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doi: 10.2522/ptj.20100233

Originally published online June 9, 20112011; 91:1184-1197.PHYS THER.

W. Major, Norman M.R. Thie and David J. MageePaulBruno R. da Costa, Inae C. Gadotti, Sharon Warren,

Susan Armijo-Olivo, Rony Silvestre, Jorge Fuentes,Flexion Test: A Cross-Sectional StudyDisorders While Performing the CraniocervicalMuscles in Patients With TemporomandibularElectromyographic Activity of the Cervical Flexor

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Electromyographic Activity of theCervical Flexor Muscles in Patients

With Temporomandibular DisordersWhile Performing the CraniocervicalFlexion Test: A Cross-Sectional StudySusan Armijo-Olivo, Rony Silvestre, Jorge Fuentes, Bruno R. da Costa,Inae C. Gadotti, Sharon Warren, Paul W. Major, Norman M.R. Thie,David J. Magee

Background. Most patients with temporomandibular disorders (TMD) have beenshown to have cervical spine dysfunction. However, this cervical dysfunction has

been evaluated only qualitatively through a general clinical examination of thecervical spine.

Purpose. The purpose of this study was to determine whether patients with TMDhad increased activity of the superficial cervical muscles when performing thecraniocervical flexion test (CCFT) compared with a control group of individuals who

were healthy.

Design. A cross-sectional study was conducted.

Methods. One hundred fifty individuals participated in this study: 47 werehealthy, 54 had myogenous TMD, and 49 had mixed TMD. All participants performedthe CCFT. Data for electromyographic activity of the sternocleidomastoid (SCM) and

anterior scalene (AS) muscles were collected during the CCFT for all participants. A3-way mixed-design analysis of variance for repeated measures was used to evaluatethe differences in EMG activity for selected muscles while performing the CCFTunder 5 incremental levels. Effect size values were calculated to evaluate the clinicalrelevance of the results.

Results. Although there were no statistically significant differences in electromyo-graphic activity in the SCM or AS muscles during the CCFT in patients with mixed andmyogenous TMD compared with the control group, those with TMD tended to haveincreased activity of the superficial cervical muscles.

Limitations. The results obtained in this research are applicable for the group of

individuals who participated in this study under the protocols used. They couldpotentially be applied to people with TMD having characteristics similar to those ofthe participants of this study.

Conclusion. This information may give clinicians insight into the importance ofevaluation and possible treatment of the deep neck flexors in patients with TMD.However, future research should test the effectiveness of this type of programthrough a randomized controlled trial in people with TMD in order to determine thereal value of treating this type of impairment in this population.

S. Armijo-Olivo, BScPT, MSc, PhD,Department of Physical Therapy,Faculty of Rehabilitation Medicine,and Alberta Research Centre for

Health Evidence, Faculty of Medi-cine and Dentistry, University ofAlberta, Edmonton, Alberta, Can-ada. Mailing address: Departmentof Physical Therapy, RehabilitationResearch Centre, Faculty of Rehabil-itation Medicine, University ofAlberta, 350 Corbett Hall, Edmon-ton, Alberta, Canada T6G 2G4.Address all correspondence to DrArmijo-Olivo at: [email protected] [email protected].

R. Silvestre, BScPT, MSc, ResearchCenter of Human Movement,Mayor University, Santiago, Chile.

J. Fuentes, BSc, MScRS, Rehabilita-tion Research Centre, Faculty ofRehabilitation Medicine, Univer-sity of Alberta, and Department ofPhysical Therapy, Catholic Univer-sity of Maule, Talca, Chile.

B.R. da Costa, BScPT, MSc, Instituteof Social & Preventive Medicine,University of Bern, Bern, Switzerland.

I.C. Gadotti, BScPT, MScPT, PhD,Department of Physical Therapy,College of Nursing and Health Sci-ences, Florida International Uni-versity, Miami, Florida.

S. Warren, PhD, Faculty of Reha-bilitation Medicine, University ofAlberta.

Author information continues onnext page.

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1184 f Physical Therapy Volume 91 Number 8 August 2011

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Temporomandibular disorders(TMD) are the most prevalentcategory of nondental chronic

pain conditions in the orofacialregion. These disorders are charac-

terized by pain affecting the masti-catory muscles, the temporo-mandibular joint (TMJ), and relatedstructures.1 Temporomandibular dis-orders interfere with daily activitiesand can significantly affect quality oflife, diminishing patients capacityfor work and ability to interact withtheir social environment.2 It hasbeen calculated that approximately$2 billion has been spent in theUnited States due to TMD directcare.3 Patients with TMD have

shown high levels of unemploymentand decreased work effectiveness.4

In a large, population-based, cross-sectional study, it was shown thatTMD chronic pain had an individualimpact and burden similar to that ofback pain, severe headache, andchest and abdominal pain.5

In a recent study,6 women com-prised more than 70% of the patientshaving TMD, and the ratio between

women and men was 2.4:1 forarthralgia, 2.5:1 for osteoarthritis,3.4:1 for myofascial pain, and 5.1:1for TMJ disk displacement.6 The lit-erature supports the fact that

women are more sensitive to painconditions, reporting more severepain, more frequent pain, and painof longer duration than men.714 Inaddition, women are more promptin seeking help than men. Therefore,it seems that women more com-

monly have TMD and may seek carefor TMD pain more often than men.3

Temporomandibular disorders havecommonly been associated withsymptoms affecting the head andneck region, such as headache,cervical spine dysfunction,15,16 andaltered head and cervical pos-ture.1721 It has been reported thatpain in the cervical musculoskeletaltissues may be referred to cranial

structures, including the jaw mus-cles22,23; thus, a connection betweencervical muscle dysfunction and jawsymptoms could exist.2427Addition-ally, animal studies have revealed

considerable convergence of cranio-facial and cervical afferents in thetrigeminocervical nucleus and uppercervical nociceptive neurons.2831

All of this evidence has been the the-oretical foundation of pain localiza-tion and referral and of neuromuscu-lar adaptations in the cervical andorofacial regions.3234 However, todate, no research has demonstrated acause-and-effect relationship.

