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Introduction: In this study, using a cone-beam computed tomography system, we evaluated the airways of 30
adults. Methods: The shapes of the 3-dimensional volume of the airway were analyzed and compared among
the subjects by using surface superimposition software techniques. Results: The airway had the greatest
variability in the hypopharynx, in the region below the epiglottis, and above the vocal folds. Moderate variation
was apparent at the nares, behind the soft palate, and at the base of the tongue. Conservation of form was seen
at the central portion of the nasal airway surrounding the inferior turbinate. Conclusions: The potential for com-
paring the shape of the airway among subjects is possible. (Am J Orthod Dentofacial Orthop 2011;140:607-15)
M
any studies in orthodontics have focused on to the level of the hard palate and foramen magnum. The
the airway and its potential importance to pharynx’s structural volume increases by approximately
modifying the development of the craniofacial 80% during growth.17 Transverse pharyngeal growth
region. Much of this research has studied how the airway at the pterygoid hamulus is completed at 2 years of
is implicated in developing abnormally long vertical age.18 Choanal width increases about 23% by maturity
facial dimensions.1-3 Orthodontists have also been with remodeling at the pterygoid laminae.17 The sagittal
actively involved in evaluating the airway and treating diameter of the nasopharynx, measured from the poste-
subjects with particular types of sleep apnea.4-6 With rior nasal spine to basion, increases only 9% because of
the advent of low-radiation, rapid computed tomogra- the influence of cranial base flexure (angle formed by
phy (CT) scanning,7-11 the potential for orthodontists sella to nasion to basion), since an acute angle leads to
to assess craniofacial growth in 3 dimensions is now more vertical pharyngeal development.19 Hormion is
available,12,13 and with that analysis is the capability displaced dorsally, increasing the length of the roof of
of evaluating the complete airway.14,15 the nasal cavity, but the posterior nasal spine has an
Determining the airway from images generated by even greater dorsal displacement.20,21 The vomer’s
cone-beam CT (CBCT) includes defining the most effec- dorsal border and the clivus become upright, and the
tive anatomic landmarks. Many previous studies have concurrent descent of the posterior nasal spine and
evaluated the airway by using 2-dimensional cephalo- basion with age tends to reduce the angle of the
metric analyses. Tourne16 showed that the bony naso- nasopharyngeal roof, but this might be cancelled with
pharynx extends from hormion (the most dorsal bone apposition at the pharyngeal aspect of the clivus.
contact point of the vomer on the body of the sphenoid) This growth counters the contribution of the growth
of the spheno-occipital synchondrosis to nasopharyn-
a
Private practice, New Braunfels, Tex. geal depth, and probably contributes to most of the in-
b
Associate clinical professor, Division of Orthodontics, Department of Orofacial crease in pharyngeal depth. The vertebral body of the
Sciences, School of Dentistry, University of California at San Francisco.
c
Professor and chair, Department of Orthodontics, Showa University, Tokyo, atlas might better represent the true posterior limit of
Japan. the anteroposterior dimension of the pharynx, but the
d
Associate clinical professor, Diagnostic Digital Imaging, Sacramento, Calif. growth effects are similar. The contribution of apposi-
e
Professor, Division of Orthodontics, Department of Orofacial Sciences, School of
Dentistry, University of California at San Francisco. tion at the posterior palatine border is minimized relative
The authors report no commercial, proprietary, or financial interest in the prod- to growth at the transpalatal suture and the tuberosities.
ucts or companies described in this article. This backward growth effect is compensated by second-
Reprint requests to: Arthur J. Miller, Division of Orthodontics, Department of
Orofacial Sciences, School of Dentistry, University of California at San Francisco, ary maxillary anterior displacement from cranial base
San Francisco, CA, 94143-0438; e-mail, art.miller@ucsf.edu. growth. The main growth direction of the pharynx is
Submitted, January 2010; revised and accepted, December 2010. vertical, with downward movement of the palate and
0889-5406/$36.00
Copyright Ó 2011 by the American Association of Orthodontists. primarily vertical growth at the spheno-occipital syn-
doi:10.1016/j.ajodo.2010.12.019 chondrosis. Growth at these areas increases the height
607
608 Stratemann et al
of the bony nasopharynx by 38% during childhood,17 impairment, other factors such as a large tongue, large
and this dimension accounts for most of the increase tonsils, or a long, draping velum, could be significant
in pharyngeal capacity, continuing until 13 years of contributing factors.
