEY WORDS: Development; Change; Airway; Hyoid bone
INTRODUCTION
The pharynx is a tube-shaped structure that extends superoinferiorly from the cranial base to the level of the inferior surface of the sixth cervical vertebra.1It lies
dorsal to the nasal and mouth cavity and is cranial to the esophagus, larynx, and trachea. The pharynx can
aGraduate MS Student, Graduate Institute of Dentistry, Col-lege of Oral Medicine, Taipei Medical University, Taipei, Taiwan. bInstructor, Graduate Institute of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan.
cResearch Assistant, Department of Dentistry, Mackey Me-morial Hospital, Taipei, Taiwan.
dProfessor, School of Oral Hygiene, College of Oral Medi-cine, Taipei Medical University, Taipei, Taiwan.
Corresponding author: Dr Hung-Huey Tsai, School of Oral Hygiene, College of Oral Medicine, Taipei Medical University, 250 Wu-Xin Street, Taipei, Taiwan 110
e-mail: hunghuey@tmu.edu.tw)
Accepted: August 2008. Submitted: June 2008.
2009 by The EH Angle Education and Research Foundation, Inc.
be anatomically separated into three parts: the naso-pharynx, oronaso-pharynx, and hypopharynx. In a midsag-ittal image, the nasopharynx extends from the nasal turbinates to the hard palate; the oropharynx can be subdivided into the retropalatal pharynx, from the hard palate to the caudal margin of the soft palate, and the retroglossal pharynx, which extends from the caudal margin of the soft palate to the base of the epiglottis; and the hypopharynx is from the base of the epiglottis to the larynx.2The pharynx plays an important role in
respiration and deglutition.
The hyoid bone is connected to the pharynx, man-dible, and cranium through muscles and ligaments.3It
is the only bone of the body that has no bony articu-lations. The hyoid bone and its connecting muscles are also part of the oropharyngeal complex. Without the hyoid bone, our facility for maintaining an airway, swallowing, preventing regurgitation, and maintaining the upright postural position of the head could not be controlled as carefully.4
Table 1. Number and Age Distribution of the Materials Male Number Age Female Number Age Mixed dentition (stage 1) 21 9.66⫾ 1.39 24 10.06⫾ 1.49 Early permanent dentition (stage 2) 29 13.58⫾ 2.13 43 13.37⫾ 2.03 Permanent dentition (stage 3) 57 22.48⫾ 1.24 65 22.09⫾ 1.54 Total 107 17.51⫾ 5.67 132 17.14⫾ 5.36
A nasal breather may change to a mouth breather because of an obstruction in the nasal or pharyngeal airway.5 Mouth breathing may be related to a specific
malocclusion such as narrowing of the maxillary arch.6
In addition, pharyngeal airway narrowing is a com-monly described characteristic in obstructive sleep ap-nea/hypopnea syndrome (OSAHS) patients.7 OSAHS
affects mainly middle-aged males, and the prevalence increases with age.8
Many cephalometric studies have shown craniofa-cial abnormalities in OSAHS patients. Despite that ob-served alterations in craniofacial morphology are not uniform, a steeper mandibular plane angle, a shorter mandibular body length, and a low hyoid bone position were consistently reported by most investigations.9
Gross changes in the hyoid bone position can be used to assess gross changes in the tongue position.4
Kon-do and Aoba10also stressed that lifting a low-postured
tongue to improve airway patency was important for the treatment stability of a narrow maxillary arch.
Interpretation of the significance of variations in growth and function is dependent on an understanding of normal developmental changes. It is necessary to determine changes in the pharyngeal airway depth and hyoid bone position that occur in healthy subjects during their active growth years and beyond. We can benefit from such information in planning treatment and further investigations into breathing-disordered diseases. Most previous studies emphasized the treat-ment effect on pharyngeal airway size and hyoid bone position11,12; however, developmental changes of the
pharyngeal airway and hyoid bone position have re-ceived little attention in the past. Bench13 stated that
the hyoid bone descends gradually from a position op-posite the lower half of the third and the upper half of the fourth cervical vertebra at the age of 3 years to a position opposite the fourth cervical vertebra in adult-hood. Tsai14 reported that changes in pharyngeal
structures were significantly greater in males than in females during development.
