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Inuence of temporomandibular joint discdisplacement on craniocervical posture

and hyoid bone position

Jung-Sub An,a Da-Mi Jeon,a Woo-Sun Jung,b Il-Hyung Yang,c Won Hee Lim,d and Sug-Joon Ahne

Seoul, Korea

Introduction: The purpose of this study was to evaluate craniocervical posture and hyoid bone position in or-

thodontic patients with temporomandibular joint (TMJ) disc displacement. Methods: The subjects consisted

of 170 female orthodontic patients who consented to bilateral magnetic resonance imaging of their TMJs.

They were divided into 3 groups based on the results of magnetic resonance imaging of their TMJs: bilateral

normal disc position, bilateral disc displacement with reduction, and bilateral disc displacement without reduc-

tion. Twenty-

ve variables from lateral cephalograms were analyzed with 1-way analysis of variance toinvestigate differences in craniocervical posture and hyoid bone position with respect to TMJ disc

displacement status. Pearson correlation coefcients were calculated to analyze the relationships between

craniofacial morphology and craniocervical posture or hyoid bone position. Results: Subjects with TMJ disc

displacement were more likely to have an extended craniocervical posture with Class II hyperdivergent patterns.

Themost signicant differences werefound between patients with bilateral normal disc position and bilateral disc

displacement without reduction. However, hyoid bone position in relation to craniofacial references was not

signicantly different among the TMJ disc displacement groups, except for variables related to the mandible.

Pearson correlation coefcients indicated that extended craniocervical posture was signicantly correlated

with backward positioning and clockwise rotation of the mandible. Conclusions: This suggests that craniocer-

vical posture is signicantly inuenced by TMJ disc displacement, which may be associated with hyperdivergent

skeletal patterns with a retrognathic mandible. (Am J Orthod Dentofacial Orthop 2015;147:72-9)

Disc displacement of the temporomandibular joint(TMJ) is a common temporomandibular disorder(TMD)1 and refers to an abnormal positional rela-

tionship between thearticular disc and thecondyle, fossa,and articular eminence.2 TMJ disc displacementgenerally progresses from a reducing to a nonreducing state andmay lead to TMJ clicking, crepitus, and in some cases,pain and jaw movement limitations.2-4 Common causesof TMJ disc displacement include trauma andparafunctional habits, such as clenching and bruxism.4

Various imaging techniques are available for evalua-tion of the TMJ, such as transcranial radiography,arthrography, tomography, computed tomography,

and magnetic resonance imaging (MRI).5 Among them, MRI is the only modality that directly depicts the discand is the gold standard in determining articular disc po-sition relative to the condyle and articular eminence

because of its high diagnostic accuracy.6 In addition, italso offers other advantages, such as noninvasiveness,lack of soft tissue distortion, minimal pain, minimal

risk potential, and lack of ionizing radiation exposure.7

Approximately 30% of asymptomatic adults and 82%of symptomatic patients have some f orm of TMJ discdisplacement, as determined by MRI.6

Previous studies have investigated the relationship between TMJ disc displacement and dentofacial charac-teristics in orthodontic patients, reporting that patients

with TMJ disc displacement have decreased posteriorfacial height as well as backward positioning and clock-

wise rotation of the mandible.8,9 Since craniocervical

posture and hyoid bone position can be associated with dentofacial morphology, both of these featurescould be signicantly inuenced by TMJ disc

From the Dental Research Institute and Department of Orthodontics, School of Dentistry, Seoul National University, Seoul, Korea.a Postgraduate student. b Researcher.cAssistant professor.dAssociate professor.e Professor.

All authors have completed and submitted the ICMJE Form for Disclosure of

Potential Conicts of Interest, and none were reported.

Address correspondence to: Sug-Joon Ahn, Dental Research Institute and

Department of Orthodontics, School of Dentistry, Seoul National University,

101 Deahak-ro, Jongno-Gu, Seoul 110-768, Korea; e-mail, [email protected].

Submitted, April 2014; revised and accepted, September 2014.

0889-5406/$36.00

Copyright 2015 by the American Association of Orthodontists.

http://dx.doi.org/10.1016/j.ajodo.2014.09.015

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ORIGINAL ARTICLE

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displacement.10,11 However, the associations between

TMJ disc displacement and craniocervical posture orhyoid bone position have not yet been fully investigated. Although the effects of TMD on

craniocervical posture and hyoid bone position have been investigated, the results remain controversial.Several studies have reported an association between

TMD and craniocervical posture,12-16 but others donot support the connection between T MD andcraniocervical posture or hyoid bone position.17-20 Thepurpose of this study was to investigate therelationships between TMJ disc displacement andcraniocervical posture, and between TMJ discdisplacement and hyoid bone position, using MRI. The

null hypothesis was that no signicant relationships would be found between TMJ disc displacement andcraniocervical posture, or between TMJ discdisplacement and hyoid bone position.

MATERIAL AND METHODS

Female subjects were recruited from patients whoconsented to bilateral MRI of their TMJs. All subjectshad a primary complaint of malocclusion, and routinelateral cephalograms were taken in natural head position

with an Asahi CX-90SP II (Asahi Roentgen, Kyoto, Japan). Natural head position was determined by having the sub-

jects look straight into a mirror in a standing position.21 Achain plumb line was suspended in front of the cassetteto indicate a true vertical line. The MRI images were takento evaluate TMJ status mainly because of TMJ symptomsincluding TMJ sounds, pain, masticatory muscle tender-ness, limited mandibular movement, and locking. Exclu-

sion criteria were (1) age less than 17 years, (2) any systemic disease, (3) history of orthodontic treatment,(4) history of facial cosmetic or orthognathic surgery,(5) history of trauma involving the TMJ, (6) juvenile rheu-matoid arthritis, (7) history of TMJ treatment, (8) airway

obstruction, (9) oral habits, (10)TMJ discdisplacementof a greater severity on the unilateral side, and (11) partial

TMJ disc displacement or TMJ disc displacement withpartial reduction. This research protocol was approved

by the institutional review board of the Seoul National University Dental Hospital (CRI11040).