age (female) or 18 years of age (male).22 These studies can now be complemented by 3-
Adenoid vegetation is the most frequently cited cause dimensional (3D) evaluation of the airway in a subject
of airway obstruction.16 The lymphoid tissue increases seeking orthodontic treatment. Many techniques are ef-
rapidly in size during infancy, slows thereafter, peaks be- fective in evaluating the airway volume and include cine-
fore adolescence, and declines in the adult. Some evi- magnetic resonance imaging,33,34 magnetic resonance
dence from cephalometric studies suggests that the imaging,34,35 spiral CT,36,37 and optical coherence
adenoids increase during the preschool and primary tomography.38 In this article, we propose 1 method using
grade years and then involute during preadolescence CBCT to compare the 3D airway among subjects.39-41
and adolescence.22,23 Lymphoid tissue does facilitate
velopharyngeal closure but can result in blockage of MATERIAL AND METHODS
the airway.1 The absolute size of the adenoids is not as CBCT data sets acquired from 30 patients were used
important as the relative space that the mass occupies in this study. Some scans of patients with pathologic
in the nasopharynx.24 Adenoid obstruction appears to conditions were included, with 4 being evaluated for
be most common among children with a long face and temporomandibular disorders, 1 with a pneumocoele
small nasopharynx.1,25 Persons with the long-face syn- of the right maxillary antrum, and 1 with an odonto-
drome have smaller nasopharyngeal cavities than those genic cyst surrounding an impacted mandibular third
with a square face, so that even a small increase in molar. Scans of subjects with developmental conditions
adenoid bulk could easily cause airway obstruction. such as impacted teeth and orofacial clefts (1 subject)
When the airway is threatened to a sufficient degree were permitted. Selection to homogenize the sample
or at another level than the oropharynx, the postural ad- with respect to age, sex, and ethnicity was not specifi-
aptation of tongue and hyoid will fail to cope, with cally performed. The sample included 13 male and 17
purely nasal respiration becoming an oronasal breathing female subjects with an average age of 22 years 8
pattern, with compensations including parting of the months 6 12 years 1 month (median, 19 years 2
lips, a drop in the mandibular rest position,26 lower1 or months). Most were white (17), followed by Asian (6),
more forward tongue position,27 and extension of the Hispanic (5), and African American (2). The most
head and neck.27,28 common reasons for referral for the CBCT scan were im-
Measurement of nasal obstruction has included pacted teeth (10 subjects) and temporomandibular joint
evaluating cross-sectional area, peak nasal flow, nasal or temporomandibular disorder evaluation (8 subjects).
resistance, and respiratory mode (identifies nasal/oral CBCT data was acquired from 2 systems: the NewTom
airflow ratio). Direct measurement of the ratio of oral QR DVT 9000 (Aperio, Sarasota, Fla) in a private radiology
to nasal airflow is an objective measure of respiratory laboratory in Sacramento, California, and the CB Mercu-
function.29-31 Ray (Hitachi Medico Technology, Tokyo, Japan) at the
Warren et al32 constructed a model of the upper air- Division of Orthodontics, University of California at San
way with a variable nasopharyngeal isthmus and a vari- Francisco.42,43 The patient is supine in the NewTom and
able oral port to determine the effects of airway size and upright with the CB MercuRay; this could modify the
shape on the aerodynamics of simulated breathing, and shape of the airway.36,41 However, the primary purpose
to develop a theoretical basis for predicting when of this study was to demonstrate the variability in airway
breathing mode will change from nasal to predomi- shape and the methods to compare these shapes.
