11
 Pharyngeal airway characterization in adolescents related to facial skeletal pattern: A preliminary study L ıgia Vieira Claudino, a Claudia Trindade Mattos, b Ant onio Carlos de Oliveira Ruellas, c and Eduardo Franzotti Sant  Anna c Rio de Janeiro, Brazil Introduction: The objective of this study was to characterize the volume and the morphology of the pharynge al air way in adole sce nt sub jec ts, relating the m to their facial skelet al pattern. Methods: Fifty-four subj ects who had cone-be am computed tomogra phy were divided into 3 gro ups skeletal Class I, Class II, and Class IIIacco rding to thei r ANB angles. The volumes of the upper pharyn gea l por tion and naso pha rynx, and the volume and morphology of the lower pharyngeal portion and its subdivisions (velopharynx, oropharynx, and hypo pha rynx ) were assessed with soft ware (ver sion 11.5; Dolphin Imaging & Manage men t Solu tions, Chatsworth, Calif). The results were compared with the Kruskal-Wallis and the Dunn multiple comparison tes ts to ide nti fy int erg roup dif fer ences . Cor rel ati ons bet wee n var iab les ass ess ed wer e tes ted by the Spearman correlation coef cient. Correlations between the logarithms of airway volumes and the ANB angle valu es were tested as con tinu ous vari able s with linea r regr essi on, con side ring the sexe s as subg rou ps. Results:  The minimum areas in the Class II group (112.9  6 42.9, 126.9  6 45.9, and 142.1  6 83.5 mm 2 ) were signicantly smaller than in Class III group (186.62 6 83.2, 234.5 6 104.9, and 231.1 6 111.4 mm 2 ) for the lowe r phar ynge al port ion, the velo pha rynx , and the orop har ynx, resp ectiv ely, and sign i cantly smaller than the Class I group for the velopharynx (201.8 6 94.7 mm 2 ). The Class II group had a statistically signi cant different morphology than did the Class I and Class III groups in the velopharynx. There was a tendency to de- creased airway volume with increased ANB angl e in the lowe r phar ynge al portion,velopha rynx , and orop hary nx. In the upper pharyngeal portion, nasopharynx, and hypopharynx, there seemed to be no association between the airway volume and the skeleta l patt ern.  Conclusions:  The Class II sub jec ts had small er minimum and mean areas (lower pharyngeal portion, velopharynx, and oropharynx) than did the Class III group and signicantly less uniform velopharynx morphology than did the Class I and Class III groups. A negative corre- lation was observed between the ANB value and airway volume in the lower pharyngeal portion and the velopharynx (both sexes) and in the oropharynx (just in male subjects). (Am J Orthod Dentofacial Orthop 2013;143:799-809) T he upper airway is a structure responsible for one of the main vital functions in the human organ- ism breathing. The interest in studying the upper airway has always been present in orthodontics, and 1 mai n obj ect ive is to clar ify the relationsh ip bet ween pharyn x struc tur es  and craniofacial comple x growth and development. 1-4 Obs tru ctive process es of mor phol ogic , phy siol ogi c, or pathologic nature, such as hypertrophy of adenoids and tonsils, chronicand alle rgic rhinitis, irri tant env iron men- tal fac tors, inf ect ions , congenital nasal def ormi tie s, nasal traumas , polyps, and tumors, are predisposing fac- tors to a blocked upper airway. When that happens, a functional imbalance results in an oral breath ing pat- tern that can alter facial morpho logy  and dental arch forms, generating a malocclusion. 2,5,6 Considering the functional matrix theory proposed  by Moss, 7 the association of respiratory and masticatory fun ctions and swallowing might act on cra niofacial development.  From the Department of Orthodontics, Universidade Federal do Rio de Janeiro,  Rio de Janeiro, Brazil. a  PhD student.  b Substitute professor. c Associate professor. The authors report no commercial, proprietary, or  nancial interest in the prod- ucts or companies described in this article.  Reprint requests to: Eduardo Franzotti Sant  Anna, Avenida Professor Rodolpho  Paulo Rocco, 325 llha do Fund ao, Rio de Janeiro, RJ, CEP: 21941-617, Brazil; e-mail,  eduardo.franzo [email protected]. Submitted, May 2012; revised and accepted, January 2013. 0889-5406/$36.00 Copyright 2013 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2013.01.015 799 ORIGINAL ARTICLE

CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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Page 1: CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 111

Pharyngeal airway characterization in adolescentsrelated to facial skeletal pattern A preliminary

study

Lıgia Vieira Claudinoa Claudia Trindade Mattosb Antonio Carlos de Oliveira Ruellasc

and Eduardo Franzotti Santrsquo Annac

Rio de Janeiro Brazil

Introduction The objective of this study was to characterize the volume and the morphology of the pharyngeal

airway in adolescent subjects relating them to their facial skeletal pattern Methods Fifty-four subjects who had

cone-beam computed tomography were divided into 3 groupsmdashskeletal Class I Class II and Class IIImdash

according to their ANB angles The volumes of the upper pharyngeal portion and nasopharynx and the

volume and morphology of the lower pharyngeal portion and its subdivisions (velopharynx oropharynx and

hypopharynx) were assessed with software (version 115 Dolphin Imaging amp Management Solutions

Chatsworth Calif) The results were compared with the Kruskal-Wallis and the Dunn multiple comparison

tests to identify intergroup differences Correlations between variables assessed were tested by the

Spearman correlation coef1047297cient Correlations between the logarithms of airway volumes and the ANB angle

values were tested as continuous variables with linear regression considering the sexes as subgroups

Results The minimum areas in the Class II group (1129 6 429 1269 6 459 and 1421 6 835 mm2)

were signi1047297cantly smaller than in Class III group (18662 6 832 2345 6 1049 and 2311 6 1114 mm2) for

the lower pharyngeal portion the velopharynx and the oropharynx respectively and signi1047297cantly smaller

than the Class I group for the velopharynx (2018 6 947 mm2) The Class II group had a statistically signi1047297cant

different morphology than did the Class I and Class III groups in the velopharynx There was a tendency to de-

creased airway volume with increased ANB angle in the lower pharyngeal portion velopharynx and oropharynx

In the upper pharyngeal portion nasopharynx and hypopharynx there seemed to be no association between

the airway volume and the skeletal pattern Conclusions The Class II subjects had smaller minimum

and mean areas (lower pharyngeal portion velopharynx and oropharynx) than did the Class III group andsigni1047297cantly less uniform velopharynx morphology than did the Class I and Class III groups A negative corre-

lation was observed between the ANB value and airway volume in the lower pharyngeal portion and the

velopharynx (both sexes) and in the oropharynx (just in male subjects) (Am J Orthod Dentofacial Orthop

2013143799-809)

T he upper airway is a structure responsible for oneof the main vital functions in the human organ-ismmdash breathing The interest in studying the upper

airway has always been present in orthodontics and 1

main objective is to clarify the relationship betweenpharynx structures and craniofacial complex growthand development1-4

Obstructive processes of morphologic physiologic or

pathologic nature such as hypertrophy of adenoids andtonsils chronic and allergic rhinitis irritant environmen-

tal factors infections congenital nasal deformitiesnasal traumas polyps and tumors are predisposing fac-tors to a blocked upper airway When that happensa functional imbalance results in an oral breathing pat-

tern that can alter facial morphology and dental archforms generating a malocclusion256

Considering the functional matrix theory proposed

by Moss7 the association of respiratory and masticatory functions and swallowing might act on craniofacialdevelopment

From the Department of Orthodontics Universidade Federal do Rio de Janeiro

Rio de Janeiro Brazila PhD student bSubstitute professorcAssociate professor

The authors report no commercial proprietary or 1047297nancial interest in the prod-

ucts or companies described in this article

Reprint requests to Eduardo Franzotti Santrsquo Anna Avenida Professor Rodolpho

Paulo Rocco 325 llha do Fund~ao Rio de Janeiro RJ CEP 21941-617 Brazil

e-mail eduardofranzottigmailcom

Submitted May 2012 revised and accepted January 2013

0889-5406$3600

Copyright 2013 by the American Association of Orthodontists

httpdxdoiorg101016jajodo201301015

799

ORIGINAL ARTICLE

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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The literature is controversial when it comes to the

possible associations among respiratory function facialmorphology and occlusion The ways in which variationin the air1047298ow can in1047298uence growth and development are

not completely elucidated These questions remain un-answered because of methodologic limitations relatedto among other factors the multifactorial etiology of

malocclusion the limitations in the cephalometricmethod and the lack of longitudinal studies assessingthe airway89

Many studies have assessed the relationship betweencraniofacial morphology and the pharyngeal airway incephalometric radiographs10-14 However lateralteleradiographs are limited because they reproduce

a 3-dimensional structure in a 2-dimensional way thatdoes not allow the assessment of cross-sectional areasand volumes of these structures1516

Techniques that allow the precise diagnosis of

changes in the upper airway considering their morphol-ogy and volume are fundamental to ensure normaldevelopment of the craniofacial complex in growingsubjects and the choice of an adequate treatmentplan1718