The purposes of this cross-sectional study were threefold: (1) to investigate changes in the pharyngeal airway depth and hyoid bone position during devel-opment from the early mixed dentition to young adult-hood in normal Taiwanese persons, (2) to identify any sexual dimorphism in these developmental changes, and (3) to evaluate the predictive value of selective variables for the hyoid bone position.
MATERIALS AND METHODS
We reviewed the lateral cephalometric radiographs from the files of our orthodontic department between 1997 and 2006 and selected 239 Taiwanese subjects (132 females and 107 males), aged 7 to 27 years. All
subjects included in this study had natural dentition and no craniofacial anomalies, syndromes, clefting, or symptoms or signs of dysfunction of the masticatory system. Standard lateral cephalometric radiographs with the teeth in habitual occlusion and with the head oriented horizontally with the Frankfort plane were tak-en with a cephalostat in accordance with standard cephalometric procedures. The materials were divided into three stages according to dental age: mixed den-tition (stage 1), early permanent denden-tition (stage 2), and complete permanent dentition (stage 3) (Table 1). All radiographs were digitized and traced by the same person, and 32 landmarks were identified (Fig-ure 1), which were used to perform 23 linear and 20 angular measurements. There were 5 linear items for the pharyngeal airway depth (Figure 2), 1 angular and 7 linear items for the hyoid bone position (Figure 3), and still another 30 items describing the craniofacial morphology (Table 2).
All landmarks were coordinated with the x- and y-ax-es. The line passing through point Or and Po was des-ignated the x-axis. The line passing through point S and perpendicular to the x-axis was designated the y-axis. All measurements were performed using the computerized cephalometric analysis software Win-ceph (version 6.0, Rise Co, Japan).
Thirty randomly selected lateral cephalometric ra-diographs were traced and measured twice 2 weeks later to estimate the error that might occur with this method. The error for each parameter was calculated based on Dahlberg’s formula (error2⫽ ⌺ d2/2n).15The
greatest error occurring among linear measurements was the distance from ANS to PNS (0.9 mm) and among angular measurements was the angle formed by the epiglottis, hyoid bone, and tongue tip (2.5⬚). Dif-ferences between the means of the first and second tracings for each variable were tested by means of a paired t-test, and all were within an acceptable range. Student’s t-test was used to analyze sexual dimor-phism in each stage. Analysis of variance was used to compare the mean values of each measurement among the three stages in both genders. Stepwise re-gression analyses were used to explore the
relation-Figure 1. Landmarks. 1 indicates S; 2, N; 3, Or; 4, ANS; 5, A; 6,
U1; 7, U1R; 8, L1; 9, L1R; 10, B; 11, Pog; 12, Gn; 13, Me; 14, GoL; 15, Go; 16, GoP; 17, Ar; 18, Po; 19, Ba; 20, PNS; 21, H (hyoid bone); 22, C3 (the most anteroinferior point of the third vertebra); 23, SPU (the point on the posterior pharyngeal wall along the palatal plane); 24, SPM (the point on the posterior pharyngeal wall where the distance to SAM is the shortest); 25, SPML (the point on the posterior pharyngeal wall where the distance to P is the shortest); 26, SPL (the point on the posterior pharyngeal wall where the dis-tance to SAL is the shortest); 27, SPLL (the point on the posterior pharyngeal wall where the distance to E is the shortest); 28, SAM (the point on the soft palate where the postpalatal airway is narrow-est); 29, P (the tip of the soft palate); 30, SAL (the point on the tongue along the mandibular lower border); 31, E (epiglottis); 32, TT (tongue tip).
Figure 2. Measurements of pharyngeal airway depth. D1 indicates
the distance between landmark 20 and 23; D2, the distance between landmark 24 and 28; D3, the distance between landmark 25 and 29; D4, the distance between landmark 26 and 30; D5, the distance between landmark 27 and 31.
ships between craniofacial morphology and hyoid bone position. All statistical analyses were performed by the Microsoft Excel statistical software package (Office 2007) and SigmaStat (version 2.0), with a 5% level of significance (P⬍ .05).