As stated above, TMD are catego-

rized as musculoskeletal disordersthat commonly involve the cervicalregion. Other musculoskeletal disor-ders associated with the cervicalregion, such as neck pain, cervico-genic headache, and whiplash-associated disorders, are character-ized by abnormal function of thecervical muscles.3537 However, it isunknown whether people with TMDhave these muscular alterations.Given the close connection between

the cervical spine and the orofacialregion, knowledge about impairmentsin the cervical spine in people withTMD could help clinicians focus theirefforts on properly evaluating andtreating these impairments.

Previous work has shown that grosschanges in strength (force-generatingcapacity) and endurance have beenobserved in cervical-related disor-ders. However, according to Jull et

al36

and Falla and Farina,38

finerchanges in cervical muscular activityof the cervical spine are present.Reduced activation of deep cervicalmuscles, augmented superficial activ-ity of the sternocleidomastoid (SCM)and anterior scalene (AS) muscles,changes in feedforward activation,reduced capacity to relax the cervi-cal muscles, and prolonged muscleactivity following voluntary contrac-tion could lead to a compromise in

P.W. Major, DDS, MSc, FRCD(c), School ofDentistry, University of Alberta.

N.M.R. Thie, BSc, MSc, DDS, TMD/OrofacialPain Graduate Program, School of Dentistry,University of Alberta.

D.J. Magee, PhD, Department of PhysicalTherapy, Faculty of Rehabilitation Medicine,University of Alberta.

[Armijo-Olivo S, Silvestre R, Fuentes J, et al.Electromyographic activity of the cervicalflexor muscles in patients with temporoman-dibular disorders while performing thecraniocervical flexion test: a cross-sectionalstudy. Phys Ther. 2011;91:11841197.]

2011 American Physical Therapy Association

Published Ahead of Print: June 9, 2011Accepted: April 8, 2011Submitted: July 14, 2010

Cervical Flexor Activity and Temporomandibular Disorders

August 2011 Volume 91 Number 8 Physical Therapy f 1185

http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/


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the control of the cervical spine andconsequently lead to pain and dys-function.36 Study of these muscularalterations has gained attention inthe last few years, as exercises

addressing these motor control alter-ations have had good results inpatients with cervical involve-ment.3941 Therefore, the assess-ment and treatment of muscularimpairments is considered a key ele-ment in the management of cervical-associated disorders. Because TMDhave been considered part of thecervical-associated disorders, it maybe plausible that similar featurescould be seen in this patient group.Knowledge about these features

would be useful for clinicians treat-ing patients with TMD. However,studies of muscular impairments inpatients with TMD are lacking.

Cervical dysfunction in patients withTMDs has been evaluated only qual-itatively through a general clinical

examination of the cervical spine.Most of the studies have looked atcervical spine signs and symptoms inpeople with TMD, but they have notinvestigated any motor alterations

in a quantitative way. For example,de Wijer and colleagues27,42

concluded that symptoms of thestomatognathic system overlap inpatients with TMD and cervicalspine disorders and that symptomsof the cervical spine overlap in thesame group of patients. Visscher etal25 found that patients with chronicTMD more often had cervical spinepain than those without this disor-der. Stiesch-Scholz et al43 found thatasymptomatic functional disorders

of the cervical spine occurred morefrequently in patients with internalderangement of the TMJ than in acontrol group. The presence of ten-der points in the cervical spine andshoulder girdle in patients with thesame diagnosis was more common,especially in upper segments of the

cervical spine, compared with a con-trol group of individuals who werehealthy. Furthermore, a recent sys-tematic review44 showed that exer-cises for the neck that also were used

to improve neck and head posturedecreased symptoms in patientswith TMD. However, the systematicreview found that details of the exer-cises and exercise programs (ie, typeof exercise, dosage, and frequency)

were lacking, as well as a clearunderlying mechanism of why theseexercises, directed toward to theneck, improved TMD symptoms.

Based on the above information, itwas evident that a more quantitative

evaluation of the motor activity ofthe cervical muscles through electro-myographic (EMG) assessment, look-ing at performance patterns ofthe cervical musculature activity inpatients with TMD, could assist inclarifying the role of the cervicalmuscles involvement in the symp-toms of these patients. Additionally,this evaluation could open an areaof study aimed at treating these alter-ations through improvement of

motor control of the cervical mus-cles in patients with TMD.

The main objective of this study wasto determine, through EMG evalua-tion, whether patients with myoge-nous TMD and mixed TMD hadaltered muscle activity (ie, higherEMG activity) of the superficial cer-

vical muscles (SCM and AS) whenperforming the CCFT compared

with a control group of individuals

who were healthy. The secondaryobjectives of this study were: (1) todetermine whether there was anassociation between the perfor-mance of the cervical flexor musclesduring the 5 stages of the CCFT andneck disability and jaw disability and(2) to determine whether there wasan association between level ofchronic disability in patients withTMD based on the Research Diagnos-tic Criteria for Temporomandibular

The Bottom Line

What do we already know about this topic?

Cervical spine dysfunction has been reported to be associated with tem-

poromandibular disorders (TMD). Temporomandibular disorders also are

commonly associated with other symptoms affecting the head and neck

region such as headache, ear-related symptoms, and altered head and

cervical posture. However, no study has investigated the presence of

cervical muscle impairments using electromyography.

What new information does this study offer?

The results of this study may give clinicians insight into the importance of

the evaluation and possible treatment of the deep neck flexors in patientswith TMD. However, randomized clinical trials are necessary to determine

the effectiveness of an exercise program targeting the deep neck flexors

in these patients.

If youre a patient, what might these findings meanfor you?

If you have a TMD, these findings may help your physical therapist

evaluate your condition. This evaluation would include an examination of

the cervical musculature as well as the TMD.





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Disorders45 (RDC/TMD) (ChronicPain Grade Disability Questionnairefor TMD), pain intensity, duration ofcomplaint, and performance of thecervical flexor muscles during the 5

stages of the CCFT.

MethodDesign

A cross-sectional study wasconducted.

ParticipantsA convenience sample of patientswho attended the TMD/OrofacialPain Clinic at the School of Dentistry,Faculty of Medicine and Dentistry,University of Alberta, and students

and staff at the University of Albertawho were healthy was recruited forthis study. The sample size for thisstudy was calculated based on arepeated-measures analysis of vari-ance (ANOVA) following the guide-lines established by Stevens (with.05, 0.20, power80%, andeffect size0.57).46 A minimum of 40participants per group was needed.