Although it might expose patients to higher levels of

radiation than isolated customary orthodontic digital ra-diography19 cone-beam computed tomography (CBCT)uses a signi1047297cantly reduced radiation dose compared

with medical computed tomography machines and isequivalent to traditional dental imaging methods such

as a full-mouth series2021 CBCT has the advantage of resulting images with good accuracy16182223 Speci1047297c

softwares and their tools make it possible to obtainhighly reliable measurements of osseous structures andfacial characteristics as well as to assess soft tissues in3 dimensions including measurements of the

oropharynx for volume morphology and minimumaxial area Many studies have been developed in thisarea24-32

Guijarro-Martınez and Swennen33 published a sys-tematic review concerning the CBCT analysis of the up-per airway and included 46 clinically or technically

relevant articles from 382 articles from 1968 to 2010found in PubMed (National Library of Medicine NCBI)The results indicate that the 3-dimensional analysis of the upper airway by using CBCT can be accurate and re-liable although important aspects still need to be eluci-dated

The aim of this study was to characterize throughCBCT and 3-dimensional image reconstruction softwarethe volumes of the upper pharyngeal portion andnasopharynx and the volume minimum axial area

and morphology of the lower pharyngeal portionand its subdivisionsmdash velopharynx oropharynx and

hypopharynxmdashin adolescent subjects relating them totheir facial skeletal patterns

MATERIAL AND METHODS

This project was approved by the research ethicscommittee of the Institute of Collective Health Studiesfrom the Universidade Federal do Rio de Janeiro in

Brazil All patients signed a consent form allowing theuse of their orthodontic records

A sample calculation was performed based on themean standard deviation from a previous study31 Asample size of at least 17 patients would be necessary in each group to detect differences of 65 mm2 in theminimum axial area and of 2500 mm3 in the oropharynx

volume with a test power of 080 (a 5 005) The for-mula used was described by Pandis34

The sample was composed of 54 CBCT scans re-quested as part of the initial records needed for diagnosis

and planning of patients starting their orthodontictreatment in the orthodontic clinics of the postgraduateprogram in our school of dentistry All CBCT scans usedso far as orthodontic records in this university were per-formed on 1 device (i-CAT Imaging Sciences Interna-tional Hat1047297eld Pa) according to a standard protocol

(120 kV 5 mA 13 3 17-cm 1047297eld of view 04-mm voxeland 20-second scanning time) The CBCT scans weremade with each subject sitting in a vertical positionand with the Frankfort horizontal plane parallel to theground and in maximum intercuspation

The CBCT scans of patients in the sample were se-lected from the sequential initial records from the clinicsThe following inclusion criteria were used in sample se-lection DICOM 1047297le no previous orthodontic treatmentor other treatment that might interfere with the natural

course of maxillomandibular growth and developmentgood health conditions no airway pathology cranio-cervical inclination between 90 and 110 (since head

posture might interfere with airway volume)35 CBCTimage including the whole fourth cervical vertebra nosevere hyperdivergence (FMA angle 19-30) and agefrom 13 to 20 years The inclination between the palatal

plane and the sella-nasion plane was measured tocharacterize the sample To take the initial angularmeasurements necessary to con1047297rm the inclusion criteriaand distribute the subjects among the groups (ANBand FMA angles and cranio-cervical inclination) 2-dimensional lateral cephalometric radiographs were

created (ray-sum technique) from the CBCT scans inthe software (version 115 Dolphin Imaging amp Manage-ment Solutions Chatsworth Calif) and measurements

were made by an experienced operator (LVC) The

subjects were then divided into 3 groups consideringthe relationship between the maxilla and the mandible

800 Claudino et al

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(ANB angle) Class I (1ANB3) Class II (ANB3)

and Class III (ANB1)31 Fewer Class I and Class III sub- jects met all inclusion criteria than Class II patients Tomaintain the sample size calculated and make thegroups more even random subjects were excluded

from the Class II group using initials and sex No numericparameters were considered

The groups were divided in the following way Class I(17 patients 12 female and 5 male) Class II (20 patients10 female and 10 male) and Class III (17 patients 11 fe-male and 6 male) The mean age of the sample was 1628

years (SD 230 years) and the mean FMA angle was2482 (SD 345) The mean inclination between thepalatal plane and the sella-nasion plane was 840 (SD360) Speci1047297c age and cephalometric characteristicsfor each group are described in Table I

The direct measurements selected for the dimensionalassessment of thepharyngeal airway in this study were (1)upper pharyngeal portion nasopharynx lower pharyn-geal portion velopharynx oropharynx and hypopharynx

volume (2) lower pharyngeal portion velopharynx oro-

pharynx and hypopharynx minimum axial area (3) lowerpharyngeal portiontotal length and upper length and(4)

velopharynx oropharynx and hypopharynx total lengthAll measurements were made with Dolphin Imaging

software The volumes and minimum axial areas weremeasured with the tool for airway volume calculation

in the 3-dimensional mode of the software in the 25

(standard) threshold values The limits for each portionof interest were de1047297ned in the sagittal slice and the soft-

ware automatically calculated the total volume and themost constricted airway area (minimum axial area) inthe region previously set out

The limits adopted for the upper phar yngeal portion were those proposed by El and Palomo27 The lower limit

was de1047297ned by the palatal plane which is the line pass-ing by the anterior nasal spine and posterior nasal spineextended to the pharyngeal posterior wall The upperlimit was de1047297ned as a slice before the nasal septummerges with the pharyngeal posterior wall ( Fig 1)

The lower limit of the nasopharynx segment was the

palatal plane its upper limit was de1047297ned in the sagittal view as the line uniting the posterior nasal spine andthe So (middle point of the sella-basion line) points18

and its posterior limit was de1047297

ned in the sagittal viewas a line approximately perpendicular to the palatalplane that intersects the So point ( Fig 2)

The lower pharyngeal portionrsquos upper limit was thepalatal plane extended to the posterior pharyngeal

wall and the lower limit was the plane parallel to the pal-atal plane that intersected the lower and most anterior

point in the fourth cervical vertebra ( Fig 3) The locationof the minimum axial area in the lower pharyngeal por-

tion was determined using the ratio proposed by Van Holsbeke et al36 between the upper airway length (dis-tance from the upper limit to the minimum axial area)and the total airway length ( Fig 3) The position ratiocan be described as follows location 5 upper airway

lengthtotal airway lengthThe 3 segments assessed in the lower pharyngeal

portionmdash velopharynx oropharynx and hypopharynxmdash were delimited by 4 cross-sectional planes constructed with previously determined points The upper limit of the velopharynx was the palatal plane and the lower

limit was a plane parallel to the palatal plane that in-tersected the uvula ( Fig 4 A) The upper limit of theoropharynx segment was the lower limit of velophar-

ynx and its lower limit was a plane parallel to the pal-atal plane intersecting the upper point of the epiglottis

( Fig 4 B) The upper limit of the hypopharynx was thelower limit of the oropharynx and its lower limit wasa plane parallel to the palatal plane intersecting thelower and most anterior point of the fourth cervical

vertebra ( Fig 4 C )Once volume minimum axial area and total length

of the lower pharyngeal portion velopharynx orophar- ynx and hypopharynx were obtained the mean areaof each segment was calculated using the following ra-tio mean area 5 volumetotal airway length

The morphologic characterizations of the lower pha-ryngeal portion velopharynx oropharynx and hypo-

pharynx were possible by calculation of the followingratio for each segment morphology 5 minimum area

mean area36 This ratio shows whether the area distribu-tion along the upper airway was uniform or irregular

Statistical analysis

All measurements were repeated in 40 of the CBCT

scans after a 2-week interval Calibration of the operator was tested with the intraclass correlation coef 1047297cient

A descriptive analysis including means and standarddeviations was performed for all quantitative variablesThe Kolmogorov-Smirnov test was applied to assess the

Table I Descriptive statistics of age and cephalomet-ric characteristics of patients in all groups classi1047297edaccording to ANB angles

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

Age (y) 1562 (217) 1683 (274) 1628 (174)

FMA () 2451 (237) 2573 (407) 2405 (352)

ANB () 218 (076) 555 (200) 205 (252)

PP-SN () 664 (389)a 87 (321)a 983 (318)a

Different superscript letters mean statistically signi1047297cant difference

(same line)

PP-SN Angle between the palatal plane and the sella-nasion line

Claudino et al 801

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normality of the data No signi1047297cant sex-related differ-ences were found therefore the data were combinedThe Kruskal-Wallis test was used to verify whether there

were statistically signi1047297cant differences (P 005)

among the groups The Dunn multiple comparison test was then used to identify where these differences wereCorrelations among the variables were tested by theSpearman correlation coef 1047297cient The P values were ad-

justed for multiple comparisons Correlations betweenthe logarithms of airway volumes and the ANB angle

values were tested as continuous variables using linear

regression with the sexes as subgroups

RESULTS

The intraclass correlation coef 1047297cient results werehigher than 095 for all variables assessed this con-1047297rmed the operatorrsquos calibration