Radiologists with MRI experience with the TMJ inter-preted the images blinded to the clinical information.According to disc position, TMJ disc status was dividedinto 3 categories as follows.

1 Normal disc position.In theclosed-mouthposition,the

intermediate zone of the disc was interposed betweenthe condyle and the posterior slope of the articulareminence, with the anterior and posterior bandsequally spacedon eitherside of thecondylar loadpoint.

2 Disc displacement with reduction. The disc was ante-riorly displaced relative to the posterior slope of thearticular eminence and the head of the condyle in theclosed-mouth position, but the disc was reduced on

mouth opening.3 Disc displacement without reduction. The disc wasanteriorly displaced relative to the posterior slopeof the articular eminence and the head of thecondyle, and the disc was not reduced on mouthopening.

The position and shape of the articular disc of theTMJ were carefully evaluated according to the classica-tion criteria. We excluded patients with a unilaterally

different disc displacement status because the possibleskeletal morphologies associated with unilateral discdisplacement would be obscured by averaging of the

right and left landmarks used to determine their loca-tion, and unilaterally different disc displacement statusmay asymmetrically inuence craniocervical posture orhyoid bone position, which is dif cult to measure in

lateral cephalometric analysis.22 From the originally selected patients, only those with bilateral normal discstatus (BN), bilateral disc displacement with reduction(DDR), and bilateral disc displacement without reduction

(DDNR) were included in this study.One investigator (S-J.A.), who was blinded to the

clinical information and the disc position, traced alllateral cephalograms. Eighteen landmarks were recorded

on each radiograph using a digitizer with a desktopcomputer, and 25 variables were calculated from these

landmarks: 9 variables for craniocervical posture, 7for hyoid bone position, and 9 for craniofacialmorphology (4 for vertical and 5 for sagittal craniofacialmorphologies). The positions and denitions of thelandmarks are shown in Figure 1, and the locations of the reference planes are shown in Figure 2. Measure-ments for craniocervical posture, hyoid bone position,

and craniofacial morphology are shown in Figures 3, 4,and 5, respectively.

Lateral cephalograms of 20 randomly selected sub-

jects were measured again to test the magnitude of mea-surement errors. The intraclass correlation coef cientsfor the reliability of tracing, landmark identication,

and analytic measurements were greater than 0.98. Descriptive statistics were calculated for all vari-

ables. The differences in the cephalometric variablesfor craniocervical posture, hyoid bone position, and

craniofacial morphology with respect to the TMJ discdisplacement status (BN, DDR, and DDNR) were tested

with 1-way analysis of variance. Scheff e multiple com-parisons were performed at a signicance level of 0.05to analyze between-group relationships. To investigate

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American Journal of Orthodontics and Dentofacial Orthopedics January 2015 Vol 147 Issue 1


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the correlations between craniofacial morphology and

craniocervical posture or hyoid bone position, Pearsoncorrelation coef cients were calculated.

RESULTS

A total of 170 female subjects were included in thisstudy (Table I). Their age range was 17.0 to 50.8 years(mean age, 24.5 6 5.7 years). There were no signicantdifferences in age distribution among the 3 study groups

(data not shown).Table II presents the differences in craniocervical

posture, hyoid bone position, and craniofacialmorphology with respect to TMJ disc displacement sta-tus (BN, DDR, and DDNR). Signicant differences werefound in craniocervical posture between the BN and

DDNR groups (Table II). Subjects with DDNR had larger

angles between the craniofacial reference planes and thecervical vertebrae (FH/CVT, NL/CVT, FH/OPT, and NL/OPT) than did the subjects with BN, indicating that sub-

jects with DDNR had extended craniocervical posturecompared with those with BN. Although the subjects

with DDR demonstrated intermediate values, there was

no signicant difference in craniocervical posture be-tween the BN and DDR groups, or between the DDRand DDNR groups. Angles between the cervical vertebraeand the true horizontal plane (HOR/CVT and HOR/OPT)

or the mandibular plane (MP/CVT and MP/OPT) werenot signicantly different among the 3 groups. Cervical

curvature (OPT/CVT) also did not vary signicantly among the different TMJ disc displacement groups.

Among the variables for hyoid bone position, only measurements related to the mandible were signicantly

inuenced by TMJ disc displacement status. Subjects with DDNR had a decreased hyoid angle (Go/Hy/Me)compared with those with BN or DDR (BN 5

DDR. DDNR). In addition, the hyoidale to the most pro-trusive point of retrognathion distance (Hy-RGn)decreased as TMJ disc displacement status increased inseverityfromBNtoDDNR(BN. DDR. DDNR). However,

distances between craniocervical landmarks or referenceplanes and the hyoid bone (Hy-Ba, Hy to NSL, Hy to NL,

Hy-cv3ia, and Hy to cv3ia-RGn) did not show signicantdifferences according to TMJ disc displacement status(Table II).