nantly oral. Several theoretical predictions resulted The entire airway as a single unit was threshold-
from their model. A nasal airway cross-sectional area segmented by using the CT numbers of each voxel and
less than 0.4 cm2 might represent an inadequate airway edited by hand with each transverse slice to remove
in adults, and mouth breathing would be expected. The any visible extraneous scatter, artifacts, or background,
amount of adenoid obstruction must be great to affect similar to the method described by Meehan et al.44 For
airway resistance. If airway resistance in the nose were areas with widely different thresholds, a combination
high, large adenoids would be a serious airway problem of threshold segmentation and manual slice editing
and induce mouth breathing. When nasal airway resis- was used to obtain refined surfaces with minimal arti-
tance is high ($4.5 cm H2O/L/s), the mouth will open facts. The segmentation process involved using the
about 0.4 to 0.6 cm2, shifting a significant amount of sculpt tool of CBWorks (CBWorks 1.0; CyberMed Inc.,
air orally and reducing airway resistance to a normal Seoul, Korea) to narrow the scan into a volume of interest
level. If morphologic changes are caused by airway including only the structure that was to be segmented.
November 2011 Vol 140 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Stratemann et al 609
Threshold segmentation tools were used to isolate the were then enlarged or compressed uniformly in the x-,
osseous structures and the airway space from the data. y-, and z- dimensions by hand with the Amira transform
Details in this approach have previously been pub- editor dialog to scale each surface to the same size as the
lished.42,43,45 After segmentation, the resulting set of arbitrary reference surface.
masks (highlighted areas representing each structure of Once the surfaces were aligned and scaled, a subset
interest in each image slice of the CBCT scan) was of 7 landmarks was used to identify the mathematically
rendered into a shaded surface mesh in the CBWorks’ “most average” surface and to rank the remaining sur-
Shaded Surface Display tool. The 30 resulting surface faces relative to it. Because the objects were now of sim-
meshes were exported from CBWorks in a Virtual ilar alignment and size, the remaining differences in the
Reality Modeling Language (.vrl) format into Amira surfaces were primarily related to differences in shape.
software (version 3.1, Mercury Computer Systems, To simplify the analytic calculations, these 7 landmarks,
Berlin, Germany) for further analysis. representing the basic form of each structure, were de-
Due to limitations in the ability of the software to fined and used with all 30 forms including 4 shapes
solve the problem of comparing nonhomeomorphic sur- that did not extend fully rostrally and caudally. The x,
faces (surfaces that do not correspond in topology and y, and z coordinates of the 7 landmarks (Ad, left and
cannot be transformed into one another by continuous right NasA, ConPS, ConPI, IAM-S, PA, and BT; Table)
and invertible mapping) or numbers of nodes (each voxel and the rectangular coordinate values were used.
comprising the surface becomes a node in a tetrahedral By averaging the coordinate data for each data set,
mesh in which each voxel is connected to its 3 nearest the centroid of each coordinate set was determined
neighbors), a reference structure was selected for indi- (Fig 1). Mean centroid coordinates were determined by
rect comparison of the individual surfaces. The reference averaging the coordinate values of the individual cen-
surface consisted of 1 surface model of 1 patient, who troids. All data sets were centered at a common centroid
was considered average as determined from a lateral located at the origin by subtracting the individual cen-
view. The reference surface was nonrigidly transformed troid coordinates from each landmark’s coordinates.
into each individual surface to provide a set of 30 sur- The distance for each landmark of each set to its corre-
faces of identical topology with the same number of no- sponding centroid was then calculated. The average
des. The nonrigid transformation was completed by distance of all landmark points in each set to the cen-
embedding 27 landmarks in each airway by using the troid was determined to be the centroid size of the
Amira landmark tool (Table). Landmarks were embedded data set. If scaling was correct, the data sets should be
pairwise in the arbitrary reference and in each individual of identical centroid size. Manual scaling was generally
structure. The Amira landmarksurfacewarp tool was set within 3% to 5% of the calculated mean centroid size.