The Kruskal-Wallis nonparametric test was applied

for all variables since the distribution of some variables was not normal Comparisons among mean values of allgroups for all dimensional variables (except for volumes)assessed for each airway segment are given in Tables IIthrough V

In the lower pharyngeal portion the Class II grouphad a signi1047297cantly smaller (P 0007) upper lengththan did the Class I group The most constricted area

was in the middle portion (50 of the total length) inthe Class II group The Class II group also showed signif-icantly smaller (P 0007) minimum airway area and

mean area than did the Class III group (Table II)

All groups showed variations in lower pharyngealportion morphology characterized by a less uniform dis-tribution of the airway area along the length of thisstructure However no statistically signi1047297cant difference

was found (Table II)

The Class II group had signi1047297cantly smaller (P 001) velopharynx minimum axial area and mean area anda greater morphologic variation than did the Class Iand Class III groups (Table III)

In the oropharynx segment the Class II group showedsigni1047297cantly smaller minimum axial area and mean areathan did the Class III group (Table IV)

Fig 1 Limits of the upper pharyngeal portion A determination of the last axial slice before the nasalseptum fuses with the pharyngeal posterior wall B the re1047298ection of that slice in the sagittal plane de-

1047297nes the upper limit and the palatal plane determines the lower limit

Fig 2 Nasopharynx limits the lower limit is the palatal

plane (pp ) extended to the posterior pharyngeal wall

and the upper limit is the line uniting PNS and So (middle

point in the Ba-S line)

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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No statistically signi1047297cant differences were observedin the hypopharynx segment in any assessed measure-

ments (Table V)The correlation analysis between airway volumes and

the variables FMA age and sex and the correlation

analysis between the palatal plane to sella-nasion andANB angles are shown in Table VI No variable had a cor-

relation with airway volumesThe plots of the correlations between airway volumes

and ANB angle ( Fig 5) showed a tendency in male

Fig 3 Lower pharyngeal portion limits and measurements A Upper limit palatal plane (ANS-PNSline)extended to the pharyngeal posterior wall and lower limit plane parallel to the palatal plane (pp ) inter-

secting the lower and most anterior point in the fourth cervical vertebra (C4 ) the horizontal white line

represents the most constricted axial area (minimum axial area) within these limits Ul Upper length

Tl total length B Axial view of the minimum axial area determined by the software within these limits

Fig 4 Limits used in the lower pharyngeal portion segments A velopharynx upper limit palatal plane(pp ) and lower limit plane parallel to the palatal plane intersecting the uvula ( U ) B oropharynx upper

limit plane parallel to the palatal plane intersecting the uvula (U ) and lower limit plane parallel to the

palatal plane intersecting the upper point in the epiglottis (EP ) C hypopharynx upper limit plane par-

allel to the palatal plane intersecting the upper point in the epiglottis (EP ) and lower limit plane parallel

to the palatal plane intersecting the lower and most anterior point in the fourth cervical vertebra (C4 )

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

Claudino et al 805

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

REFERENCES

1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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The literature is controversial when it comes to the

possible associations among respiratory function facialmorphology and occlusion The ways in which variationin the air1047298ow can in1047298uence growth and development are

not completely elucidated These questions remain un-answered because of methodologic limitations relatedto among other factors the multifactorial etiology of

malocclusion the limitations in the cephalometricmethod and the lack of longitudinal studies assessingthe airway89

Many studies have assessed the relationship betweencraniofacial morphology and the pharyngeal airway incephalometric radiographs10-14 However lateralteleradiographs are limited because they reproduce

a 3-dimensional structure in a 2-dimensional way thatdoes not allow the assessment of cross-sectional areasand volumes of these structures1516

Techniques that allow the precise diagnosis of

changes in the upper airway considering their morphol-ogy and volume are fundamental to ensure normaldevelopment of the craniofacial complex in growingsubjects and the choice of an adequate treatmentplan1718

Although it might expose patients to higher levels of

radiation than isolated customary orthodontic digital ra-diography19 cone-beam computed tomography (CBCT)uses a signi1047297cantly reduced radiation dose compared

with medical computed tomography machines and isequivalent to traditional dental imaging methods such

as a full-mouth series2021 CBCT has the advantage of resulting images with good accuracy16182223 Speci1047297c

softwares and their tools make it possible to obtainhighly reliable measurements of osseous structures andfacial characteristics as well as to assess soft tissues in3 dimensions including measurements of the

oropharynx for volume morphology and minimumaxial area Many studies have been developed in thisarea24-32

Guijarro-Martınez and Swennen33 published a sys-tematic review concerning the CBCT analysis of the up-per airway and included 46 clinically or technically

relevant articles from 382 articles from 1968 to 2010found in PubMed (National Library of Medicine NCBI)The results indicate that the 3-dimensional analysis of the upper airway by using CBCT can be accurate and re-liable although important aspects still need to be eluci-dated

The aim of this study was to characterize throughCBCT and 3-dimensional image reconstruction softwarethe volumes of the upper pharyngeal portion andnasopharynx and the volume minimum axial area

and morphology of the lower pharyngeal portionand its subdivisionsmdash velopharynx oropharynx and

hypopharynxmdashin adolescent subjects relating them totheir facial skeletal patterns

MATERIAL AND METHODS

This project was approved by the research ethicscommittee of the Institute of Collective Health Studiesfrom the Universidade Federal do Rio de Janeiro in

Brazil All patients signed a consent form allowing theuse of their orthodontic records

A sample calculation was performed based on themean standard deviation from a previous study31 Asample size of at least 17 patients would be necessary in each group to detect differences of 65 mm2 in theminimum axial area and of 2500 mm3 in the oropharynx

volume with a test power of 080 (a 5 005) The for-mula used was described by Pandis34

The sample was composed of 54 CBCT scans re-quested as part of the initial records needed for diagnosis

and planning of patients starting their orthodontictreatment in the orthodontic clinics of the postgraduateprogram in our school of dentistry All CBCT scans usedso far as orthodontic records in this university were per-formed on 1 device (i-CAT Imaging Sciences Interna-tional Hat1047297eld Pa) according to a standard protocol

(120 kV 5 mA 13 3 17-cm 1047297eld of view 04-mm voxeland 20-second scanning time) The CBCT scans weremade with each subject sitting in a vertical positionand with the Frankfort horizontal plane parallel to theground and in maximum intercuspation

The CBCT scans of patients in the sample were se-lected from the sequential initial records from the clinicsThe following inclusion criteria were used in sample se-lection DICOM 1047297le no previous orthodontic treatmentor other treatment that might interfere with the natural

course of maxillomandibular growth and developmentgood health conditions no airway pathology cranio-cervical inclination between 90 and 110 (since head

posture might interfere with airway volume)35 CBCTimage including the whole fourth cervical vertebra nosevere hyperdivergence (FMA angle 19-30) and agefrom 13 to 20 years The inclination between the palatal

plane and the sella-nasion plane was measured tocharacterize the sample To take the initial angularmeasurements necessary to con1047297rm the inclusion criteriaand distribute the subjects among the groups (ANBand FMA angles and cranio-cervical inclination) 2-dimensional lateral cephalometric radiographs were

created (ray-sum technique) from the CBCT scans inthe software (version 115 Dolphin Imaging amp Manage-ment Solutions Chatsworth Calif) and measurements

were made by an experienced operator (LVC) The

subjects were then divided into 3 groups consideringthe relationship between the maxilla and the mandible

800 Claudino et al

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(ANB angle) Class I (1ANB3) Class II (ANB3)

and Class III (ANB1)31 Fewer Class I and Class III sub- jects met all inclusion criteria than Class II patients Tomaintain the sample size calculated and make thegroups more even random subjects were excluded

from the Class II group using initials and sex No numericparameters were considered

The groups were divided in the following way Class I(17 patients 12 female and 5 male) Class II (20 patients10 female and 10 male) and Class III (17 patients 11 fe-male and 6 male) The mean age of the sample was 1628

years (SD 230 years) and the mean FMA angle was2482 (SD 345) The mean inclination between thepalatal plane and the sella-nasion plane was 840 (SD360) Speci1047297c age and cephalometric characteristicsfor each group are described in Table I

The direct measurements selected for the dimensionalassessment of thepharyngeal airway in this study were (1)upper pharyngeal portion nasopharynx lower pharyn-geal portion velopharynx oropharynx and hypopharynx

volume (2) lower pharyngeal portion velopharynx oro-

pharynx and hypopharynx minimum axial area (3) lowerpharyngeal portiontotal length and upper length and(4)

velopharynx oropharynx and hypopharynx total lengthAll measurements were made with Dolphin Imaging

software The volumes and minimum axial areas weremeasured with the tool for airway volume calculation

in the 3-dimensional mode of the software in the 25

(standard) threshold values The limits for each portionof interest were de1047297ned in the sagittal slice and the soft-

ware automatically calculated the total volume and themost constricted airway area (minimum axial area) inthe region previously set out