Fig 2. Craniocervical reference planes used in this study:

1, nasion-sella line (NSL,planethroughnasion and sella);

2 , true horizontal plane (HOR, true horizontal plane pass-

ing through sella); 3 , Frankfort horizontal plane (FH, plane

through porion and orbitale); 4 , nasal line (NL, line

through the posterior nasal spine and anterior nasal

spine); 5 , mandibular plane (MP, line through gonion

and menton); 6 , cervical vertebrae tangent (CVT, line

through cv2tg and cv4ip); 7 , odontoid process tangent

(OPT, line through cv2tg and cv2ip).

Fig 1. Landmarks used in this study:1, nasion;2 , sella;3 ,

orbitale; 4 , porion; 5 , basion; 6 , anterior nasal spine; 7 ,

posterior nasal spine; 8 , Point A;9 , Point B;10 , pogonion;

11, menton; 12 , gonion; 13 , RGn (most protrusive point of

retrognathion); 14 , hyoidale (Hy, most superior and ante-

rior point on the body of the hyoid bone); 15 , cv2tg

(tangent point of the superoposterior extremity of the sec-

ond cervical vertebra); 16 , cv2ip (most posteroinferior

point on the second cervical vertebra);17 , cv3ia (most an-

teroinferior point on the third cervical vertebra); 18 , cv4ip

(most posteroinferior point on the fourth cervical

vertebra).

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As previously reported, subjects with TMJ discdisplacement have a retrognathic mandi ble with a hy-perdivergent skeletal pattern (Table II).8,9 Our study

showed that increased ANB, and decreased SNB and Nperpendicular to pogonion (PNP), are specic sagittal

craniofacial morphologies in subjects with TMJ discdisplacement. In addition, these skeletal characteristics

became more severe as TMJ disc displacementprogressed from BN to DDNR. However, variables

representing maxillary position (SNA and Nperpendicular to point A [ANP]) were not signicantly different among the 3 groups. Subjects with DDNRhad a hyperdivergent skeletal pattern: eg, increased

Frankfort-mandibular plane angle (FMA), decreasedposterior facial height (PFH), and decreased facial heightratio (FHR) compared with those with BN or DDR. In

contrast to sagittal craniofacial morphology, verticalcraniofacial morphology did not vary signicantly be-tween the BN and DDR groups (Table II).

Correlations between craniofacial morphology andcraniocervical posture or hyoid bone position are

presented in Table III. Generally, craniocervical posture

(FH/CVT, NL/CVT, FH/OPT, and NL/OPT) was signi-cantly correlated with variables representing sagittal(ANB, SNB, and PNP) and vertical (FMA and FHR)craniofacial morphologies, and subjects with extendedcraniocervical posture had a retrognathic mandible

with a hyperdivergent skeletal pattern. However, cervical

curvature (OPT/CVT) was not signicantly correlated with craniofacial morphology.

The hyoid angle (Go/Hy/Me) and the distance be-

tween the hyoidale and the most protrusive point of ret-rognathion (Hy-RGn) were signicantly correlated with

craniofacial morphologic variables (Table III). Both values decreased as the skeletal pattern became more hy-

perdivergent (increased FMA and decreased FHR) and asthe mandible was located more posteriorly (increasedANB and decreased SNB and PNP).

DISCUSSION

The relationships between TMJ status and craniocervical posture have not been fully addressed, specically in orthodontic patients. This may be due to the

Fig 4. Variables of the hyoid bone position (all are linear

measurements except for Go/Hy/Me): 1, linear distance

between the hyoidale and basion (Hy-Ba); 2 , perpendic-

ular distance between the hyoidale to nasion-sella line

(Hy to NSL); 3 , perpendicular distance between the hyoi-

dale to nasal line (Hy to NL); 4 , linear distance between

the hyoidale and RGn (Hy-RGn); 5 , linear distance be-

tween the hyoidale and cv3ia (Hy-cv3ia);6 , perpendicular

distance between the hyoidale and cv3ia-RGn plane (Hy

to cv3ia-RGn, positive when the Hy is located below the

cv3ip-RGn plane); 7 , hyoid angle, angle of Go-Hy-Me

(Go/Hy/Me, the angle is larger when the hyoidale is

located above the mandibular plane).

Fig 3. Variables of craniocervical posture (all are angular

measurements): 1, true horizontal plane to cervical verte-

brae tangent angle (HOR/CVT); 2 , Frankfort horizontal

plane to cervical vertebrae tangent angle (FH/CVT); 3 ,

nasal line to cervical vertebrae tangent angle (NL/CVT);

4 , mandibular plane to cervical vertebrae tangent angle

(MP/CVT); 5 , true horizontal plane to odontoid process

tangent angle (HOR/OPT); 6 , Frankfort horizontal plane

to odontoid process tangent angle (FH/OPT); 7 , nasal

line to odontoid process tangent angle (NL/OPT); 8 ,

mandibular plane to odontoid process tangent angle

(MP/OPT); 9 , the cervical curvature, downward-opening

angle between odontoid process tangent and cervical

vertebrae tangent (OPT/CVT, positive when the cv4ip is

located on the left side of odontoid process tangent).