in a rigid transformation method to align the surfaces Therefore, a correction factor (ratio of the mean centroid
based on the embedded landmarks. Individual surfaces size to the individual centroid size) was applied to the
American Journal of Orthodontics and Dentofacial Orthopedics November 2011 Vol 140 Issue 5
610 Stratemann et al
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Stratemann et al 611
Fig 4. Lateral view of the surface-rendered volumetric airway from each of the 30 subjects ranked by
the signed root mean square error as compared with the reference surface. The spectrum of shapes
proceeds from the smaller, more vertically oriented airway ( root mean square end) to the larger
and more horizontal airway (1root mean square end). RS is the reference surface with which all
other surfaces were compared. The 7 landmarks to determine the ranking were used in all 30 airways
including 4 volumes that are partially abbreviated rostrally and caudally.
transformation method. The reference surface, which each structure in the sample. First, to remove rotational
was one of the 30 surfaces, was warped to the remaining and translational differences, the warped version of each
29 surfaces in groups of 5, primarily because of limita- surface was aligned to the coordinate system of the over-
tions of the computer hardware and software. Groups all average surface by using the Amira tool, alignsurfa-
for warping were determined by the signed root mean ces, which minimized the root mean square distance
square rank of the individual surfaces, so that surfaces between points of the model surface to the correspond-
1 through 5, 6 through 10, 11 through 15, 16 through ing closest points on the reference surface by using the
20, 21 through 25, and 26 through 30 were clustered iterative closest point algorithm. Colors were set from
together. Each group of 5 surfaces was then combined 0 mm (dark blue) to 3 mm (bright red), and the included
by weighted surface interpolation to yield a local average portion of the spectrum was divided proportionally.
surface. The 6 local average surfaces were then interpo- Color maps were generated for the warped reference sur-
lated again to yield the overall average shape. face version of each airway. An interpolation procedure
With the mean surfaces generated, the next step to similar to that performed to create the local average sur-
make the 3D description of anatomic structures useful faces was completed, yielding 6 local color maps applied
was to add a color map depicting the variability across to the local average surfaces. The 6 local average
American Journal of Orthodontics and Dentofacial Orthopedics November 2011 Vol 140 Issue 5
612 Stratemann et al
Fig 5. Frontal view of the airways ranked by signed root mean square error. RS is the reference surface
with which all other surfaces were compared.
surfaces and their color maps were subsequently put hypopharynx. The airway components were evaluated
through another interpolation step to produce a surface as inside (constricted), similar to, or outside (dilated)
representing the overall mean form with an associated the mean, and assigned respective values of 1, 0, or
color map describing variations of the surface in the 1. The airway had the greatest variability in the hypo-
sample population. pharynx, in the region below the epiglottis and sur-
rounding the vocal folds (Figs 6 and 7). Moderate
RESULTS variation was apparent at the nares, behind the soft
The airways ranked by signed root mean square errors palate, and at the base of the tongue. Conservation
are shown in lateral (Fig 4) and frontal (Fig 5) views. This was seen at the central portion of the nasal airway
spectrum roughly corresponds to thinking of the airways surrounding the inferior turbinate.
as small and more vertical at the minus root mean square
end, and large and more horizontal at the plus root mean DISCUSSION
square end. Asymmetries of the airway were particularly CBCT is suited to aiding our understanding the upper
noted in the frontal views. Extreme narrowing or restric- airway; all of the intricacies are visible and not hidden in
tions were evident in both the lateral and frontal views of the shadows of x-ray projections. In addition, surface
the airway. The distance color map for the airway was data that can be derived from the CT studies can be ma-
imposed on the mean surface along with an aligned nipulated in CT, engineering, and mathematical soft-
and scaled translucent individual airway. For the airway, ware. These types of programs not only improve
constriction of the overall tubular structure was judged visualization of head and neck anatomy, but also
at the nasal airway, nasopharynx, oropharynx, and open orthodontics to the possibilities of integrating
November 2011 Vol 140 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Stratemann et al 613
Fig 6. Six airway color maps, lateral view. Each airway represents a warping of the reference surface
by using groups of 5 surfaces at a time and warping by the signed root mean square rank of the
individual surfaces. Each of these 6 surfaces was combined to yield an overall average shape. The
spectrum ranges from 0 mm (dark blue) to 3 mm (red).