The limits adopted for the upper phar yngeal portion were those proposed by El and Palomo27 The lower limit

was de1047297ned by the palatal plane which is the line pass-ing by the anterior nasal spine and posterior nasal spineextended to the pharyngeal posterior wall The upperlimit was de1047297ned as a slice before the nasal septummerges with the pharyngeal posterior wall ( Fig 1)

The lower limit of the nasopharynx segment was the

palatal plane its upper limit was de1047297ned in the sagittal view as the line uniting the posterior nasal spine andthe So (middle point of the sella-basion line) points18

and its posterior limit was de1047297

ned in the sagittal viewas a line approximately perpendicular to the palatalplane that intersects the So point ( Fig 2)

The lower pharyngeal portionrsquos upper limit was thepalatal plane extended to the posterior pharyngeal

wall and the lower limit was the plane parallel to the pal-atal plane that intersected the lower and most anterior

point in the fourth cervical vertebra ( Fig 3) The locationof the minimum axial area in the lower pharyngeal por-

tion was determined using the ratio proposed by Van Holsbeke et al36 between the upper airway length (dis-tance from the upper limit to the minimum axial area)and the total airway length ( Fig 3) The position ratiocan be described as follows location 5 upper airway

lengthtotal airway lengthThe 3 segments assessed in the lower pharyngeal

portionmdash velopharynx oropharynx and hypopharynxmdash were delimited by 4 cross-sectional planes constructed with previously determined points The upper limit of the velopharynx was the palatal plane and the lower

limit was a plane parallel to the palatal plane that in-tersected the uvula ( Fig 4 A) The upper limit of theoropharynx segment was the lower limit of velophar-

ynx and its lower limit was a plane parallel to the pal-atal plane intersecting the upper point of the epiglottis

( Fig 4 B) The upper limit of the hypopharynx was thelower limit of the oropharynx and its lower limit wasa plane parallel to the palatal plane intersecting thelower and most anterior point of the fourth cervical

vertebra ( Fig 4 C )Once volume minimum axial area and total length

of the lower pharyngeal portion velopharynx orophar- ynx and hypopharynx were obtained the mean areaof each segment was calculated using the following ra-tio mean area 5 volumetotal airway length

The morphologic characterizations of the lower pha-ryngeal portion velopharynx oropharynx and hypo-

pharynx were possible by calculation of the followingratio for each segment morphology 5 minimum area

mean area36 This ratio shows whether the area distribu-tion along the upper airway was uniform or irregular

Statistical analysis

All measurements were repeated in 40 of the CBCT

scans after a 2-week interval Calibration of the operator was tested with the intraclass correlation coef 1047297cient

A descriptive analysis including means and standarddeviations was performed for all quantitative variablesThe Kolmogorov-Smirnov test was applied to assess the

Table I Descriptive statistics of age and cephalomet-ric characteristics of patients in all groups classi1047297edaccording to ANB angles

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

Age (y) 1562 (217) 1683 (274) 1628 (174)

FMA () 2451 (237) 2573 (407) 2405 (352)

ANB () 218 (076) 555 (200) 205 (252)

PP-SN () 664 (389)a 87 (321)a 983 (318)a

Different superscript letters mean statistically signi1047297cant difference

(same line)

PP-SN Angle between the palatal plane and the sella-nasion line

Claudino et al 801

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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normality of the data No signi1047297cant sex-related differ-ences were found therefore the data were combinedThe Kruskal-Wallis test was used to verify whether there

were statistically signi1047297cant differences (P 005)

among the groups The Dunn multiple comparison test was then used to identify where these differences wereCorrelations among the variables were tested by theSpearman correlation coef 1047297cient The P values were ad-

justed for multiple comparisons Correlations betweenthe logarithms of airway volumes and the ANB angle

values were tested as continuous variables using linear

regression with the sexes as subgroups

RESULTS

The intraclass correlation coef 1047297cient results werehigher than 095 for all variables assessed this con-1047297rmed the operatorrsquos calibration

The Kruskal-Wallis nonparametric test was applied

for all variables since the distribution of some variables was not normal Comparisons among mean values of allgroups for all dimensional variables (except for volumes)assessed for each airway segment are given in Tables IIthrough V

In the lower pharyngeal portion the Class II grouphad a signi1047297cantly smaller (P 0007) upper lengththan did the Class I group The most constricted area

was in the middle portion (50 of the total length) inthe Class II group The Class II group also showed signif-icantly smaller (P 0007) minimum airway area and

mean area than did the Class III group (Table II)

All groups showed variations in lower pharyngealportion morphology characterized by a less uniform dis-tribution of the airway area along the length of thisstructure However no statistically signi1047297cant difference

was found (Table II)

The Class II group had signi1047297cantly smaller (P 001) velopharynx minimum axial area and mean area anda greater morphologic variation than did the Class Iand Class III groups (Table III)

In the oropharynx segment the Class II group showedsigni1047297cantly smaller minimum axial area and mean areathan did the Class III group (Table IV)

Fig 1 Limits of the upper pharyngeal portion A determination of the last axial slice before the nasalseptum fuses with the pharyngeal posterior wall B the re1047298ection of that slice in the sagittal plane de-

1047297nes the upper limit and the palatal plane determines the lower limit

Fig 2 Nasopharynx limits the lower limit is the palatal

plane (pp ) extended to the posterior pharyngeal wall

and the upper limit is the line uniting PNS and So (middle

point in the Ba-S line)

802 Claudino et al

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No statistically signi1047297cant differences were observedin the hypopharynx segment in any assessed measure-

ments (Table V)The correlation analysis between airway volumes and

the variables FMA age and sex and the correlation

analysis between the palatal plane to sella-nasion andANB angles are shown in Table VI No variable had a cor-

relation with airway volumesThe plots of the correlations between airway volumes

and ANB angle ( Fig 5) showed a tendency in male

Fig 3 Lower pharyngeal portion limits and measurements A Upper limit palatal plane (ANS-PNSline)extended to the pharyngeal posterior wall and lower limit plane parallel to the palatal plane (pp ) inter-

secting the lower and most anterior point in the fourth cervical vertebra (C4 ) the horizontal white line

represents the most constricted axial area (minimum axial area) within these limits Ul Upper length

Tl total length B Axial view of the minimum axial area determined by the software within these limits

Fig 4 Limits used in the lower pharyngeal portion segments A velopharynx upper limit palatal plane(pp ) and lower limit plane parallel to the palatal plane intersecting the uvula ( U ) B oropharynx upper

limit plane parallel to the palatal plane intersecting the uvula (U ) and lower limit plane parallel to the

palatal plane intersecting the upper point in the epiglottis (EP ) C hypopharynx upper limit plane par-

allel to the palatal plane intersecting the upper point in the epiglottis (EP ) and lower limit plane parallel

to the palatal plane intersecting the lower and most anterior point in the fourth cervical vertebra (C4 )

Claudino et al 803

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

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1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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(ANB angle) Class I (1ANB3) Class II (ANB3)

and Class III (ANB1)31 Fewer Class I and Class III sub- jects met all inclusion criteria than Class II patients Tomaintain the sample size calculated and make thegroups more even random subjects were excluded

from the Class II group using initials and sex No numericparameters were considered

The groups were divided in the following way Class I(17 patients 12 female and 5 male) Class II (20 patients10 female and 10 male) and Class III (17 patients 11 fe-male and 6 male) The mean age of the sample was 1628

years (SD 230 years) and the mean FMA angle was2482 (SD 345) The mean inclination between thepalatal plane and the sella-nasion plane was 840 (SD360) Speci1047297c age and cephalometric characteristicsfor each group are described in Table I

The direct measurements selected for the dimensionalassessment of thepharyngeal airway in this study were (1)upper pharyngeal portion nasopharynx lower pharyn-geal portion velopharynx oropharynx and hypopharynx

volume (2) lower pharyngeal portion velopharynx oro-

pharynx and hypopharynx minimum axial area (3) lowerpharyngeal portiontotal length and upper length and(4)

velopharynx oropharynx and hypopharynx total lengthAll measurements were made with Dolphin Imaging

software The volumes and minimum axial areas weremeasured with the tool for airway volume calculation

in the 3-dimensional mode of the software in the 25

(standard) threshold values The limits for each portionof interest were de1047297ned in the sagittal slice and the soft-

ware automatically calculated the total volume and themost constricted airway area (minimum axial area) inthe region previously set out

The limits adopted for the upper phar yngeal portion were those proposed by El and Palomo27 The lower limit

was de1047297ned by the palatal plane which is the line pass-ing by the anterior nasal spine and posterior nasal spineextended to the pharyngeal posterior wall The upperlimit was de1047297ned as a slice before the nasal septummerges with the pharyngeal posterior wall ( Fig 1)

The lower limit of the nasopharynx segment was the

palatal plane its upper limit was de1047297ned in the sagittal view as the line uniting the posterior nasal spine andthe So (middle point of the sella-basion line) points18

and its posterior limit was de1047297

ned in the sagittal viewas a line approximately perpendicular to the palatalplane that intersects the So point ( Fig 2)