The inclusion and exclusion criteria

for the individuals who were healthyand the patients with TMD havebeen described elsewhere.47,48 Inbrief, people who were healthy wereincluded if they were womenbetween the ages of 18 and 50

years16 and they did not have a his-tory of musculoskeletal pain, TMDsymptoms, neurological disease, sys-temic disease, or mental illness thatcould interfere with the outcomes.Patients with TMD were included if

they were women between 18 and50 years of age, had pain in the mas-ticatory muscles or TMJ of at least 3months duration, and had a moder-ate or severe baseline pain score(30 mm) on a 100-mm visual ana-log scale (VAS).49 Patients were clas-sified as having myogenous TMDbased on the classification Ia and Ibof Dworkin and LeResche.45 In addi-tion, they had to have pain uponpalpation in at least 3 of the 12 mus-

cular points proposed by Fricton andSchiffman.5052 Patients were diag-nosed as having mixed TMD if theycomplained of muscular symptomsin addition to TMJ symptoms suchas painful clicking, crepitation, orpain in the TMJ at rest or duringfunction53 and during a compressiontest.54

A total 168 individuals were assessedfor inclusion in this study. A total of18 individuals were excluded. Themain reasons for exclusion were: nottotally healthy (n9), older than 50

years of age (n2), having a neuro-logical disease (n1), having cancer(n1), and having a pain score lowerthan 30 mm on the VAS (n5). Onehundred fifty participants provideddata for this study: 47 were healthy,

54 had myogenous TMD, and 49 hadmixed TMD.

The general demographics for eachgroup and the clinical characteristicsof the participants are displayed inTable 1. There were no significantdifferences in age and height in thesample (P.05). However, weight

was significantly different betweenparticipants with mixed TMD andthose with myogenous TMD (meandifference8.0 kg, 95% confidenceinterval [CI]1.9 to 14.2; P.006)and between participants withmixed TMD and those who werehealthy (mean difference7.8 kg,95% CI1.4 to 14.2; P.01).

Participants with mixed TMD weresimilar to those with myogenous

Table 1.Descriptive Statistics of Height, Weight, and Age and Clinical Characteristics ofParticipants by Groupa

Variable Group X SD

Height (cm) Myogenous TMD (n54) 165.1 5.1

Healthy (n47) 165.0 6.8

Mixed TMD (n49) 166.3 5.9

Weight (kg) Myogenous TMD 64.1b 9.9

Healthy 64.3b 12.7

Mixed TMD 72.1c 15.9

Age (y) Myogenous TMD 31.4 9.0

Healthy 28.3 7.5

Mixed TMD 31.3 8.3

Duration of complaint (y) Myogenous TMD 6.5c 6.4

Healthy 0.0 0.0

Mixed TMD 8.3c 6.4

Pain intensity (0100 mm) Myogenous TMD 45.3c 17.3

Healthy 0.0 0.0

Mixed TMD 49.0c 16.1

Neck Disability Index

(050 points)

Myogenous TMD 10.5c 5.5

Healthy 1.6 1.6

Mixed TMD 12.6c 6.8

Jaw Function Scale

(1050 points)

Myogenous TMD 18.6b,c 6.6

Healthy 10.1 0.4

Mixed TMD 22.7c 7.1

a TMDtemporomandibular disorders.b Significantly different compared with participants with mixed TMD at .05.c Significantly different compared with participants who were healthy at .05.





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TMD in most of the general charac-teristics such as duration of com-plaint and pain intensity (P.05).Both groups had a moderate inten-sity of pain in the jaw and a long

history of pain. Both groups also hada mild level of disability in the neckand a moderate level of disability inthe jaw (Tab. 1). The Limitations ofDaily Functions in TMD Question-naire/Jaw Function Scale (JFS) dis-ability score was significantly higherfor participants with mixed TMDcompared with those with myoge-nous TMD (mean difference4.1points, 95% CI1.4 to 6.9; P.001).

The prevalence of neck pain in the

sample of participants with TMD washigh. Approximately 88% (87.5%) ofthe participants with myogenousTMD and 87.8% of those with mixedTMD had self-reported neck pain.

Clinical ExaminationThe participants underwent a clini-cal examination by a physical thera-pist with experience in musculo-skeletal rehabilitation to determineeligibility for this study and to deter-

mine their diagnosis. The clinicalexamination followed the guidelinesof the RDC/TMD.45 All participantsread an informational letter andsigned an informed consent state-ment in accordance with the Univer-sity of Albertas policies on researchusing human subjects.

ProcedureDemographic data were collectedon all participants who satisfied the

inclusion criteria. In addition, allincluded participants were askedto report specific characteristicsregarding their jaw problem (eg,onset, duration of symptoms, treat-ments received) and their intensityof pain in the jaw (VAS score)49,5558

and to complete the Neck DisabilityIndex (NDI),59,60 the JFS,61 and aquestionnaire for history of jaw painused by the RDC/TMD.45 In addition,participants were asked to complete

the Chronic Pain Grade DisabilityQuestionnaire for TMD used by theRDC/TMD to evaluate the level ofchronic disability due to TMDs.45

The reliability and validity of these

tools have been reported else-where.45,59 61 After the participantswere evaluated clinically and hadcompleted the questionnaires, theyperformed the CCFT. This testing

was performed in one session.

Electromyographic Evaluation ofthe Cervical Flexor MusclesElectrode placement. Surface elec-trodes were located on the sternalhead of the SCM muscle and on the

AS muscle as described in the proto-

col used by Falla and colleagues.62,63

A reference electrode was placed onthe wrist.

Normalization procedure for EMGdata. For normalization purposes,EMG data were collected for 5 sec-onds during a maximal voluntarycontraction (MVC). The EMG activityof the SCM and AS muscles wasrecorded during this maximal con-traction and saved in the computer.

This procedure was repeated a sec-ond time. Submaximal contractionsobtained during the CCFT were nor-malized using these 2 MVC values.Submaximal contractions wereexpressed as a percentage of the3-second root mean square (RMS)

value obtained during the MVC. Theaverage between the normalized con-tractions using the 2 MVC measure-ments was used for statistical analysis.