RESULTS
Table 3 shows the mean values and standard de-viations of measurements of the pharyngeal airway depth among each stage for both genders. Results in-dicated that except for the retroglossal-pharyngeal depth (D4) of females, all other measurements in both genders significantly increased from stages 1 to 3. Sexual dimorphism appeared in the lower part of the pharyngeal airway in stages 1 (D5) and 3 (D4 and D5). Table 4 shows the mean values and standard de-viations of the measurements for the hyoid bone
po-sition among each stage for both genders. Few mea-surements exhibited significant differences between males and females in stages 1 (H4, H7) and 2 (H2, H4), but the means of H2, H3, H4, H5, H6, and H7 were greater and that of H8 was smaller in males than females in stage 3. The distance between the hyoid bone and epiglottis (H4) remained constant from stag-es 1 to 3 in both genders. The distance from the hyoid bone to the mandibular plane did not significantly change from stages 1 to 3 in females; no significant differences were present in the angle formed by the epiglottis, hyoid bone, and tongue tip from stages 1 to 3 in males.
The stepwise regression analysis showed that the distance from the hyoid bone to the mandibular plane (H7) could be predicted by the facial angle in males (Figure 4) and Ar-Go in females (Figure 5). On the other hand, Ar-Go in males and the facial angle in fe-males had predictive values for the distance between the hyoid bone to the C3-Me plane (H6) (Figures 6 and 7).
DISCUSSION
During inhalation, the conjoint activity of the inter-costal muscles and the diaphragm creates negative airway pressure. Once this pressure surpasses the
Figure 3. Measurements of hyoid bone position. H1 indicates H-Me;
H2, H-C3; H3, H-PNS; H4, H-E; H5, H-TT; H6, the perpendicular distance from hyoid bone to the plane formed by C3 and Me; H7, the perpendicular distance from hyoid bone to the mandibular plane; H8, the angle formed by E, H, and TT.
Table 2. Measurements of Craniofacial Morphology
Linear Measurements Angular Measurements
S-N Facial angle
N-ANS Convexity
ANS-Me A-B plane
N-Me Y-axis
S-Go FH-SN
Ar-Go SNA
Go-Me SNB
ANS-PNS ANB
C3-Me Nasal floor to SN
P-PNS Mandibular plane to SN
Facial height ratio Nasal floor to mandibular plane Ramus plane to SN
Gonial angle U1 to SN
L1 to mandibular plane Interincisal angle Saddle angle (N-S-Ar) Artical angle (S-Ar-Go(P)) ANS-PNS-E
force generated by the pharyngeal muscles, the phar-ynx will collapse and occlude the airway. The patency of the pharyngeal airway is mainly dependent on the activity of the oropharyngeal muscles.16Three
pharyn-geal segments tend to collapse—the retropalatal ynx, the retroglossal pharynx, and retroepiglottic phar-ynx (posterior to the epiglottis)—because the anterior and lateral walls of these segments have no bony sup-port.17 That was the reason why we focused on
de-velopmental changes over the five sites we selected in the pharyngeal airway.
Martin et al18conducted a study on 60 men and 54
women (median age, 35 years; range, 16–74 years) and concluded that all upper airway dimensions, ex-cept the oropharyngeal junction, decreased with in-creasing age in both men and women. Our study re-vealed that the depth of the pharyngeal airway signif-icantly increased from childhood to young adulthood in both genders, except that of the retroglossal-pha-ryngeal airway depth (D4) in females. The average chronologic age of our subjects was younger than that of Martin’s subjects, and the difference between the two studies implies that the developmental pattern of the pharyngeal sagittal depth in young people might differ from that in middle-age persons.