The lower pharyngeal portionrsquos upper limit was thepalatal plane extended to the posterior pharyngeal

wall and the lower limit was the plane parallel to the pal-atal plane that intersected the lower and most anterior

point in the fourth cervical vertebra ( Fig 3) The locationof the minimum axial area in the lower pharyngeal por-

tion was determined using the ratio proposed by Van Holsbeke et al36 between the upper airway length (dis-tance from the upper limit to the minimum axial area)and the total airway length ( Fig 3) The position ratiocan be described as follows location 5 upper airway

lengthtotal airway lengthThe 3 segments assessed in the lower pharyngeal

portionmdash velopharynx oropharynx and hypopharynxmdash were delimited by 4 cross-sectional planes constructed with previously determined points The upper limit of the velopharynx was the palatal plane and the lower

limit was a plane parallel to the palatal plane that in-tersected the uvula ( Fig 4 A) The upper limit of theoropharynx segment was the lower limit of velophar-

ynx and its lower limit was a plane parallel to the pal-atal plane intersecting the upper point of the epiglottis

( Fig 4 B) The upper limit of the hypopharynx was thelower limit of the oropharynx and its lower limit wasa plane parallel to the palatal plane intersecting thelower and most anterior point of the fourth cervical

vertebra ( Fig 4 C )Once volume minimum axial area and total length

of the lower pharyngeal portion velopharynx orophar- ynx and hypopharynx were obtained the mean areaof each segment was calculated using the following ra-tio mean area 5 volumetotal airway length

The morphologic characterizations of the lower pha-ryngeal portion velopharynx oropharynx and hypo-

pharynx were possible by calculation of the followingratio for each segment morphology 5 minimum area

mean area36 This ratio shows whether the area distribu-tion along the upper airway was uniform or irregular

Statistical analysis

All measurements were repeated in 40 of the CBCT

scans after a 2-week interval Calibration of the operator was tested with the intraclass correlation coef 1047297cient

A descriptive analysis including means and standarddeviations was performed for all quantitative variablesThe Kolmogorov-Smirnov test was applied to assess the

Table I Descriptive statistics of age and cephalomet-ric characteristics of patients in all groups classi1047297edaccording to ANB angles

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

Age (y) 1562 (217) 1683 (274) 1628 (174)

FMA () 2451 (237) 2573 (407) 2405 (352)

ANB () 218 (076) 555 (200) 205 (252)

PP-SN () 664 (389)a 87 (321)a 983 (318)a

Different superscript letters mean statistically signi1047297cant difference

(same line)

PP-SN Angle between the palatal plane and the sella-nasion line

Claudino et al 801

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normality of the data No signi1047297cant sex-related differ-ences were found therefore the data were combinedThe Kruskal-Wallis test was used to verify whether there

were statistically signi1047297cant differences (P 005)

among the groups The Dunn multiple comparison test was then used to identify where these differences wereCorrelations among the variables were tested by theSpearman correlation coef 1047297cient The P values were ad-

justed for multiple comparisons Correlations betweenthe logarithms of airway volumes and the ANB angle

values were tested as continuous variables using linear

regression with the sexes as subgroups

RESULTS

The intraclass correlation coef 1047297cient results werehigher than 095 for all variables assessed this con-1047297rmed the operatorrsquos calibration

The Kruskal-Wallis nonparametric test was applied

for all variables since the distribution of some variables was not normal Comparisons among mean values of allgroups for all dimensional variables (except for volumes)assessed for each airway segment are given in Tables IIthrough V

In the lower pharyngeal portion the Class II grouphad a signi1047297cantly smaller (P 0007) upper lengththan did the Class I group The most constricted area

was in the middle portion (50 of the total length) inthe Class II group The Class II group also showed signif-icantly smaller (P 0007) minimum airway area and

mean area than did the Class III group (Table II)

All groups showed variations in lower pharyngealportion morphology characterized by a less uniform dis-tribution of the airway area along the length of thisstructure However no statistically signi1047297cant difference

was found (Table II)

The Class II group had signi1047297cantly smaller (P 001) velopharynx minimum axial area and mean area anda greater morphologic variation than did the Class Iand Class III groups (Table III)

In the oropharynx segment the Class II group showedsigni1047297cantly smaller minimum axial area and mean areathan did the Class III group (Table IV)

Fig 1 Limits of the upper pharyngeal portion A determination of the last axial slice before the nasalseptum fuses with the pharyngeal posterior wall B the re1047298ection of that slice in the sagittal plane de-

1047297nes the upper limit and the palatal plane determines the lower limit

Fig 2 Nasopharynx limits the lower limit is the palatal

plane (pp ) extended to the posterior pharyngeal wall

and the upper limit is the line uniting PNS and So (middle

point in the Ba-S line)

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No statistically signi1047297cant differences were observedin the hypopharynx segment in any assessed measure-

ments (Table V)The correlation analysis between airway volumes and

the variables FMA age and sex and the correlation

analysis between the palatal plane to sella-nasion andANB angles are shown in Table VI No variable had a cor-

relation with airway volumesThe plots of the correlations between airway volumes

and ANB angle ( Fig 5) showed a tendency in male

Fig 3 Lower pharyngeal portion limits and measurements A Upper limit palatal plane (ANS-PNSline)extended to the pharyngeal posterior wall and lower limit plane parallel to the palatal plane (pp ) inter-

secting the lower and most anterior point in the fourth cervical vertebra (C4 ) the horizontal white line

represents the most constricted axial area (minimum axial area) within these limits Ul Upper length

Tl total length B Axial view of the minimum axial area determined by the software within these limits

Fig 4 Limits used in the lower pharyngeal portion segments A velopharynx upper limit palatal plane(pp ) and lower limit plane parallel to the palatal plane intersecting the uvula ( U ) B oropharynx upper

limit plane parallel to the palatal plane intersecting the uvula (U ) and lower limit plane parallel to the

palatal plane intersecting the upper point in the epiglottis (EP ) C hypopharynx upper limit plane par-

allel to the palatal plane intersecting the upper point in the epiglottis (EP ) and lower limit plane parallel

to the palatal plane intersecting the lower and most anterior point in the fourth cervical vertebra (C4 )

Claudino et al 803

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

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18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

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19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

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21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

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22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

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23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

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24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

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25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

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31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

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June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

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33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

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1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

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35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

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36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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normality of the data No signi1047297cant sex-related differ-ences were found therefore the data were combinedThe Kruskal-Wallis test was used to verify whether there

were statistically signi1047297cant differences (P 005)

among the groups The Dunn multiple comparison test was then used to identify where these differences wereCorrelations among the variables were tested by theSpearman correlation coef 1047297cient The P values were ad-

justed for multiple comparisons Correlations betweenthe logarithms of airway volumes and the ANB angle

values were tested as continuous variables using linear

regression with the sexes as subgroups

RESULTS

The intraclass correlation coef 1047297cient results werehigher than 095 for all variables assessed this con-1047297rmed the operatorrsquos calibration

The Kruskal-Wallis nonparametric test was applied

for all variables since the distribution of some variables was not normal Comparisons among mean values of allgroups for all dimensional variables (except for volumes)assessed for each airway segment are given in Tables IIthrough V

In the lower pharyngeal portion the Class II grouphad a signi1047297cantly smaller (P 0007) upper lengththan did the Class I group The most constricted area

was in the middle portion (50 of the total length) inthe Class II group The Class II group also showed signif-icantly smaller (P 0007) minimum airway area and

mean area than did the Class III group (Table II)

All groups showed variations in lower pharyngealportion morphology characterized by a less uniform dis-tribution of the airway area along the length of thisstructure However no statistically signi1047297cant difference

was found (Table II)

The Class II group had signi1047297cantly smaller (P 001) velopharynx minimum axial area and mean area anda greater morphologic variation than did the Class Iand Class III groups (Table III)

In the oropharynx segment the Class II group showedsigni1047297cantly smaller minimum axial area and mean areathan did the Class III group (Table IV)

Fig 1 Limits of the upper pharyngeal portion A determination of the last axial slice before the nasalseptum fuses with the pharyngeal posterior wall B the re1047298ection of that slice in the sagittal plane de-

1047297nes the upper limit and the palatal plane determines the lower limit

Fig 2 Nasopharynx limits the lower limit is the palatal

plane (pp ) extended to the posterior pharyngeal wall

and the upper limit is the line uniting PNS and So (middle

point in the Ba-S line)

802 Claudino et al

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No statistically signi1047297cant differences were observedin the hypopharynx segment in any assessed measure-

ments (Table V)The correlation analysis between airway volumes and

the variables FMA age and sex and the correlation

analysis between the palatal plane to sella-nasion andANB angles are shown in Table VI No variable had a cor-

relation with airway volumesThe plots of the correlations between airway volumes

and ANB angle ( Fig 5) showed a tendency in male

Fig 3 Lower pharyngeal portion limits and measurements A Upper limit palatal plane (ANS-PNSline)extended to the pharyngeal posterior wall and lower limit plane parallel to the palatal plane (pp ) inter-

secting the lower and most anterior point in the fourth cervical vertebra (C4 ) the horizontal white line

represents the most constricted axial area (minimum axial area) within these limits Ul Upper length