EMG data processing. Data onEMG activity of the SCM and ASmuscles were obtained using theBagnoli-8 EMG system* in a bipolarconfiguration with DE-2.1 elec-trodes.* This system is designed tomake the acquisition of EMG signalseasy and reliable (common-moderejection ratio92 dB, system

noise1.2 V [RMS]). The EMGactivity was recorded (analog rawsignal) with a data acquisition pro-gram, written in Labview 7.1,whichcollected data at 1,024 Hz using a

PCMCIA card

filtered between 20and 450/Hz 10% and amplifiedusing a gain of 1,000 according tothe established standards for EMGacquisition and reporting.64,65 Toobtain a measure of EMG amplitude,maximum root mean square (RMS)

was calculated for 4 seconds duringthe 10-second submaximal contrac-tions for each muscle while per-forming the CCFT using IGORPro5.1 and was expressed a per-centage of the 3-second EMG activity

obtained during the MVC normaliza-tion procedure.

Instrumentation for Registeringthe Pressure Exerted WhilePerforming the CCFT

An air-filled pressure sensor (pres-sure biofeedback unit) was placedin the suboccipital region of eachpatients neck and inflated to a pres-sure of 20 mm Hg. The cuff wasconnected to a pressure transducer

(miniature pressure cell) designedto register increases in pressure withthe movement of nodding action forthe CCFT. Electrical signals from thepressure transducer were amplifiedto a visual feedback device and pro-

jected onto a computer screen sothat the participants were able to seethe targeted pressure level. Graphs

with the performance of each partic-ipant during the CCFT were storedusing Igor Pro5.1. These data wereanalyzed offline by a blinded assessor.

Craniocervical Flexion Test:Description and ProceduresBefore testing began, participants

were asked to perform a warm-up,which consisted of 2 movements ofthe neck and head in all directions

* Delsys Inc, PO Box 15734, Boston, MA02215.

National Instruments Corporation, 11500 NMopac Expwy, Austin, TX 78759-3504.WaveMetrics Inc, PO Box 2088, LakeOswego, OR 97035.





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(flexion [forward neck movement],extension, side flexion [lateral move-ment of the neck], and rotation). Theparticipants were placed in a relaxedsupine position with the knees

flexed and the head and neck main-tained in a mid-position (ie, neutralposition, no flexion or extension)following a protocol established pre-

viously.66 The head and chin wereparallel to the plinth (Fig. 1).

The CCFT is a low-load test that isthe most common method used toevaluate the performance of thedeep cervical muscles (ie, longuscolli and rectus capitis). The CCFTconsists of a craniocervical flexion

(nodding) movement, which com-bines the action of flexion at thecraniocervical junction, performedby the longus capitis muscles, along

with the flattening of the cervicallordosis, an action of the longus collimuscles. Electromyographic activityof the superficial cervical flexor mus-cles such as the SCM and AS may beregistered during the CCFT. ElevatedEMG activity may be a compensationfor reduced or impaired activity of

the deep cervical flexor muscles inindividuals with cervical-associatedpain compared with those who arehealthy.67

The CCFT required each participantto perform the craniocervical flexionmovement in 5 progressive stages ofincreasing pressure (22, 24, 26, 28,and 30 mm Hg) with the aid of a

visual feedback device. Participantswere instructed to perform this gen-

tle nodding movement (craniocervi-cal flexion) and at practiced progres-sive targeted pressure levels. Theorder of the targeted pressure level

was randomized by an independentassessor. Participants had to main-tain a steady pressure at each tar-geted level for a duration of 10 sec-onds (Fig. 1). They repeated eachtargeted level 2 times, with a restperiod of 1 minute between repeti-tions to avoid the effects of fatigue.68

Data Analysis

The normalized data of the EMGactivity of all muscles were analyzeddescriptively (ie, mean, standarddeviation). Variables were tested fornormality, homogeneity of variance,and linearity. All EMG variables werereasonably normally distributed. His-tograms and box plots show thatmost of the variables were slightlyskewed to the right. However,

ANOVA analysis is robust to thesemild deviations from normality and

can provide accurate estimates ofthe analyzed variables.69

A 3-way mixed-design ANOVA forrepeated measures (3 independent

variables: muscles [SCM and AS], test[5 levels], and groups [myogenousTMD, mixed TMD, and control]) wasused to evaluate the differences inEMG activity for selected muscles(dependent variable) while perform-ing the CCFT at 5 levels of pressure.

Pair-wise comparisons using the

Bonferroni procedure were adminis-tered to evaluate the differencesbetween variables and groups (ie,control and TMD groups) in all ofthe different conditions (objective1). The Spearman rho test was usedto evaluate the relationship amongNDI, JFS, and clinical variables withEMG variables (correlational matrix)(objectives 2 and 3). The correlation

was considered important when thecorrelation coefficient value was

higher than .70. The reference val-ues to make this decision were basedon values reported by Munro.70

To clearly show the impact of theresults for clinical practice, clinicalrelevance of the results was assessedusing a distribution-based method.71

The effect size (Cohen d) valueswere calculated to determine clinicalrelevance of the differences in theEMG measurements across different

Figure 1.Craniocervical flexion test.





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levels of pressure and groups.72

Effect sizes of 0.4 or higher wereconsidered clinically relevant.73 Asubgroup analysis also was con-ducted to determine differencesbetween participants with pureTMD (ie, without neck pain) and

those who were healthy.

The level of significance was set at.05. The SPSS version 17 andSTATA version 10 statistical pro-grams were used to perform the sta-tistical analysis. The analysis was per-formed blinded to group condition.

ResultsEMG Activity of the CervicalFlexors Muscles WhilePerforming the CCFTLarge variability of the normalizedEMG activity across conditions andgroups was observed (Fig. 2). Using

a 3-way mixed-design ANOVA forrepeated measures, we foundthat the main effects of muscles(F18.5, P.0001) and pressure lev-els (F27.3, P.0001) were statisti-cally significant. This finding meansthat there was a statistically signifi-cant difference in EMG activityamong muscles and among pressurelevels. The interaction between mus-cles and pressure also was statisti-cally significant (F2.9, P.001).