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methodologic problems of previous studies, such asinadequate sample sizes and subjective criteria for clas-sifying TMJ status.12,13,17,18,23 In this study, we used alarge sample size (170 subjects) including a control

group (BN TMJs). In addition, the subjects wereobjectively classied with MRI of their TMJs, not withsubjective signs and symptoms. Furthermore, thesubjects were carefully controlled. Only subjects withthe same TMJ disc displacement conditions bilaterally

were included. Men were excluded to prevent skewingthe cephalometric measurements with sex-related dif-

ferences. To prevent growth-related size differences,only female patients over the age of 17 years wereselected.24

This study showed an association between TMJ discdisplacement and craniocervical posture. Subjects with

DDNR had increased FH/CVT, NL/CVT, FH/OPT, and

NL/OPT compared with those with BN (Table II).Although there were no signicant differences in the an-gles between the BN and DDR groups, or between the

DDR and DDNR groups, there was a tendency towardincreased angles between the craniofacial referenceplanes and the cervical vertebrae as TMJ disc displace-

ment progressed from BN to DDNR. This means thathead or cervical posture can change according to TMJdisc displacement status. Since neither angle betweenthe cervical vertebrae and the true horizontal plane(HOR/CVT and HOR/OPT) or the cervical curvature(OPT/CVT) was signicantly different among the 3 discdisplacement statuses, head posture may rotate above

the second vertebra without changes in cervical vertebralposition in relation to the true horizontal plane.Although direct comparison was not possible, our nd-ings are similar to those of previous studies reporting

that patients with TMD have a more extended craniocervical posture than the control group, without signicantdifferences in cervical curvature,12 and that there are nosignicant differences in the curvature of the cervical

vertebrae between the third and seventh vertebrae aftercomparing cervical vertebral alignment bet ween sub-

jects with TMD and volunteers without TMD.19

Despite changes in head posture, the positional rela-tionships between the cervical vertebrae and themandibular plane (MP/CVT and MP/OPT) did not showsignicant differences among the 3 TMJ groups. This

might be because mandibular position is signicantly associated with TMJ disc displacement status. Subjects

with TMJ disc displacement generally had an increasedmandibular plane angle with extended craniocervicalposture (Table II). Because both cervical vertebrae andthe mandible are rotated clockwise in relation to the

craniofacial reference planes in subjects with TMJ discdisplacement, there may be no signicant differences

in relationships between the cervical vertebrae and themandibular plane.

The association between TMJ disc displacement andextended craniocervical posture can be explained in 2

ways. The rst possibility is that extended craniocervicalposture may inuence TMJ disc displacement. Previousstudies have reported that abnormal craniocervicalposture is an etiologic factor of TMD, postulating thatas the cranium rotates backward, the mandibular denti-tion will be located more posteriorly in relation to themaxillary dentition; in turn, the mandible will be

advanced to obtain occlusal support.12,13 Increasedmuscular activity that develops as a result will lead todisc displacement.12,13 Although the subjects with TMJdisc displacement had a more extended craniocervicalposture in this study, they had a more posteriorly

Fig 5. Variables of craniofacial morphology: 1, Frankfort

horizontal plane to mandibular plane angle (FMA); 2 ,

anterior facial height (AFH, linear distance between na-

sion and menton); 3 , posterior facial height (PFH, linear

distance between sella and gonion); 4 , ANB angle; 5 ,

SNA angle; 6 , SNB angle; 7 , N perpendicular to Point A

(ANP); 8 , N perpendicular to pogonion (PNP); 9 , facial

height ratio (FHR, ratio of posterior facial height [3 ] to

anterior facial height [2 ]).

Table I. Number and age distribution of subjects with

BN, DDR, and DDNR

Group BN DDR DDNR Total

Subjects, n (%) 53 (31.2) 55 (32.4) 62 (36.5) 170 (100)

Age (y)

Mean 23.7 6 6.6 25.1 6 5.4 24.6 6 5.3 24.5 6 5.7

Range 18.3-50.8 17.3-42.0 17.0-41.0 17.0-50.8

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located mandible than did subjects with BN (Table II);this differs from previous studies.

The second possibility is that TMJ disc displacement

may induce extended craniocervical posture. Previousstudies have reported that the severity of TMJ discdisplacement increases as the sagittal skeletal classica-tion changes from skeletal Class III to skeletal Class II,and the vertical skeletal classication changes from hy-podivergent to hyperdivergent.8,9,25 As a result, subjects

with skeletal Class II or hyperdivergent deformities have

a high possibility of severe TMJ disc displacement. Inaddition, experimentally induced TMJ discdisplacement leads to signicant impairment of

vertical and horizontal mandibular growth, and theamount of vertical or horizontal skeletal changegradually increased as TMJ disc displacement increased

in severity in animal studies.26,27 Because TMJ discdisplacement frequently occurs during puberty, itseems that TMJ disc displacement can lead to aretrognathic mandible with a hyperdivergent skeletal

pattern; this in turn may reduce upper airway space with the same craniocervical posture.28 Therefore,

extended craniocervical posture associated with TMJdisc displacement may result from protective responsesto maintain upper airway space. This hypothesis is sup-

ported by our ndings, indicating that extended cranio-cervical posture is positively related to a hyperdivergentand Class II skeletal pattern (Table III). de Farias Netoet al16 also postulated that in the patients with TMD,altered mobility of the articular disc limits the biome-chanics of mouth opening and triggers compensatory extension of the cervical vertebrae to prevent compres-

sion of the upper airway. However, the cause-and-effect relationships are not clear because the results

were derived from cross-sectional data.Interestingly, TMJ disc displacement did not signi-

cantly inuence the positional relationships of the hyoid bone to the craniofacial references and the cervical

vertebrae, but it signicantly inuenced the positionalrelationships of the hyoid bone to the mandible (Go/