Tl total length B Axial view of the minimum axial area determined by the software within these limits

Fig 4 Limits used in the lower pharyngeal portion segments A velopharynx upper limit palatal plane(pp ) and lower limit plane parallel to the palatal plane intersecting the uvula ( U ) B oropharynx upper

limit plane parallel to the palatal plane intersecting the uvula (U ) and lower limit plane parallel to the

palatal plane intersecting the upper point in the epiglottis (EP ) C hypopharynx upper limit plane par-

allel to the palatal plane intersecting the upper point in the epiglottis (EP ) and lower limit plane parallel

to the palatal plane intersecting the lower and most anterior point in the fourth cervical vertebra (C4 )

Claudino et al 803

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

804 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

Claudino et al 805

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

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Ann Arbor Center for Human Growth and Development Univer-

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3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

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198078495-503

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7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

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8 Shapiro PA Effects of nasal obstruction on facial development J

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10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

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11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

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Class II malocclusions and different growth patterns Am J Orthod

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12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

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dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

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14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

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mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

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18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

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137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

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June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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No statistically signi1047297cant differences were observedin the hypopharynx segment in any assessed measure-

ments (Table V)The correlation analysis between airway volumes and

the variables FMA age and sex and the correlation

analysis between the palatal plane to sella-nasion andANB angles are shown in Table VI No variable had a cor-

relation with airway volumesThe plots of the correlations between airway volumes

and ANB angle ( Fig 5) showed a tendency in male

Fig 3 Lower pharyngeal portion limits and measurements A Upper limit palatal plane (ANS-PNSline)extended to the pharyngeal posterior wall and lower limit plane parallel to the palatal plane (pp ) inter-

secting the lower and most anterior point in the fourth cervical vertebra (C4 ) the horizontal white line

represents the most constricted axial area (minimum axial area) within these limits Ul Upper length

Tl total length B Axial view of the minimum axial area determined by the software within these limits

Fig 4 Limits used in the lower pharyngeal portion segments A velopharynx upper limit palatal plane(pp ) and lower limit plane parallel to the palatal plane intersecting the uvula ( U ) B oropharynx upper

limit plane parallel to the palatal plane intersecting the uvula (U ) and lower limit plane parallel to the

palatal plane intersecting the upper point in the epiglottis (EP ) C hypopharynx upper limit plane par-

allel to the palatal plane intersecting the upper point in the epiglottis (EP ) and lower limit plane parallel

to the palatal plane intersecting the lower and most anterior point in the fourth cervical vertebra (C4 )

Claudino et al 803

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

804 Claudino et al

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

Claudino et al 805

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

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10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

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11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

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12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

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1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

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14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subjects toward greater volumes than in females except

for the nasopharynx where there was no difference Inthe lower pharyngeal portion velopharynx and oro-

pharynx the linear regression coef 1047297cient (R2) was moreconsistent the greater the ANB angle the smaller theairway volume In the oropharynx this was signi1047297cantonly in male subjects In the upper pharyngeal portion

nasopharynx and hypopharynx there seemed to be noassociation between airway volume and skeletal pattern

DISCUSSION

The main objective of this study was to assess the vol-umes of the upper pharyngeal portion and nasopharynx

and the volumes the minimum axial areas and the mor-phology of the lower pharyngeal portion and its seg-ments (velopharynx oropharynx and hypopharynx)using CBCT scans of 13- to 20-year-old subjects divided

into Class I Class II and Class III groups according totheir ANB angles

The Dolphin Imaging software we used is userfriendly and provides quick upper airway segmenta-tionmdashgood segmentation sensitivity that can be checkedin 2-dimensional slices (axial coronal and sagittal)mdashandminimum cross-sectional area analysis It is considerably more accurate than orsimilar to other softwares in upper

airway assessments2737 Its disadvantages include cost

lack of tools to adjust or correct the segmentation in2-dimensional slices and threshold interval units thatare not comparable with other imaging softwares37

Many studies have been performed to assess the rela-tionship between upper airway and dentomaxillofacialmorphology using CBCT2526303138 Nevertheless

most of these studies assessed only airway segmentsthat do not necessarily represent the complete upperportion of this complex structure The assessment of the entire upper airway is necessary to establish

a correct diagnosis28 We were concerned with determi-nation of the anatomic limits of the upper airway and its

Table II Intergroup comparison of LPP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

LPP total length (mm) 667 (70)a 670 (78)a 7022 (54)a

LPP upper length (mm) 508 (145)a 3130 (152) b 4681 (1765)ab

LPP minimum area (mm2) 13245 (485)ab 1129 (429)a 18662 (832) b

LPP mean area (mm2) 20538 (687)ab 2118 (529)a 29993 (9316) b

Minimum area location (UlTl) 07 (02)a 05 (02) b 06 (03)ab

LPP morphology (AminAmean) 05 (01)a 05 (01)a 06 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

LPP Lower pharyngeal portion Ul upper airway length Tl total airway length AminAmean minimum areamean area

Table III Intergroup comparison of VP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

VP length (mm) 295 (49)a 287 (41)a 315 (37)a

VP minimum area (mm2) 2018 (947)a 1269 (459) b 2345 (1049)a

VP mean area (mm2) 2910 (936)a 2188 (878) b 3279 (1120)a

VP morphology (AminAmean) 07 (01)a 06 (01) b 07 (02)a

Different superscript letters mean statistically signi1047297cant difference (same line)

VP Velopharynx AminAmean minimum areamean area

Table IV Intergroup comparison of OP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Class III (n 5 17)Mean (SD)

OP length (mm) 1856 (39)a 1473 (54)a 160 (58)a

OP minimum area (mm2) 1602 (626)ab 1421 (835)a 2311 (1114) b

OP mean area (mm2) 2109 (869)ab 1951 (853)a 2834 (1241) b

OP morphology (AminAmean) 076 (01)a 07 (01)a 08 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

OP Oropharynx AminAmean minimum areamean area

804 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

Claudino et al 805

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

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2 Rubin RM The orthodontistrsquos responsibility in preventing facial

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Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

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5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

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7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 711

subdivisions in segments that could be more susceptibleto morphologic changes in Class I Class II and Class IIIsubjects Additionally the assessment of the whole up-per airway represented by the lower pharyngeal portion

was considered necessary The lower pharyngeal portionlimits used in this study are wider than those frequently

used and described in the literatureThe sample division into Class I Class II and Class III

skeletal patterns according to the ANB angle was chosen

because this is one of the most used criteria in the deter-

mination of the anteroposterior relationship betweenthe maxilla and the mandible14283139 Neverthelessthis angle might be in1047298uenced by the anteroposteriorposition of nasion relative to Points A and B amongother factors and some authors have suggested thatthe diagnosis of such discrepancies must be based on

more than 1 anteroposterior appraisal2840-42 Despite

its limitation the ANB angle was used alone becausethe use of 2 criteria to eliminate such limitations is notalways coincident Many studies have demonstratednegative correlations between the oropharynx volumeand the ANB angle314344 Our study showed

signi1047297cant negative correlations between the lowerpharyngeal portion and the velopharynx volumes andthe ANB angle ( Fig 5)

Our sample included subjects with an FMA anglefrom 19 to 30 Therefore no subject with severe man-dibular hypodivergency or hyperdivergency was in-cluded in the sample because this aspect can in1047298uence

airway dimensions as described by Joseph et al45 Theseauthors observed greater pharyngeal anteroposteriornarrowing in hyperdivergent subjects at the levels of the hard palate and the oropharynx the soft-palatetip and the mandible Ucar and Uysal14 reached similarconclusions when comparing craniofacial dimensions

and airway and tongue width in healthy Class I subjects with different vertical growth patterns They observedsmaller nasopharynx airway dimensions in hyperdiver-gent subjects compared with hypodivergent and normo-divergent subjects In our study no correlation was

found between airway volume and FMA angle (Table VI) this is probably because subjects with a severe diver-gence were eliminated from the sample These 1047297ndingsagree with the results of El and Palomo31 in normodiver-gent subjects (FMA angle 19-31) No correlation wasobserved between the inclination of the palatal plane

and the ANB angle (Table VI)The age range in this study was selected to observe

airway differences in growing adolescents with differentskeletal patterns According to Schendel et al17 airway dimensions increase until age 20 years after this mod-erate stability is observed No statistically signi1047297cant dif-

ferences were observed in the upper pharyngeal portionand the nasopharynx volume among our groups Never-theless a slight tendency of increase was observed withan increase of ANB angles ( Fig 5 A and B) These resultsmight be explained by the dif 1047297culty in the assessment of the upper pharyngeal portion volume in areas where na-

sal conchae presented a more complex anatom y Thisdif 1047297culty was also reported by El and Palomo31 How-ever they did not 1047297nd a statistically signi1047297cant smaller

volume in this region in their Class II subjectsSome studies have demonstrated that the parameters

used to determine pharyngeal airway dimensions such

Table V Intergroup comparison of HP dimensional measurements and morphology

Class I (n 5 17)Mean (SD)