However, there was no significantdifference in EMG activity of the ana-lyzed muscles among groups (ie,mixed TMD, myogenous TMD, andcontrol) across conditions (F2.6,P.07). Weight was not significantlyassociated with EMG activity (P.49),

so it was not included in the model.

Subgroup Analysis: EMG Activityin Patients With Pure TMD(Without Neck Pain) ComparedWith Participants Who WereHealthy

When analyzing a subgroup of par-ticipants with TMD but withoutneck pain (n13) compared withthe control group (n47), statisti-cally significant differences in EMG

SPSS Inc, 233 S Wacker Dr, Chicago, IL60606. StataCorp LP, 4905 Lakeway Dr, College Sta-tion, TX 77845.

Mixed TMDHealthyMyogenous TMD

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AvSCMR_26mm

Hg

Figure 2.Normalized electromyographic (EMG) activity of sternocleidomastoid (SCM) and anterior scalene (AS) muscles in participants withmyogenous temporomandibular disorders (TMD), those with mixed TMD, and those who were healthy while performing thecraniocervical flexion test. Error bars95% confidence interval. %MVCpercentage of maximum voluntary contraction,

AvSCMR_22mmHgaverage right SCM muscle EMG activity at 22 mm Hg, AvSCML_22mmHgaverage left SCM muscle EMGactivity at 22 mm Hg, AvASR_22mmHGaverage right AS muscle EMG activity at 22 mm Hg, AvASL_22mmHgaverage left

AS muscle EMG activity at 22 mm Hg, AvSCMR_24mmHgaverage right SCM muscle EMG activity at 24 mm Hg,AvSCML_24mmHgaverage left SCM muscle EMG activity at 24 mm Hg, AvASR_24mmHgaverage right AS muscle EMG activityat 24 mm Hg, AvASL_24mmHgaverage left AS muscle EMG activity at 24 mm Hg, AvSCMR_26mmHgaverage right SCM muscleEMG activity at 26 mm Hg, AvSCML_26mmHgaverage left SCM muscle EMG activity at 26 mm Hg, AvASR_26mmHgaverageright AS muscle EMG activity at 26 mm Hg, AvASL_26mmHgaverage left AS muscle EMG activity at 26 mm Hg,

AvSCMR_28mmHgaverage right SCM muscle EMG activity at 28 mm Hg, AvSCML_28mmHgaverage left SCM muscle EMGactivity at 28 mm Hg, AvASR_28mmHgaverage right AS muscle EMG activity at 28 mm Hg, AvASL_28mmHgaverage left AS

muscle EMG activity at 28 mm Hg, AvSCMR_30mmHgaverage right SCM muscle EMG activity at 30 mm Hg,AvSCML_30mmHgaverage left SCM muscle EMG activity at 30 mm Hg, AvASR_30mmHgaverage right AS muscle EMG activityat 30 mm Hg, AvASL_30mmHgaverage left AS muscle EMG activity at 30 mm Hg.





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activity were found between groups(F4.831, P.01). Post hoc analysisusing a Bonferroni test indicatedthere were many statistically signifi-

cant differences between groups inthe analyzed muscles and conditions(Tab. 2).

Association Between EMGVariables and Clinical VariablesWhile Performing the CCFT

Very weak (although statistically sig-

nificant) correlations were found,mainly between the EMG activity ofthe SCM muscles during the 5 stages

of the CCFT and clinical variablessuch as pain intensity, duration ofcomplaint, neck disability, jaw dis-ability, and level of chronic disability

of TMD based on the RDC/TMD(Chronic Pain Grade Disability Ques-tionnaire for TMDs) (Tab. 3).

Table 3.Correlations Between Electromyographic Activity and Neck Disability (as Measured by Neck Disability Index), Chronic Pain GradeClassification, Jaw Disability (as Measured by Jaw Function Scale), Pain Intensity, and Duration of Complainta

Electromyographic

Activity

Neck

Disability

Chronic Pain

Grade Classification

Jaw

Disability

Pain

Intensity

Duration of

Complaint (y)

Average SCM at 22 mm Hg .23b .26b .26b .32b .15

Average AS at 22 mm Hg .13 .15 .15 .21b .05

Average SCM at 24 mm Hg .23b

.26b

.30b

.32b

.19c

Average AS at 24 mm Hg .14 .16 .17c .21c .08

Average SCM at 26 mm Hg .18c .19c .24b .29b .09

Average AS at 26 mm Hg .13 .12 .15 .21b .04

Average SCM at 28 mm Hg .18c .17 .23b .27b .13

Average AS at 28 mm Hg .13 .10 .17c .22b .03

Average SCM at 30 mm Hg .24b .21c .28b .33b .16c

Average AS at 30 mm Hg .20c .18c .22b .28b .11

a SCMsternocleidomastoid muscle, ASanterior scalene muscle.b Correlation is significant at the .05 level.c Correlation is significant at the .01 level.

Table 2.Subgroup Analysis Between Participants With Pure Temporomandibular Disorders and Participants Who Were Healthy:Electromyographic Activity of the Analyzed Muscles While Performing the Craniocervical Flexion Test a

Muscle

Pressure

(mm Hg) Group Group

Mean

DifferenceBetween Groups

(%MVC)

Standard

Error Pb

95% Confidence

Interval for

Difference

Lower

Bound

Upper

Bound

SCMR 22 Myogenous TMD Healthy 9.51c 3.315 .017 1.35 17.68

24 Myogenous TMD Healthy 11.06c 3.719 .013 1.90 20.22



SCML 22 Healthy Myogenous TMD 6.80c 2.715 .045 13.48 0.11

Mixed TMD 9.54c 3.380 .019 17.87 1.22

24 Healthy Myogenous TMD 7.32c 2.922 .045 14.52 0.124

Mixed TMD 12.64c 3.637 .003 21.59 3.68

26 Healthy Mixed TMD 10.68 4.393 .050 21.50 0.014

ASR 22 Myogenous TMD Healthy 9.74 3.981 .050 0.062 19.55

ASL 24 Healthy Mixed TMD 17.43c 6.631 .033 33.759 1.093

aValues based on estimated marginal means. TMDtemporomandibular disorders, SCMRright sternocleidomastoid, SCMLleft sternocleidomastoid,ASRright anterior scalene, and ASLleft anterior scalene.b Bonferroni adjustment for multiple comparisons.c The mean difference is significant at the .05 level.