Hy/Me and Hy-RGn) (Table II). Subjects with TMJ discdisplacement, and specically those with DDNR, had a

smaller hyoid angle (Go/Hy/Me) and a shorter hyoidaleto the most protrusive point of retrognathion distance

Table II. Comparisons of cephalometric variables among the BN, DDR, and DDNR groups

Variable BN DDR DDNR Signi cance z Multiple comparisons

Craniocervical posture

HOR/CVT () 98.7 6 6.9 99.5 6 5.8 99.6 6 5.9 NS

FH/CVT () 96.6 6 8.2 98.3 6 6.3 100.3 6 7.1 * BN\ DDNR NL/CVT () 96.1 6 8.7 98.3 6 6.4 99.6 6 6.9 * BN\ DDNR

MP/CVT () 67.3 6 8.8 67.6 6 7.0 64.7 6 8.5 NS

HOR/OPT () 93.6 6 7.4 94.9 6 7.1 94.7 6 6.4 NS

FH/OPT () 91.5 6 8.5 93.7 6 7.3 95.4 6 7.4 * BN\ DDNR

NL/OPT () 91.0 6 8.8 93.7 6 7.2 94.7 6 7.1 * BN\ DDNR

MP/OPT () 62.2 6 8.6 63.0 6 7.9 59.8 6 8.5 NS

OPT/CVT () 5.1 6 2.8 4.6 6 2.9 4.9 6 2.5 NS

Hyoid bone position

Hy-Ba (mm) 76.3 6 5.6 77.0 6 6.0 75.1 6 6.1 NS

Hy to NSL (mm) 107.0 6 6.4 108.2 6 7.6 108.4 6 6.4 NS

Hy to NL (mm) 60.7 6 5.2 61.8 6 6.0 62.6 6 5.7 NS

Hy-RGn (mm) 38.4 6 5.7 35.5 6 5.5 32.3 6 5.5 y BN . DDR . DDNR

Hy-cv3ia (mm) 36.2 6 3.8 36.5 6 3.0 35.2 6 3.4 NS

Hy to cv3ia-RGn (mm)

1.56

6.1 0.06

5.0 0.56

5.9 NSGo/Hy/Me () 154.3 6 18.0 151.0 6 14.8 143.4 6 15.1 * BN 5 DDR . DDNR

Vertical craniofacial morphology

FMA () 28.9 6 7.0 30.6 6 6.7 35.5 6 7.0 y BN 5 DDR\ DDNR

FHR (ratio) 0.63 6 0.06 0.62 6 0.05 0.59 6 0.06 y BN 5 DDR . DDNR

AFH (mm) 132.8 6 5.5 133.7 6 6.5 133.3 6 6.0 NS

PFH (mm) 83.7 6 7.6 82.6 6 6.6 77.9 6 6.7 y BN 5 DDR . DDNR

Sagittal craniofacial morphology

ANB () 2.4 6 4.5 5.1 6 2.4 7.7 6 2.8 y BN\ DDR\ DDNR

SNA () 81.1 6 3.1 81.6 6 3.2 81.4 6 2.8 NS

SNB () 78.7 6 4.9 76.5 6 2.9 73.8 6 3.6 y BN . DDR . DDNR

ANP (mm) 1.7 6 3.0 2.3 6 2.8 1.5 6 3.2 NS

PNP (mm) 1.32 6 10.43 6.32 6 6.65 14.05 6 7.73 y BN . DDR . DDNR

NS , Not signicant.

*P \

0.05;

y

P \

0.001;

z

Scheff e multiple comparisons were used to analyze the intergroup difference at the level of

a 50.05.

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(Hy-RGn) than did the subjects with BN, whereas the dis-tances between the hyoid bone and the craniofacial ref-erences (Hy-Ba, Hy to NSL, and Hy to NL) or the cervical

vertebrae (Hy-cv3ia), and the relationship between the

hyoid bone and the craniocervical reference (Hy tocv3ia-RGn), were not signicantly different among the

3 TMJ disc displacement groups. The relationship be-tween the hyoid bone and the mandible can be explained

by the compensatory response of the hyoid bone to pre-serve upper airway space. It seems that the position of the hyoid bone may not signicantly change duringthe protective process, which maintains the pharyngealairway space and swallowing functions against back-

ward positioning and clockwise rotation of the mandibleassociated with TMJ disc displacement. As a result, the

subjects with TMJ disc displacement have backwardpositioning and clockwise rotation of the mandible

with a relatively stable hyoid bone position, which may

change the positional relationships of the hyoid boneto the mandible signicantly. This hypothesis is partly supported by previous research that found no signicant

differences in hyoid bone positions between subjects with and without TMD.19 Other research regardingTMJ disc displacement status with MRI also documentedthat the position of the hyoid bone was not signicantly

different between subjects with a normal disc positionand those with disc displacement.20

Generally, the facial prole is important in the diag-nosis and treatment planning for orthodontic patients.This study showed that TMJ disc displacement can

inuence craniocervical posture, although the cause-and-effect relationship remains unclear. As a result,in subjects with TMJ disc displacement, the retro-gnathic prole is compromised by extending their

craniocervical posture despite the backward positioningand rotation of the mandible. Recently, the importance

of the soft tissue paradigm has been emphasized, and anormal soft tissue proportion is considered a primary

treatment goal in orthodontic or surgical-orthodontictreatment.29-31 Because craniocervical posture isdirectly related to the soft tissue prole of the face,this study suggests that clinicians should carefully evaluate relationships between the craniocervicalposture and the facial prole in patients withpotential TMJ disc displacement before orthodontic

treatment.This study has the following limitations. The causal

relationships between TMJ disc displacement and cra-

niocervical posture, or between TMJ disc displacementand the hyoid bone position, are not clear becauseour results were derived from cross-sectional data. In

addition, these results are based on lateral cephalo-grams with static posture; hence, they do not showthe function associated with mandibular kinetics.