There was no sexual difference in the depths of the
retropalatal-pharyngeal airway (D1-D3); however, this phenomenon existed in the retroepiglottic-pharyngeal airway (D5) during childhood. The dimensions of the retroglossal- and retroepiglottic-pharyngeal airway (D4 and D5) increased more with age in males than in fe-males; therefore, a smaller depth in males during childhood produced no sexual difference in the early permanent dentition stage, and more obvious sexual dimorphism appeared in adulthood.
A previous study concluded that there was no sex-ual dimorphism in hyoid bone position in normal Tai-wanese children from the deciduous dentition to the early permanent dentition, and the hyoid bone position was consistently above the line connecting C3 and Me.4Our data showed similar findings. We performed
eight measurements on the hyoid bone position. Only two measurements showed a significant difference be-tween genders in the mixed dentition and early per-manent dentition stages, respectively, whereas seven measurements revealed significant differences in the permanent dentition stage, indicating that gender’s ef-fects on the hyoid bone position might begin during the period of adolescence because of the active growth of teenagers.
The epiglottis is suspended at its base by the hyo-epiglottic ligament and the hyoid bone. During inspi-ration, the patency of the retroepiglottic pharynx relies on the activity of the hyoid muscles. The actions of these muscles (the geniohyoid, sternohyoid, and thy-rohyoid muscles) bring the hyoid bone to a forward position and stabilize the retroepiglottic pharynx by tensing the hyoepiglottic ligament.16,19 Our study
showed that the distance between the hyoid bone and epiglottis did not significantly change in either gender from childhood to young adulthood; however, sexual
Table 3. The Results of Statistics Analysis of Measurements for Pharyngeal Airway Depth among each Stage (ANOVA) and between Males and Females (Student’s t-test)
Measurement, mm Sex t-Test Stage 1 Mean SD Stage 2 Mean SD Stage 3 Mean SD ANOVAa D1 Female 23.58 5.31 26.52 4.02 28.55 2.79 Pⱕ .001 Male 23.34 3.64 27.46 3.25 28.54 3.77 Pⱕ .001 t-test NS NS NS D2 Female 10.18 2.76 12.41 2.83 14.03 2.56 Pⱕ .001 Male 9.85 1.77 12.50 3.06 13.39 3.01 Pⱕ .001 t-test NS NS NS D3 Female 9.85 2.88 10.76 2.28 12.18 2.34 Pⱕ .001 Male 9.15 1.88 13.24 6.28 12.78 3.25 Pⱕ .001 t-test NS NS NS D4 Female 11.66 2.81 12.29 3.00 12.93 3.12 NS Male 10.05 2.68 13.11 2.56 15.59 3.37 Pⱕ .001 t-test NS NS Pⱕ .001 D5 Female 15.02 3.06 16.36 2.83 16.85 2.83 P⫽ .031 Male 13.11 2.28 16.80 3.23 20.25 2.81 Pⱕ .001 t-test P⫽ .022 NS Pⱕ .001
aANOVA indicates analysis of variance.
Table 4. The Results of Statistics Analysis of Measurements among each Stage (ANOVA) and between Males and Females (Student’s t-test) Measurement Sex t-Test Stage 1 Mean SD Stage 2 Mean SD Stage 3 Mean SD ANOVAa H1, mm Female 37.58 6.01 40.92 6.54 43.06 4.83 Pⱕ .001 Male 34.24 6.07 40.17 6.12 44.60 6.49 Pⱕ .001 t-test NS NS NS H2, mm Female 33.61 3.70 35.45 3.63 35.74 2.87 P⫽ .025 Male 33.43 3.05 38.52 4.25 41.08 3.69 Pⱕ .001 t-test NS P⫽ .002 Pⱕ .001 H3, mm Female 54.78 4.92 60.47 6.46 60.36 4.71 Pⱕ .001 Male 57.56 4.88 60.61 6.72 71.66 5.40 Pⱕ .001 t-test NS NS Pⱕ .001 H4, mm Female 13.76 3.16 13.70 2.80 13.94 2.33 NS Male 15.67 2.80 16.64 3.58 15.61 3.08 NS t-test P⫽ .037 Pⱕ .001 Pⱕ .001 H5, mm Female 56.59 4.57 60.66 6.63 63.14 5.28 Pⱕ .001 Male 56.49 5.13 59.49 4.74 68.24 6.01 Pⱕ .001 t-test NS NS Pⱕ .001 H6, mm Female ⫺1.88* 4.44 ⫺2.34* 5.10 ⫺4.09* 3.94 P⫽ .047 Male ⫺1.85* 5.05 ⫺3.58* 4.04 1.69 5.50 Pⱕ .001 t-test NS NS Pⱕ .001 H7, mm Female 11.18 3.36 12.48 4.77 10.30 5.24 NS Male 8.96 3.66 10.66 5.92 14.46 6.12 Pⱕ .001 t-test P⫽ .041 NS Pⱕ .001 H8,⬚ Female 138.76 15.53 144.37 13.05 148.36 11.18 P⫽ .007 Male 135.97 14.61 144.31 12.67 142.05 13.53 NS t-test NS NS P⫽ .006
aANOVA indicates analysis of variance.