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Clinical RelevanceEffect sizes of comparisons betweenmixed TMD and myogenous TMDgroups compared with the controlgroup while performing the CCFT

are displayed in Table 4 and Figures3 and 4.

DiscussionThe main finding of this study wasthat, although statistically significantdifferences in EMG activity of theSCM and AS muscles in patients withTMD compared with participants

who were healthy while performingthe CCFT were not attained (P.07),there was a trend for patients with

TMD to have consistently higherEMG activity in all of the analyzedmuscles. This increased activity ofthe superficial muscles of the cervi-cal spine might be associated with

the neck disturbances seen inpatients with TMD. This informationmay give clinicians insight into theimportance of evaluation and possi-ble treatment of the deep neck flex-ors in patients with TMD. However,at this point, more research on theseissues is necessary to provide defi-nite conclusions.

The results of this study cannot bedirectly compared with those of

other studies of cervical flexor mus-cle performance in patients withTMD because no studies investigat-ing this issue in this population werefound. However, the CCFT has

widely been used by physical thera-pists to determine alterations in themotor control of the craniocervicalflexor muscles in people with cervi-cal disorders such as neck pain,

whiplash-associated disorders, andcervicogenic headache becauseimpairment of the deep flexor mus-cles appears to be generic to neckdisorders.37 All of the studies analyz-ing craniocervical performance usingthe CCFT36,63,74,75 converge in that

Table 4.Moderate Effect Sizes for Comparisons Among Groups at Different Levels of Pressure While Performing the Craniocervical FlexionTesta

Outcome Measure:

Electromyographic Activity

Raw Differences Standardized Effect Size

Mean

Difference

(%MVC)

Confidence Interval

for Difference

Effect

Size

Confidence Interval

for Effect Size

Effect Size

Based onHealthy Group

Standard

Deviation

Lower

Bound

Upper

Bound

Lower

Bound

Upper

Bound

Average SCMR at 22 mm Hg,

mixed TMD vs healthy

5.36 1.65 9.07 0.59 0.17 0.99 0.73



5.88 1.83 9.93 0.59 0.18 0.99 0.72



5.94 0.77 11.11 0.47 0.06 0.87 0.54



6.31 0.67 11.95 0.45 0.04 0.85 0.48

Average SCML at 22 mm Hg,

myogenous TMD vs healthy

5.10 0.66 9.54 0.45 0.06 0.85 0.72



5.79 2.06 9.52 0.63 0.21 1.03 0.82



4.87 0.79 8.95 0.47 0.07 0.87 0.66



6.53 2.49 10.57 0.66 0.24 1.06 0.89



4.63 0.25 9.01 0.43 0.02 0.83 0.50



5.19 0.06 10.32 0.41 0.00 0.81 0.42

Average ASR at 22 mm Hg,


6.39 0.49 12.29 0.43 0.03 0.82 0.60



12.07 1.02 23.12 0.43 0.03 0.82 0.72



8.24 0.17 16.31 0.41 0.01 0.81 0.49

a TMDtemporomandibular disorders, SCMRright sternocleidomastoid muscle, SCMLleft sternocleidomastoid muscle, ASRright anterior scalene muscle,%MVCpercentage of maximum voluntary contraction.





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patients with cervical involvementhave an impaired performance of thedeep and superficial flexor cervicalmuscles. The increased activity inthe superficial muscles could be seenas a strategy to compensate for thedysfunction of the deep flexor mus-cles. Sterling et al76 suggested thatthe presence of pain could lead toinhibition or delayed activation of

specific muscles or group of musclesin the spine. This inhibition gener-ally occurs in deep muscles such asthe longus colli and longus capitis,

which control joint stability.76

The results of this study are not intotal agreement with those ofthe majority of the above-mentionedstudies. In our study, we found no

statistically significant differences insuperficial cervical flexor muscularactivity among groups while per-forming the CCFT, as evaluatedthough EMG analysis. One possibleexplanation for these results couldbe the level of dysfunction presentedby the participants with TMD. Wefound that the level of dysfunction,not only at the level of the neck but

Study or

Subgroup

Mixed TMD Healthy

Weight

Mean Difference Mean Difference

X SD Total X SD Total IV, Fixed, 95% CI IV, Fixed, 95% CI

ASR at 30 mm Hg 38.09 22.55 49 29.85 16.7 47 3.2% 8.24 (0.32, 16.16)

SCML at 22 mm Hg 22.83 10.83 49 17.04 7.09 47 14.8% 5.79 (2.14, 9.44)

SCML at 24 mm Hg 24.85 11.93 49 18.32 7.36 47 12.7% 6.53 (2.58, 10.48)SCML at 26 mm Hg 26.61 12.07 49 21.98 9.29 47 10.7% 4.63 (0.33, 8.93)

SCML at 28 mm Hg 28.82 12.5 49 24.2 10.4 47 9.4% 4.62 (0.03, 9.21)

SCML at 30 mm Hg 30.49 12.93 49 25.3 12.35 47 7.7% 5.19 (0.13, 10.25)

SCMR at 22 mm Hg 21.01 10.59 49 15.65 7.34 47 15.0% 5.36 (1.73, 8.99)

SCMR at 24 mm Hg 23.19 11.48 49 17.31 8.15 47 12.5% 5.88 (1.91, 9.85)

SCMR at 28 mm Hg 28.57 14.25 49 22.63 10.98 47 7.7% 5.94 (0.86, 11.02)

SCMR at 30 mm Hg 30.58 14.5 49 24.2 13.27 47 6.4% 6.38 (0.82, 11.94)

Total (95% CI) 490 470 100.0% 5.68 (4.27, 7.08)

Heterogeneity: 21.16, df9 (P1.00), I20%

Test for overall effect: Z7.92 (P.00001)

Figure 3.Moderate effect sizes found for comparisons between participants with mixed temporomandibular disorders (TMD) and those whowere healthy at different levels of pressure while performing the craniocervical flexion test. IVinverse variance, 95% CI95%confidence interval, ASRright anterior scalene muscle, SCMLleft sternocleidomastoid muscle, SCMRright sternocleidomastoidmuscle.