Further studies with longitudinal data are needed to

clarify the relationships of intra-articular distance,mandibular kinematics, and mandibular loading with

craniocervical posture. This would be helpful for thediagnosis and treatment planning of patients withTMJ disc displacement.

Table III. Correlations between craniofacial morphology and craniocervical posture or hyoid bone position

Variable

Correlation

FMA FHR AFH PFH ANB SNA SNB ANP PNP

Craniocervical posture HOR/CVT () 0.241y NS 0.196* NS 0.240y 0.169* 0.332y 0.153* 0.334y

FH/CVT () 0.381y 0.247y 0.270y NS 0.399y 0.205y 0.499y 0.316y 0.591y

NL/CVT () 0.256y 0.192* 0.262y NS 0.315y 0.248y 0.454y 0.193* 0.416y

MP/CVT () 0.547y 0.556y NS 0.512y NS NS NS NS NS

HOR/OPT () 0.258y 0.154* 0.153* NS 0.242y 0.168* 0.333y NS 0.325y

FH/OPT () 0.396y 0.256y 0.234y NS 0.399y 0.207y 0.501y 0.290y 0.578y

NL/OPT () 0.283y 0.208y 0.231y NS 0.326y 0.253y 0.467y 0.178* 0.422y

MP/OPT () 0.498y 0.519y NS 0.468y NS NS NS NS NS

OPT/CVT () NS NS NS NS NS NS NS NS NS

Hyoid bone position

Hy-Ba (mm) NS 0.152* 0.247y 0.281y 0.162* 0.162* 0.257y NS 0.174*

Hy to NSL (mm) NS NS 0.341y 0.289y NS 0.281y NS NS NS

Hy to NL (mm) 0.237y NS 0.247y NS 0.236y NS 0.161* NS 0.267y

Hy-RGN (mm) 0.519y 0.388y NS 0.396y 0.584y NS 0.421y NS 0.562y

Hy-cv3ia (mm) 0.181* 0.191* 0.165* 0.278y NS NS NS NS NS

Hy to cv3ia-RGn (mm) NS NS NS NS 0.174* NS NS NS NS

Go/Hy/Me () 0.385y 0.358y 0.168* 0.447y 0.324y NS 0.339y 0.151* 0.367y

NS , Not signicant.

*Pearson correlation is signicant at the .05 level; y Pearson correlation is signicant at the .01 level.

78 An et al


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8/8

CONCLUSIONS

This study was performed to evaluate the relation-

ships between TMJ disc displacement and craniocervicalposture, and between TMJ disc displacement and hyoid

bone position, in adult orthodontic patients. The subjects with TMJ disc displacement were more likely tohave an extended craniocervical posture with Class II hy-perdivergent patterns. In contrast, hyoid bone position

was relatively stable irrespective of TMJ disc displace-

ment status. Therefore, the null hypothesis of our study was partially rejected. Extended craniocervical posture was signicantly correlated with backward positioningand clockwise rotation of the mandible. This study sug-gests that craniocervical posture is signicantly inu-enced by TMJ disc displacement, which may be

associated with a hyperdivergent skeletal pattern with

a retrognathic mandible.

REFERENCES

1. Liu MQ, Chen HM, Yap AU, Fu KY. Condylar remodeling accompa-

nying splint therapy: a cone-beam computerized tomography

study of patients with temporomandibular joint disk displacement.

Oral Surg Oral Med Oral Pathol Oral Radiol 2012;114:259-65.

2. Dolwick MF, Katzberg RW, Helms CA. Internal derangements of

the temporomandibular joint: fact or ction? J Prosthet Dent

1983;49:415-8.

3. Murakami S, Takahashi A, Nishiyama H, Fujishita M, Fuchihata H.

Magnetic resonance evaluation of the temporomandibular joint

disc position and conguration. Dentomaxillofac Radiol 1993;

22:205-7.

4. Okeson JP. Management of temporomandibular disorders and

occlusion. St Louis: Elsevier/Mosby; 2013.

5. Westesson PL. Reliability and validity of imaging diagnosis of

temporomandibular joint disorder. Adv Dent Res 1993;7:137-51.

6. Tasaki MM, Westesson PL, Isberg AM, Ren YF, Tallents RH. Classi-

cation and prevalence of temporomandibular joint disk displace-

ment in patients and symptom-free volunteers. Am J Orthod

Dentofacial Orthop 1996;109:249-62.

7. Nebbe B, Major PW. Prevalence of TMJ disc displacement in a pre-

orthodontic adolescent sample. Angle Orthod 2000;70:454-63.

8. Nebbe B, Major PW, Prasad N. Female adolescent facial pattern

associated with TMJ disk displacement and reduction in disk

length: part I. Am J Orthod Dentofacial Orthop 1999;116:

168-76.

9. Kwon HB, Kim H, Jung WS, Kim TW, Ahn SJ. Gender differences indentofacial characteristics of adult patients with temporomandib-

ular disc displacement. J Oral Maxillofac Surg 2013;71:1178-86.

10. Solow B, Sandham A. Cranio-cervical posture: a factor in the

development and function of the dentofacial structures. Eur J

Orthod 2002;24:447-56.