Class II (n 5 20)Mean (SD)

Classs III (n 5 17)Mean (SD)

HP length (mm) 192 (54)a 218 (51)a 223 (52)a

HP minimum area (mm2) 1474 (519)a 1496 (530)a 2065 (930)a

HP mean area (mm2) 2241 (592)a 2354 (699)a 2839 (807)a

HP morphology (AminAmean) 06 (01)a 06 (01)a 07 (01)a

Different superscript letters mean statistically signi1047297cant difference (same line)

HP Hypopharynx AminAmean minimum areamean area

Table VI Spearman correlation coef 1047297cients betweenairway volumes and the variables FMA age and sexand between the palatal plane to sella-nasion andANB angles

ANB FMA Age Sex

PP-SN 0045 - - -

UPP volume - 0151 0197 0077

LPP volume - 0050 0229 0299

NP volume - 0107 0356 0094

VP volume - 0011 0185 0260

OP volume - 0183 0052 0404

HP volume - 0023 0162 0178

P 0002 is statistically signi1047297cant (adjusted for multiple compari-

sons)

PP-SN Angle between the palatal plane and the sella-nasion line

UPP upper pharyngeal portion LPP lower pharyngeal portion

NP nasopharynx VP velopharynx OP oropharynx HP hypophar-

ynx

Number 1 was adopted for the male sex and number 2 for the fe-male sex

Claudino et al 805

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7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

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Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 911

as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

American Journal of Orthodontics and Dentofacial Orthopedics June 2013 Vol 143 Issue 6

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1011

CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

REFERENCES

1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

Page 8: CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 811

Fig 5 Plots showing the linear regression analyses between the logarithms of airway volume and the

ANB angle values tested as continuous variables with the sexes as subgroups The blue circles repre-

sent males and the green circles represent females The black line represents the mean correlation of

the entire sample The blue and green lines represent the mean correlations for male and female sub-

jects respectively Segmentsanalyzed A upper pharyngeal portion B nasopharynx C lower pharyn-

geal portion D velopharynx E oropharynx F hypopharynx P 005 P 001 P 0001

806 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 911

as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

American Journal of Orthodontics and Dentofacial Orthopedics June 2013 Vol 143 Issue 6

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1011

CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

REFERENCES

1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

Page 9: CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 911

as volume minimum cross-sectional area length and

form are correlated with obstructive sleep apnea syn-drome and its gravity46-49 The probability of itsdevelopment increases with minimum cross-sectional

area narrowing which is considered severe when it issmaller than 52 mm2 intermediate when it is between52 and 110 mm2 and less severe if it is above 110

mm250 Our Class II subjects had signi1047297cantly smallerlower pharyngeal portions velopharynx and oropharynxminimum axial areas and mean areas than did the ClassIII group and a mean lower pharyngeal portion mini-

mum axial area of 1129 mm2 One subject in the ClassII group even had a minimum axial area smaller than52 mm2 which is considered severe This 1047297nding led to

the conclusion that Class II subjects are more susceptibleto the development of obstructive sleep apnea syndromethan are patients with different skeletal patterns

Additionally studies show that most obstructive

sleep apnea subjectsrsquo airway constriction occurs at thelevel of the oropharynx near the occlusal plane3651 Inthis study the Class II group had smaller minimumaxial areas which were located in the oropharynxsegment

The upper airway morphology is also described in the

literature as a parameter that can predict the chance of obstructions developing in these structures3646 In ourstudy the morphology was characterized by the ratio

between the minimum axial area and the mean axialarea and it was considered more irregular if the value

obtained from the ratio was lower When this ratio inthe lower pharyngeal portion was compared amongthe groups all groups had irregularities in airway morphology as shown by the morphology values(Table II) and no statistically signi1047297cant difference was

found among the groups Nevertheless the velopharynxsegment was more sensitive to morphologic changesand the Class II group had a less uniform area distribu-tion compared with the Class I and Class III groups(Table III)

Another fact from this study was that subjects with

higher ANB values had smaller lower pharyngeal por-

tions and velopharynx volumes and velopharynx mini-mum axial areas compared with the other groupsAlves et al39 reached similar conclusions when evaluat-ing the dimensions of the pharyngeal airway space in50 awake upright children with different anteroposte-rior skeletal patterns using CBTC The patients were di-

vided into 2 groups according to their ANB angles(group I 2

ANB 5 group II ANB 5) Those au-thors concluded that the pharyngeal airway space wasstatistically larger in group I than in group II indicatingthat the dimensions of the pharyngeal airway space areaffected by different anteroposterior skeletal patterns

Additionally our results show that when a negative

correlation was found between airway volume andANB angle (lower pharyngeal portion and velopharynx)a difference between the sexes was notable although

this difference was not enough to trigger a signi1047297

cantcorrelation between airway volume and sex Male sub- jects had greater airway volumes than did f emales this

is similar to the results of Shigeta et al24 who foundlarger airway volumes in men than in women When

we considered the whole lower pharyngeal portionthis difference seemed to decrease with higher ANB

values which meant that men and women with severeskeletal Class II problems have no great differences in

lower pharyngeal portion volumes Speci1047297cally in the ve-lopharynx segment the difference between the sexespersisted no matter what the ANB value

Therefore orthodontists must be aware that speci1047297c

dimensional characteristics such as a greater constrictionmight be associated with the skeletal pattern Dimen-sional airway assessments of the upper airway that in-clude 3- and 2-dimensional measurements such asthose we used in this study are relevant informationfor the orthodontic diagnosis and treatment plan Con-

sidering this information an orthodontist must de1047297nethe best treatment for each patient avoiding treatmentsthat could compromise airway dimensions in those whoare already prone to have smaller dimensions in this

structureThese 1047297ndings should be considered with caution

since this was a preliminary study The small samplesize did not allow an adequate statistical appreciationof the differences between the sexes Based on these re-sults we intend to evaluate a larger sample and to adopt

the lower limit of the oropharynx since the hypopharynxshowed no differences between the groups for any vari-able That will simplify sample selection since many pa-tients were excluded from this study because they didnot have the lower limit adopted (fourth cervical verte-

bra) in the tomographic image

The comparison between Class I and Class III subjectsshowed similar airway dimensions con1047297rmed by the fact

that no statistically signi1047297cant difference was found inany measurement between these groups The Class II

group however had statistically signi1047297cant smaller di-mensions in many segments compared with the other2 groups especially the Class III group this was similarto the 1047297ndings of El and Palomo31

Longitudinal studies of airway changes in subjects

with different skeletal patterns in speci1047297c craniofacialgrowth and development periods should be performedto elucidate detailed knowledge on the relationship be-tween upper airway morphology and function and cra-niomaxillofacial characteristics

Claudino et al 807

American Journal of Orthodontics and Dentofacial Orthopedics June 2013 Vol 143 Issue 6

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1011

CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

REFERENCES

1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

Page 10: CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1011

CONCLUSIONS

Based on the results from this study the following

conclusions can be inferred

1 Class II subjects have smaller minimum and meanareas in the lower pharyngeal portion and the velo-pharynx and oropharynx segments than do Class IIIsubjects

2 No dimensional differences were observed amongthe groups in the hypopharynx segment

3 The velopharynx segment was more sensitive to air- way morphologic changes and the Class II grouphad the greatest irregularity in this region

4 No statistically signi1047297cant difference in airway di-

mensions was observed between the Class I andClass III groups

5 A negative correlation was observed between ANB

value and airway volume in the lower pharyngealportion and the velopharynx (both sexes) and in

the oropharynx only in male subjects

REFERENCES

1 Linder-Aronson S Respiratory function in relation to facial mor-

phology and the dentition Br J Orthod 1979659-71

2 Rubin RM The orthodontistrsquos responsibility in preventing facial

deformity In McNamara JA Jr editor Naso-respiratory function

and craniofacial growth Monograph 9 Craniofacial Growth Series

Ann Arbor Center for Human Growth and Development Univer-

sity of Michigan 1979

3 McNamara JA Jr In1047298uence of respiratory pattern on craniofacial

growth Angle Orthod 198151269-300

4 Kluemper GT Vig PS Vig KW Nasorespiratory characteristics and

craniofacial morphology Eur J Orthod 199517491-5

5 Diamond O Tonsils and adenoids why the dilemma Am J Orthod

198078495-503

6 Bresolin D Shapiro PA Shapiro GG Chapko MK Dassel S Mouth

breathing in allergic children its relationship to dentofacial devel-

opment Am J Orthod 198383334-40

7 Moss-SalentijnL MelvinL Moss and the functional matrixJ Dent

Res 1997761814-7

8 Shapiro PA Effects of nasal obstruction on facial development J

Allergy Clin Immunol 198881967-71

9 Moyers RE Ortodontia 4th ed Rio de Janeiro Brazil Guanabara

Koogan 1991

10 Abu Allhaija ES Al-Khateeb SN Uvulo-glosso-pharyngeal dimen-sions in different anteroposterior skeletal patterns Angle Orthod