Study or

Subgroup

Myogenous TMD Healthy

Weight

Mean Difference Mean Differen ce

X SD Total X SD Total IV, Fixed, 95% CI IV, Fixed, 95% CI

ASR at 22 mm Hg 26.05 17.83 54 19.66 10.59 47 19.3% 6.39 (0.75, 12.03)

ASR at 30 mm Hg 41.92 34.82 54 29.85 16.73 47 5.6% 12.07 (1.62, 22.52)

SCML at 22 mm Hg 22.14 13.83 54 17.04 7.09 47 34.7% 5.10 (0.89, 9.31)

SCML at 24 mm Hg 23.19 12.3 54 18.32 7.36 47 40.4% 4.87 (0.97, 8.77)

Total (95% CI) 216 188 100.0% 5.65 (3.17, 8.13)

Heterogeneity: 21.74, df3 (P.63), I20%

Test for overall effect: Z4.47 (P.00001)

Figure 4.Moderate effect sizes found for comparisons between participants with myogenous temporomandibular disorders (TMD) and thosewho were healthy at different levels of pressure while performing the craniocervical flexion test. IVinverse variance, 95% CI95%confidence interval, ASRright anterior scalene muscle, SCMLleft sternocleidomastoid muscle.





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also at the level of the jaw, wasconsidered mild for our participants

with TMD. We might speculate thatbecause the disability was mild, it didnot have an impact on function or

physical impairment, which gener-ally is found in people with moredisabling pain. Our results are inagreement with the results obtainedby Falla et al63 in individuals with alevel of disability similar to that ofthe participants in this present study(mean NDI score12.4 points,SD9.563). Falla et al63 found thateven though the normalized EMGamplitude of the deep cervical flexormuscles was significantly lower inpatients with neck pain compared

with individuals who were healthy(P.05), the increase in EMG activityof the superficial muscles did notreach statistical significance,although there was a trend ofincreased EMG activity for the super-ficial muscles in patients with neckpain. The main explanation of thisfinding was the large variability inthe EMG activity found acrossgroups and conditions. These resultsagree with our findings, which also

showed a large amount of variabilityin EMG activity among muscles andconditions (as evidenced by the

wide CIs). When interpreting CIs,lower and upper boundaries need tobe taken into account to make con-clusions.77 Based on this interpreta-tion, we can say that 95% of the timethe estimated difference betweengroups could fall between theselower and upper boundaries. If welook at the upper boundaries of the

CIs for the raw mean differences(Tab. 4), we can see that the differ-ence between groups can be as highas 8.95% to 23.12% of MVC. How-ever, if we look at the lower bound-aries, the difference between groupscan be as low as 0.06% to 2.49% ofMVC. Therefore, based on this large

variability, we could have a situationwhere a clinically significant differ-ence between groups as well as a

nonclinically significant differencebetween groups could occur.

Although there was great variabilityin EMG activity, the mean EMG activ-

ity of the superficial muscles wasalways higher for participants withTMD pain compared with the con-trol group across all conditions andmuscles (Fig. 2). However, the large

variability of the normalized EMGactivity across participants andgroups did not lead to a finding ofstatistical significance.

The large variability seen in theEMG activity of the cervical flexormuscles also has been observed in

other regions such as the low back.78

Hodges et al78 found that peopleresponded differently to experimen-tal pain in the low back muscles.They reported that no 2 individualsshowed identical patterns ofincreased activity of the low backmuscles when they underwentexperimental pain. If this phenome-non were extrapolated to the cervi-cal spine, it could be speculated thateach individual has a different mus-

cle activation strategy to adapt topain. The motor response in the cer-

vical spine, especially in people withpain, would be an increase of theactivity of the SCM and AS muscles;however other strategies, using dif-ferent muscles not investigated inthis research, also could be present.Further research investigating possi-ble cervical motor strategies in peo-ple with TMD under different condi-tions would help further clarify the

role of the cervical muscles in TMD.

Our study did not measure directlythe activity of the deep cervicalflexor muscles because the tech-nique for measuring the activity ofthe deep cervical muscles is invasiveand adherence to the testing proto-col would have been impaired. Wemeasured the superficial cervicalmuscles such as the SCM and AS onlyas an indirect measure of impairment

of the activity of the deep cervicalflexor muscles. Thus, it is still uncer-tain whether deep cervical muscleactivity was impaired in thesepatients. In addition, because the

cervical spine is a very complex sys-tem characterized by a high degreeof redundancy in the muscular sys-tem,36,79 it is not surprising thatother motor strategies and musclesnot analyzed in this study (other thanSCM and AS muscles) could be usedby people with pain to stabilize thecervical spine.

The CCFT has become a gold stan-dard for isolating the activation ofthe deep flexor muscles and identi-

fying possible co-contraction pat-terns of superficial muscles in thecervical spine.63,75,80 Its construct

validity66,81 as well as its reliability67

have been established; however,other psychometric properties suchas concurrent validity with clinical

variables such as neck disability andpain intensity of this test need to beascertained. Thus, this study investi-gated the associations between themuscular activity of the analyzed

muscles through the 5 stages of theCCFT and clinical variables such asthe level of chronic pain grade clas-sification of TMD based on theRDC/TMD, pain intensity, time ofcomplaint, jaw disability, and neckdisability. Most of the associations

were positive but weak, indicatingthat the performance of the CCFT isnot strongly related to other clinical

variables such as pain intensity, neckdisability, or jaw disability. These

results are in agreement with thoseof Falla et al,82 who reported thatreduction in pain in patients withneck pain after a training program

was not accompanied by animprovement in performance of thecervical flexor muscles. It appearsthat pain and physical performanceof the craniocervical muscles repre-sent different aspects of disability inpeople with cervical involvement.83

Thus, a more focused evaluation





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regarding disability and its relatedfactors in future research is neededto understand the intricacies amongphysical impairments, pain, anddisability.

Because of the variability of EMGactivity among groups and condi-tions found in this study, an analysisof the clinical relevance of theresults through the calculation ofeffect sizes was conducted to evalu-ate the relevance of these findings.To our knowledge, this is the firsttime that a study has evaluated theclinical relevance of EMG activity.