11. Adamidis IP, Spyropoulos MN. Hyoid bone position and orienta-

tion in Class I and Class III malocclusions. Am J Orthod Dentofacial

Orthop 1992;101:308-12.

12. Huggare JA, Raustia AM. Head posture and cervicovertebral and

craniofacial morphology in patients with craniomandibular

dysfunction. Cranio 1992;10:173-7.

13. Nicolakis P, Nicolakis M, Piehslinger E, Ebenbichler G, Vachuda M,

Kirtley C, et al. Relationship between craniomandibular disorders

and poor posture. Cranio 2000;18:106-12.

14. D'Attilio M, Epifania E, Ciuffolo F, Salini V, Filippi MR, Dolci M,

et al. Cervical lordosis angle measured on lateral cephalograms;

ndings in skeletal Class II female subjects with and withoutTMD: a cross sectional study. Cranio 2004;22:27-44.

15. Munhoz WC, Marques AP, Siqueira JT. Radiographic evaluation of

cervical spine of subjects with temporomandibular joint internal

disorder. Braz Oral Res 2004;18:283-9.

16. de Farias Neto JP, de Santana JM, de Santana-Filho VJ, Quintans-

Junior LJ, de Lima Ferreira AP, Bonjardim LR. Radiographic mea-

surement of the cervical spine in patients with temporomandibular

dysfunction. Arch Oral Biol 2010;55:670-8.

17. HackneyJ, Bade D, Clawson A. Relationship between forward head

posture and diagnosed internal derangement of the temporoman-

dibular joint. J Orofac Pain 1993;7:386-90.

18. Visscher CM, De Boer W, Lobbezoo F, Habets LL, Naeije M. Is there

a relationship between head posture and craniomandibular pain?

J Oral Rehabil 2002;29:1030-6.

19. Andrade AV, Gomes PF, Teixeira-Salmela LF. Cervical spine align-ment and hyoid bone positioning with temporomandibular disor-

ders. J Oral Rehabil 2007;34:767-72.

20. Matheus RA, Ramos-Perez FM, Menezes AV, Ambrosano GM,

Haiter-Neto F, Boscolo FN, et al. The relationship between tempo-

romandibular dysfunction and head and cervical posture. J Appl

Oral Sci 2009;17:204-8.

21. Solow B, Tallgren A. Natural head position in standing subjects.

Acta Odontol Scand 1971;29:591-607.

22. Ahn SJ, Lee SP, Nahm DS. Relationship between temporomandib-

ular joint internal derangement and facial asymmetry in women.

Am J Orthod Dentofacial Orthop 2005;128:583-91.

23. Olivo SA, Bravo J, Magee DJ, Thie NM, Major PW, Flores-Mir C.

The association between head and cervical posture and temporo-

mandibular disorders: a systematic review. J Orofac Pain 2006;20:

9-23.

24. Lee SJ, An H, Ahn SJ, Kim YH, Pak S, Lee JW. Early stature predic-

tion method using stature growth parameters. Ann Hum Biol

2008;35:509-17.

25. Ahn SJ, Baek SH, Kim TW, Nahm DS. Discrimination of TMJ inter-

nal derangement by lateral cephalometric analysis. Am J Orthod

Dentofacial Orthop 2006;130:331-9.

26. Bryndahl F, Eriksson L, Legrell PE, Isberg A. Bilateral TMJ disk

displacement induces mandibular retrognathia. J Dent Res 2006;

85:1118-23.

27. Legrell PE, Isberg A. Mandibular height asymmetry following

experimentally induced temporomandibular joint disk displace-

ment in rabbits. Oral Surg Oral Med Oral Pathol Oral Radiol Endod

1998;86:280-5.

28. Isberg A, Hagglund M, Paesani D. The effect of age and gender onthe onset of symptomatic temporomandibular joint disk displace-

ment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85:

252-7.

29. Prof t WR, Fields HW, Sarver DM. Contemporary orthodontics. St

Louis: Elsevier/Mosby; 2013.

30. Yu YH, Kim YJ, Lee DY, Lim YK. The predictability of dentoskeletal

factors for soft-tissue chin strain during lip closure. Korean J

Orthod 2013;43:279-87.

31. Toureno L, Kook YA, Bayome M, Park JH. The effect of western

adaptation of Hispanic-Americans on their assessment of Korean

facial proles. Korean J Orthod 2014;44:28-35.