Fig 7. Six airway color maps, frontal aspect. The spectrum ranges from 0 mm (dark blue) to 3 mm (red).
sophisticated morphometric methodologies with a phys- defined predominantly in the central region of the air-
iologic understanding of the fluid dynamics of air pass- way and used for registration across subjects. It was ex-
ing through the nose and throat. The segmentation pected that there would be fewer changes in shape close
techniques used in this study allow incorporation of to the registration center and that greater changes
conventional linear and angular measurements into would be evident farther from the registration site. The
graphic, shape-based strategies that help to describe location of the landmarks and whether they represent
the features of a patient in the context of overall popu- peripheral boundaries of the airway and its general shape
lation variation. can affect the centroid. Although we did not evaluate the
Our data suggest that subjects can vary much more in wide variety of problems and issues that can affect the
the hypopharyngeal region than at the oropharynx or airway, including subjects with chronic sleep apnea,
nasopharynx. However, part of this finding might also this study does demonstrate that the airway has some
depend on the position of the centroid, which was variability in shape. We were particularly interested in
American Journal of Orthodontics and Dentofacial Orthopedics November 2011 Vol 140 Issue 5
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November 2011 Vol 140 Issue 5 American Journal of Orthodontics and Dentofacial Orthopedics
Stratemann et al 615
22. Handelman CS, Osborne G. Growth of the nasopharynx and ade- and 3-dimensional reconstruction from cone-beam computed to-
noid development from one to eighteen years. Angle Orthod mography. Am J Orthod Dentofacial Orthop 2009;135:468-79.
1976;46:243-59. 40. Shi H, Scarfe WC, Farman AG. Upper airway segmentation and di-
23. Linder-Aronson S, Leighton BC. A longitudinal study of the devel- mensions estimation from cone-beam CT image datasets. Int J
opment of the posterior nasopharyngeal wall between 3 and 16 CARS 2006;1:177-86.
years of age. Eur J Orthod 1983;5:47-58. 41. Osoria F, Perilla M, Doyle D, Palomo J. Cone beam computed to-
24. Kerr WJ. The nasopharynx, face height and overbite. Angle Orthod mography: an innovative tool for airway assessment. Anesth Analg
1985;55:31-6. 2008;106:1803-7.
25. Esmile RD, Massler M, Zwemer JD. Mouth breathing: etiology and 42. Stratemann S. 3D craniofacial imaging: airway and craniofacial
effects. J Am Dent Assoc 1952;44:506-21. morphology [thesis]. San Francisco: University of California at
26. Tarvonen P, Koski K. Craniofacial skeleton of 7-year-old children San Francisco; 2005. p. 367.
with enlarged adenoids. Am J Orthod Dentofacial Orthop 1987; 43. Stratemann S, Huang J, Maki K, Miller A, Hatcher D. Comparison
91:300-4. of cone beam computed tomography imaging with physical mea-
27. Ricketts RM. Respiratory obstruction syndrome. Am J Orthod sures. Dentomaxillofac Radiol 2008;37:80-93.
1968;54:495-507. 44. Meehan M, Teschner M, Girod S. Three-dimensional simulation
28. Wenzel A, Hojensgaard E, Henriksen J. Craniofacial morphology and prediction of craniofacial surgery. Orthod Craniofac Res
and head posture in children with asthma and perennial rhinitis. 2003;6(Suppl 1):102-7.
Eur J Orthod 1985;7:83-92. 45. Stratemann SA, Huang JC, Maki K, Hatcher DC, Miller AJ. Evalu-
29. Vig PS, Sarver DM, Hall DJ, Warren DW. Quantitative evaluation of ating the mandible with cone-beam computed tomography. Am
nasal airflow in relation to facial morphology. Am J Orthod 1981; J Orthod Dentofacial Orthop 2010;137(4 Suppl):S58-70.
79:263-72. 46. Aboudara C. Nasopharyngeal airway size determined on lateral
30. Vig PS, Spalding PM, Lints RR. Sensitivity and specificity of cephalometric headfilms and cone-beam CT scans [thesis]. San
diagnostic tests for impaired nasal respiration. Am J Orthod Francisco: University of California at San Francisco; 2003. p. 60.