According to Musselman,71 effectsize calculation is one of the most

common ways to evaluate clinicalrelevance after the fact.71,84 Thelarger this effect size index, thelarger the difference betweengroups and the larger the clinical rel-evance of the results.71 It is recog-nized that effect sizes of 0.2, 0.5, and0.8 correspond to small, moderate,and large effects.73 Although there isno known research that establishes acutoff of EMG activity (percentage ofMVC) to be considered clinically rel-

evant when comparing the EMGactivity of different groups, it hasbeen shown that EMG activity as lowas 2% to 5% of MVC can be related topain in neck-shoulder areas.8587 Inaddition, a minimally important dif-ference for EMG activity has beenfound to be 2.9% of MVC.88

Although a large variability in theestimates of effect sizes was presentin this data set (which had wide CIs),

based on the calculated mean effectsizes (ie, standardized mean differ-ences ranging between 0.41 and0.66) and the raw mean differencesobtained from the comparisons(ranging from 4.63% to 12.07% ofMVC), differences in EMG activity

were found in some of the compari-sons between patients with TMDand the control group (Tab. 3). Thus,standardized effect sizes and mini-mally important difference could

serve as an index to guide cliniciansin the relevance of the findings. Itcould be said that in the absence ofknowledge and guidelines to deter-mine the clinical relevance of certain

outcomes, calculation of the clinicalrelevance, based on the distributionmethods, could be an option. Theseresults could be of importance forclinicians who work in this fieldbecause this analysis might indicatethat patients with TMD tended tohave increased activity of the super-ficial cervical muscles compared

with the control group. In addition,the results of the subgroup analysisconsidering only patients with pureTMD provide more support for these

findings. Furthermore, preliminaryevidence has shown that exercisesaddressing these types of impair-ments (ie, training of neck flexormuscles) as part of cervical spinetreatment in people with TMDreduced pain and improved function(ie, increased pain-free mouth open-ing) in patients with TMD, whichpotentially supports the fact thatpatients with TMD could benefitfrom treatment of impaired cervical

flexor muscles.89 Therefore, theseresults might be considered whenevaluating and treating patients withTMD.

Nevertheless, it is necessary toimplement a randomized controlledtrial that addresses these cervicalimpairments through cervical flexorexercises in patients with TMDand test whether these exercisesdecrease pain and improve function

and quality of life in patients withTMD. In this way, research couldadvance clinical practice in this area.

LimitationsThe results obtained in this researchare applicable for the group of indi-

viduals who participated in thisstudy under the protocols used.They potentially could be applied topeople with TMD having character-istics similar to those of the partici-

pants in this study. This limitationshould be taking into consideration

when attempting to extrapolatethese results. In addition, it must beacknowledged that because this

project was cross-sectional, a cause-and-effect relationship between cervi-cal muscular impairment and TMDcannot be established.

ConclusionsThere were no statistically signifi-cant differences (P.07) in EMGactivity in the SCM or the AS musclesin patients with mixed and myoge-nous TMD compared with individu-als who were healthy when perform-ing the CCFT. However, the patients

with TMD tended to have increasedactivity of the superficial cervicalmuscles compared with the controlgroup. This increased activity of thesuperficial muscles of the cervicalspine might be associated with theneck disturbances seen in patients

with TMD. This information maygive clinicians insight into the impor-tance of evaluation and possibletreatment of the deep neck flexorsin patients with TMD. However,

future research should test the effec-tiveness of this type of programthrough a randomized controlledtrial in individuals with TMD todetermine the real value of treatingthis type of impairment in thispopulation.

Dr Armijo-Olivo, Dr Warren, Dr Major, andDr Magee provided concept/idea/researchdesign. Dr Armijo-Olivo, Mr da Costa, DrGadotti, Dr Major, Dr Thie, and Dr Mageeprovided writing. Dr Armijo-Olivo, Mr Fuen-

tes, Mr da Costa, and Dr Gadotti provideddata collection. Dr Armijo-Olivo and Dr War-ren provided data analysis. Dr Armijo-Olivoand Dr Magee provided project manage-ment. Dr Armijo-Olivo provided fund pro-curement. Dr Magee provided facilities/equipment and institutional liaisons. DrArmijo-Olivo, Mr Fuentes, Mr da Costa, DrGadotti, Dr Warren, Dr Major, Dr Thie, andDr Magee provided consultation (includingreview of manuscript before submission).

The authors thank all of the participants inthis study and Darrel Goertzen, Luis Cam-





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pos, and Rodrigo Guzman for their technicalassistance.

The study was approved by the Ethics Com-mittee of the University of Alberta, Edmon-ton, Alberta, Canada.

This research was presented at the XVIIIInternational Conference of the InternationalSociety of Electrophysiology and Kinesiol-ogy, June 16 19, 2010, Aalborg, Denmark;the 5th International Conference on Orofa-cial Pain and Temporomandibular Disorders,August 26 30, 2009, Praia do Forte, Bahia,Brazil; and the 13th World Conference onPain, August 29September 2, 2010, Mon-treal, Quebec, Canada.

Dr Armijo-Olivo was supported by the Cana-dian Institutes of Health Research (CIHR), theAlberta Provincial CIHR Training Program inBone and Joint Health, an Izaak Walton Kil-lam Scholarship from the University ofAlberta, and the Physiotherapy Foundationof Canada through an Ann Collins WhitmoreMemorial Award.Mr Fuentes is supportedbythe government of Chile (BECAS Chile Schol-arship Program) and Catholic University ofMaule, Chile.

DOI: 10.2522/ptj.20100233

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doi: 10.2522/ptj.20100233

Originally published online June 9, 20112011; 91:1184-1197.PHYS THER.

W. Major, Norman M.R. Thie and David J. MageePaulBruno R. da Costa, Inae C. Gadotti, Sharon Warren,

Susan Armijo-Olivo, Rony Silvestre, Jorge Fuentes,Flexion Test: A Cross-Sectional StudyDisorders While Performing the CraniocervicalMuscles in Patients With TemporomandibularElectromyographic Activity of the Cervical Flexor

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