An et al 79

A i J l f O th d ti d D t f i l O th di J 2015 V l 147 I 1
http://refhub.elsevier.com/S0889-5406(14)00867-1/sref1http://refhub.elsevier.com/S0889-5406(14)00867-1/sref1http://refhub.elsevier.com/S0889-5406(14)00867-1/sref1http://refhub.elsevier.com/S0889-5406(14)00867-1/sref1http://refhub.elsevier.com/S0889-5406(14)00867-1/sref2http://refhub.elsevier.com/S0889-5406(14)00867-1/sref2http://refhub.elsevier.com/S0889-5406(14)00867-1/sref2http://refhub.elsevier.com/S0889-5406(14)00867-1/sref2http://refhub.elsevier.com/S0889-5406(14)00867-1/sref2http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref3http://refhub.elsevier.com/S0889-5406(14)00867-1/sref4http://refhub.elsevier.com/S0889-5406(14)00867-1/sref4http://refhub.elsevier.com/S0889-5406(14)00867-1/sref5http://refhub.elsevier.com/S0889-5406(14)00867-1/sref5http://refhub.elsevier.com/S0889-5406(14)00867-1/sref5http://refhub.elsevier.com/S0889-5406(14)00867-1/sref6http://refhub.elsevier.com/S0889-5406(14)00867-1/sref6http://refhub.elsevier.com/S0889-5406(14)00867-1/sref6http://refhub.elsevier.com/S0889-5406(14)00867-1/sref6http://refhub.elsevier.com/S0889-5406(14)00867-1/sref6http://refhub.elsevier.com/S0889-5406(14)00867-1/sref7http://refhub.elsevier.com/S0889-5406(14)00867-1/sref7http://refhub.elsevier.com/S0889-5406(14)00867-1/sref8http://refhub.elsevier.com/S0889-5406(14)00867-1/sref8http://refhub.elsevier.com/S0889-5406(14)00867-1/sref8http://refhub.elsevier.com/S0889-5406(14)00867-1/sref8http://refhub.elsevier.com/S0889-5406(14)00867-1/sref9http://refhub.elsevier.com/S0889-5406(14)00867-1/sref9http://refhub.elsevier.com/S0889-5406(14)00867-1/sref9http://refhub.elsevier.com/S0889-5406(14)00867-1/sref10http://refhub.elsevier.com/S0889-5406(14)00867-1/sref10http://refhub.elsevier.com/S0889-5406(14)00867-1/sref10http://refhub.elsevier.com/S0889-5406(14)00867-1/sref11http://refhub.elsevier.com/S0889-5406(14)00867-1/sref11http://refhub.elsevier.com/S0889-5406(14)00867-1/sref11http://refhub.elsevier.com/S0889-5406(14)00867-1/sref12http://refhub.elsevier.com/S0889-5406(14)00867-1/sref12http://refhub.elsevier.com/S0889-5406(14)00867-1/sref12http://refhub.elsevier.com/S0889-5406(14)00867-1/sref13http://refhub.elsevier.com/S0889-5406(14)00867-1/sref13http://refhub.elsevier.com/S0889-5406(14)00867-1/sref13http://refhub.elsevier.com/S0889-5406(14)00867-1/sref14http://refhub.elsevier.com/S0889-5406(14)00867-1/sref14http://refhub.elsevier.com/S0889-5406(14)00867-1/sref14http://refhub.elsevier.com/S0889-5406(14)00867-1/sref14http://refhub.elsevier.com/S0889-5406(14)00867-1/sref14http://refhub.elsevier.com/S0889-5406(14)00867-1/sref15http://refhub.elsevier.com/S0889-5406(14)00867-1/sref15http://refhub.elsevier.com/S0889-5406(14)00867-1/sref15http://refhub.elsevier.com/S0889-5406(14)00867-1/sref16http://refhub.elsevier.com/S0889-5406(14)00867-1/sref16http://refhub.elsevier.com/S0889-5406(14)00867-1/sref16http://refhub.elsevier.com/S0889-5406(14)00867-1/sref16http://refhub.elsevier.com/S0889-5406(14)00867-1/sref17http://refhub.elsevier.com/S0889-5406(14)00867-1/sref17http://refhub.elsevier.com/S0889-5406(14)00867-1/sref17http://refhub.elsevier.com/S0889-5406(14)00867-1/sref17http://refhub.elsevier.com/S0889-5406(14)00867-1/sref18http://refhub.elsevier.com/S0889-5406(14)00867-1/sref18http://refhub.elsevier.com/S0889-5406(14)00867-1/sref18http://refhub.elsevier.com/S0889-5406(14)00867-1/sref19http://refhub.elsevier.com/S0889-5406(14)00867-1/sref19http://refhub.elsevier.com/S0889-5406(14)00867-1/sref19http://refhub.elsevier.com/S0889-5406(14)00867-1/sref20http://refhub.elsevier.com/S0889-5406(14)00867-1/sref20http://refhub.elsevier.com/S0889-5406(14)00867-1/sref20http://refhub.elsevier.com/S0889-5406(14)00867-1/sref20http://refhub.elsevier.com/S0889-5406(14)00867-1/sref21http://refhub.elsevier.com/S0889-5406(14)00867-1/sref21http://refhub.elsevier.com/S0889-5406(14)00867-1/sref22http://refhub.elsevier.com/S0889-5406(14)00867-1/sref22http://refhub.elsevier.com/S0889-5406(14)00867-1/sref22http://refhub.elsevier.com/S0889-5406(14)00867-1/sref23http://refhub.elsevier.com/S0889-5406(14)00867-1/sref23http://refhub.elsevier.com/S0889-5406(14)00867-1/sref23http://refhub.elsevier.com/S0889-5406(14)00867-1/sref23http://refhub.elsevier.com/S0889-5406(14)00867-1/sref24http://refhub.elsevier.com/S0889-5406(14)00867-1/sref24http://refhub.elsevier.com/S0889-5406(14)00867-1/sref24http://refhub.elsevier.com/S0889-5406(14)00867-1/sref25http://refhub.elsevier.com/S0889-5406(14)00867-1/sref25http://refhub.elsevier.com/S0889-5406(14)00867-1/sref25http://refhub.elsevier.com/S0889-5406(14)00867-1/sref26http://refhub.elsevier.com/S0889-5406(14)00867-1/sref26http://refhub.elsevier.com/S0889-5406(14)00867-1/sref26http://refhub.elsevier.com/S0889-5406(14)00867-1/sref27http://refhub.elsevier.com/S0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