2005751012-8

11 de Freitas MR Alcazar NM Janson G de Freitas KM Henriques JF

Upper and lower pharyngeal airways in subjects with Class I and

Class II malocclusions and different growth patterns Am J Orthod

Dentofacial Orthop 2006130742-5

12 Muto T Yamazaki A Takeda S Sato Y Accuracy of predicting

the pharyngeal airway space on the cephalogram after man-

dibular setback surgery J Oral Maxillofac Surg 200866

1099-103

13 Zhong Z Tang Z Gao X Zeng XL A comparison study of upper

airway among different skeletal craniofacial patterns in nonsnor-

ing Chinese children Angle Orthod 201080267-74

14 Ucar FIUysal T Orofacialairwaydimensions in subjects with Class

I malocclusion and different growth patterns Angle Orthod 2011

81460-8

15 Montgomery WM Vig PS Staab EV Matteson SR Computed to-

mography a three-dimensional study of thenasalairway Am J Or-

thod 197976363-7516 Aboudara C Nielsen I Huang JC Maki K Miller AJ Hatcher D

Comparison of airway space with conventional lateral head1047297lms

and 3-dimensional reconstruction from cone-beam computed to-

mography Am J Orthod Dentofacial Orthop 2009135468-79

17 Schendel SA Jacobson R Khalessi S Airway growth and develop-

ment a computerized 3-dimensional analysis J Oral Maxillofac

Surg 2012702174-83

18 Lenza MGLenza MMDalstra M MelsenB Cattaneo PMAn anal-

ysis of different approaches to the assessment of upper airway

morphology a CBCT study Orthod Craniofac Res 201013

96-105

19 Greurounheid T Kokbeck Schieck JR Pliska BT Ahmad M Larson BE

Dosimetry of a cone-beam computed tomography machine com-

pared with a digital x-ray machine in orthodontic imaging Am J

Orthod Dentofacial Orthop 2012141436-4320 Mah JK Danforth RA Bumann A Hatcher D Radiation absorbed

in maxillofacial imaging with a new dental computed tomography

device OralSurg OralMed OralPatholOral RadiolEndod 200396

508-13

21 Loubele M Bogaerts R Van Dijck E Pauwels R Vanheusden S

Suetens P et al Comparison between effective radiation dose of

CBCT and MSCT scanners for dentomaxillofacial applications

Eur J Radiol 200971461-8

22 Kumar V Ludlow JB Mol A Cevidanes L Comparison of conven-

tional and cone beam CT synthesized cephalograms Dentomaxil-

lofac Radiol 200736263-9

23 Hechler LS Cone-beam CTapplicationsin orthodontics Dent Clin

North Am 200852809-23

24 Shigeta Y Ogawa T Venturin J Nguyen M Clark GT Enciso R

Gender- and age-based differences in computerized tomographic

measurements of the orophaynx Oral Surg Oral Med Oral Pathol

Oral Radiol Endod 2008106563-70

25 Grauer D Cevidanes LS Styner MA Ackerman JL Prof 1047297t WR Pha-

ryngeal airway volume and shape from cone-beam computed to-

mography relationship to facial morphology Am J Orthod

Dentofacial Orthop 2009136805-14

26 Iwasaki T Hayasaki H Takemoto Y Kanomi R Yamasaki Y Oro-

pharyngeal airwayin children with Class III malocclusion evaluated

by cone-beam computed tomography Am J Orthod Dentofacial

Orthop 2009136318e1-9 discussion 318-9

27 El H Palomo JM Measuring the airway in 3 dimensions a reliabil-

ity and accuracy study Am J Orthod Dentofacial Orthop 2010

137(Supp)S50e1-9 discussion S50-2

28 Kim YJ Hong JS Hwang YI Park YH Three-dimensional analysisof pharyngeal airway in preadolescent children with different an-

teroposterior skeletal patterns Am J Orthod Dentofacial Orthop

2010137306e1-11 discussion 306-7

29 Zinsly SR Moraes LC Moura P Ursi W Avaliac~ao do espaco aereo

farıngeo por meio da tomogra1047297a computadorizada de feixe

conico Dent Press J Orthod 201015150-8

30 Valiathan M El H Hans MG Palomo MJ Effects of extraction ver-

sus non-extraction treatment on oropharyngeal airway volume

Angle Orthod 2010801068-74

31 El H Palomo JM Airway volume for different dentofacial skeletal

patterns Am J Orthod Dentofacial Orthop 2011139511-21

32 Alves M Jr Baratieri C Nojima LI Nojima MC Ruellas AC Three-

dimensional assessment of pharyngeal airway in nasal- and

808 Claudino et al

June 2013 Vol 143 Issue 6 American Journal of Orthodontics and Dentofacial Orthopedics

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

35 Muto T Takeda S Kanazawa M Yamazaki A Fujiwara Y

Mizoguchi I The effect of head posture on the pharyngeal airway

space (PAS) Int J Oral Maxillofac Surg 200231579-83

36 Van HolsbekeC De BackerJ VosW Verdonck PVan RansbeeckP

Claessens T et al Anatomical and functional changes in the upper

airways of sleep apnea patients due to mandibular repositioning

a large scale study J Biomech 201144442-9

37 Weissheimer A Menezes LM Sameshima GT Enciso R Pham J

Grauer D Imaging software accuracy for 3-dimensional analysis

of the upper airway Am J Orthod Dentofacial Orthop 2012142

801-13

38 Iwasaki T Saitoh I Takemoto Y Inada E Kanomi R Hayasaki H

et al Evaluation of upper airway obstruction in Class II children with 1047298uid-mechanical simulationAm J Orthod DentofacialOrthop

2011139135-45

39 Alves M Jr Franzotti ES Baratieri C Nunes LK Nojima LI

Ruellas AC Evaluation of pharyngeal airway space amongst differ-

ent skeletal patterns Int J Oral Maxillofac Surg 2012231-6

40 Hussels W Nanda RS Analysis of factors affecting angle ANB Am

J Orthod 198485411-23

41 Jacobson A The ldquo Witsrdquo appraisal of jaw disharmony Am J Orthod

197567125-38

42 Ferrario VF Sforza C Miani A Jr Tartaglia GM The use of linear

and angular measurements of maxillo-mandibular anteroposterior

discrepancies Clin Orthod Res 1999234-41

43 Ceylan I Oktay H A study on the pharyngeal size in different

skeletal patterns Am J Orthod Dentofacial Orthop 1995108

69-75

44 Hong JS Park YH Kim YJ Hong SM Oh KM Three-dimensional

changes in pharyngealairway in skeletal Class IIIpatientsundergo-

ing orthognathic surgery J Oral Maxillofac Surg 201169401-845 Joseph AA Elbaum J Cisneros GJ Eisig SB A cephalometric com-

parative study of the soft tissue airway dimensions in persons with

hyperdivergent and normodivergent facial patterns J Oral Maxil-

lofac Surg 199856135-40

46 Enciso R Nguyen M Shigeta Y Ogawa T Clark GT Comparison of

cone-beam CT parameters and sleep questionnaires in sleep apnea

patients and control subjects Oral Surg Oral Med Oral Pathol Oral

Radiol Endod 2010109285-93

47 Abramson Z Susarla S August M Troulis M Kaban L Three-di-

mensional computed tomographic analysis of airway anatomy in

patients with obstructive sleep apnea J Oral Maxillofac Surg

201068354-62

48 Walsh JH Leigh MS Paduch A Maddison KJ Philippe DL

Armstrong JJ et al Evaluation of pharyngeal shape and size using

anatomical optical coherence tomography in individuals with and without obstructive sleep apnoea J Sleep Res 200817230-8

49 Vos W De Backer J Devolder A Vanderveken O Verhulst S

Salgado R et al Correlation between severity of sleep apnea and

upper airway morphology based on advanced anatomical and

functional imaging J Biomech 2007402207-13

50 Ogawa T Enciso R Shintaku WH Clark GT Evaluation of cross-

section airway con1047297guration of obstructive sleep apnea Oral

Surg Oral Med Oral Pathol Oral Radiol Endod 2007103102-8

51 Lowe AA Gionhaku N Takeuchi K Fleetham JA Three-dimen-

sional CT reconstructions of tongue and airway in adult subjects

with obstructive sleep apnea Am J Orthod Dentofacial Orthop

198690364-74

Claudino et al 809

Page 11: CLAUDINO Et Al., 2013. Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

7212019 CLAUDINO Et Al 2013 Pharyngeal Airway Characterization in Adolescents Related to Facial Skeletal Pattern

httpslidepdfcomreaderfullclaudino-et-al-2013-pharyngeal-airway-characterization-in-adolescents-related 1111

mouth-breathing children Int J Pediatr Otorhinolaryngol 2011

751195-9

33 Guijarro-Martınez R Swennen GR Cone-beam computerized to-

mography imaging and analysis of the upper airway a systematic

review of the literature Int J Oral Maxillofac Surg 201140

1227-3734 PandisA Sample calculations forcomparison of 2 meansAm J Or-

thod Dentofacial Orthop 2012141519-21

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