Dentofacial Orthop 1991;99:354-60. 47. Aboudara CA, Hatcher D, Nielsen IL, Miller A. A three-dimensional
31. Vig PS, Zajac D. Age and gender differences on nasorespiratory evaluation of the upper airway in adolescents. Orthod Craniofac
function. Cleft Palate Craniofac J 1993;30:279-84. Res 2003;6(Suppl 1):173-5.
32. Warren DW, Lehman MD, Hinton VA. Analysis of simulated upper 48. Arens R, McDonough JM, Corbin AM, Rubin NK, Carroll ME,
airway breathing. Am J Orthod 1984;86:197-206. Pack AI, et al. Upper airway size analysis by magnetic resonance
33. Donnelly LF, Surdulescu V, Chini BA, Casper KA, Poe SA, Amin RS. imaging of children with obstructive sleep apnea syndrome. Am
Upper airway motion depicted at cine MR imaging performed J Respir Crit Care Med 2003;167:65-70.
during sleep: comparison between young patients with and 49. Abbott MB, Donnelly LF, Dardzinski BJ, Poe SA, Chini BA,
those without obstructive sleep apnea. Radiology 2003;227:239-45. Amin RS. Obstructive sleep apnea: MR imaging volume segmenta-
34. Fricke BL, Abbott MB, Donnelly LF, Dardzinski BJ, Poe SA, Kalra M, tion analysis. Radiology 2004;232:889-95.
et al. Upper airway volume segmentation analysis using cine MRI 50. Ryan CF, Lowe AA, Li D, Fleetham JA. Magnetic resonance imaging
findings in children with tracheostomy tubes. Korean J Radiol of the upper airway in obstructive sleep apnea before and after
2007;8:506-11. chronic nasal continuous positive airway pressure therapy. Am
35. Arens R, McDonough JM, Costarino AT, Mahboubi S, Rev Respir Dis 1991;144:939-44.
Tayag-Kier CE, Maislin G, et al. Magnetic resonance imaging of 51. Ryan CF, Lowe AA, Li D, Fleetham JA. Three-dimensional upper
the upper airway structure of children with obstructive sleep apnea airway computed tomography in obstructive sleep apnea. A pro-
syndrome. Am J Respir Crit Care Med 2001;164:698-703. spective study in patients treated by uvulopalatopharyngoplasty.
36. Li H, Chen N, Wang C, Shu Y, Wang P. Use of 3-dimensional com- Am Rev Respir Dis 1991;144:428-32.
puted tomography scan to evaluate upper airway patency for pa- 52. Galvin JR, Rooholamini SA, Stanford W. Obstructive sleep apnea:
tients undergoing sleep-disordered breathing surgery. Otolaryngol diagnosis with ultrafast CT. Radiology 1989;171:775-8.
Head Neck Surg 2003;129:336-42. 53. Avrahami E, Englender M. Relation between CT axial
37. Bhattacharyya N, Blake SP, Fried MP. Assessment of the airway in cross-sectional area of the oropharynx and obstructive sleep apnea
obstructive sleep apnea syndrome with 3-dimensional airway syndrome in adults. AJNR Am J Neuroradiol 1995;16:135-40.
computed tomography. Otolaryngol Head Neck Surg 2000;123: 54. Avrahami E, Solomonovich A, Englender M. Axial CT measure-
444-9. ments of the cross-sectional area of the oropharynx in adults
38. Armstrong JJ, Leigh MS, Sampson DD, Walsh JH, Hillman DR, with obstructive sleep apnea syndrome. AJNR Am J Neuroradiol
Eastwood PR. Quantitative upper airway imaging with anatomic 1996;17:1107-11.
optical coherence tomography. Am J Respir Crit Care Med 2006; 55. Tso HH, Lee JS, Huang JC, Maki K, Hatcher D, Miller AJ. Evaluation
173:226-33. of the human airway using cone-beam computerized tomography.
39. Aboudara C, Nielsen I, Huang JC, Maki K, Miller AJ, Hatcher D. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:
Comparison of airway space with conventional lateral headfilms 768-76.
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