* the hyoid bone is above the plane formed by C3 and Me.
dimorphism in the hyoid bone position was evident during young adulthood, which might affect the activity of the muscles and ligaments attached to the hyoid bone, leading to gender differences in the retroepi-glottic-pharyngeal airway depth in young adults.
A previous investigation suggested that the use of
the relative position of the hyoid bone with both the vertebra and mandible may be a more accurate and easier way of evaluating the vertical hyoid bone posi-tion compared with using other reference points or planes.20From our data, we found that the direction of
Figure 4. The dependent variable H7 can be predicted from the
independent variable facial angle in males.
Figure 6. The dependent variable H6 can be predicted from the
independent variable Ar-Go in males.
Figure 5. The dependent variable H7 can be predicted from the
independent variable Ar-Go in females.
Figure 7. The dependent variable H6 can be predicted from the
independent variable facial angle in females.
between genders. From the mixed dentition stage to the permanent dentition stage, the hyoid bone moved upward in females but upward and then downward in males. Through a stepwise regression analysis, we found that the vertical position of the hyoid bone had a strong relationship with the ramus length (Ar-Go) and the facial angle, but the tendency differed com-pletely between genders. In females, a larger facial angle or longer ramus length indicated a more supe-riorly positioned hyoid bone; in males, the indication was reversed. We know that the geniohyoid and my-lohyoid muscles are attached near or at the symphysis of the mandible, and the anterior belly of the digastric muscle also arises from a depression on the inner side of the lower border of the mandible. Adamidis and Spyropoulos21 compared the hyoid bone position in
class I to that in class III malocclusion and concluded that class III patients, especially boys, showed a dif-ferent hyoid bone position, and they deduced that the
suprahyoid muscles might affect mandibular growth. Spyropoulos et al22 conducted animal studies and
proved that the absence of the suprahyoid muscula-ture affects both skeletal growth and the orientation of the mandible. Based on those results, we thought that the suprahyoid muscles play a vital role in relation-ships between the hyoid bone position and mandibular morphology or position, but there might be different ways of regulating them between males and females. OSAHS is reported to affect 9% of males and 4% of females.23OSAHS patients suffer periodic cessation
of airflow during sleep. It is a potentially life-threaten-ing condition because epidemiologic studies have shown that sleep apnea is a risk factor for arterial hy-pertension.24 Numerous cephalometric studies have
tried to find discriminative characteristics of craniofa-cial morphology in OSAHS patients, and a steeper mandibular plane angle, a shorter mandibular body length, and a low hyoid bone position were
consis-tently reported by most investigations.9Does this imply
that a man with a short ramus length or smaller facial angle combined with an inferiorly positioned hyoid bone in his early 20s is predisposed to OSAHS in mid-dle age? We consider it an interesting issue that de-serves further investigation.
CONCLUSIONS
• Developmental changes occur in the pharyngeal air-way depth and hyoid position from childhood to young adulthood.
• Sexual dimorphism appeared in the lower pharyn-geal airway and the direction of change in the ver-tical position of the hyoid bone.
• The findings might shed some light on the reason why some breathing disorders are male predomi-nant.
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