research article muscle fatigue in the temporal and

7
Research Article Muscle Fatigue in the Temporal and Masseter Muscles in Patients with Temporomandibular Dysfunction Krzysztof Wofniak, 1 Mariusz Lipski, 2 Damian Lichota, 3 and Liliana Szyszka-Sommerfeld 1 1 Department of Orthodontics, Pomeranian Medical University of Szczecin, 70111 Szczecin, Poland 2 Department of Preclinical Conservative Dentistry and Preclinical Endodontics, Pomeranian Medical University of Szczecin, 70111 Szczecin, Poland 3 Department of Conservative Dentistry, Pomeranian Medical University of Szczecin, 70111 Szczecin, Poland Correspondence should be addressed to Krzysztof Wo´ zniak; [email protected] Received 8 August 2014; Revised 11 September 2014; Accepted 14 September 2014 Academic Editor: Mieszko Wieckiewicz Copyright © 2015 Krzysztof Wo´ zniak et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. e aim of this study is to evaluate muscle fatigue in the temporal and masseter muscles in patients with temporomandibular dysfunction (TMD). Two hundred volunteers aged 19.3 to 27.8 years (mean 21.50, SD 0.97) participated in this study. Electromyographical (EMG) recordings were performed using a DAB-Bluetooth Instrument (Zebris Medical GmbH, Germany). Muscle fatigue was evaluated on the basis of a maximum effort test. e test was performed during a 10-second maximum isometric contraction (MVC) of the jaws. An analysis of changes in the mean power frequency of the two pairs of temporal and masseter muscles (MPF%) revealed significant differences in the groups of patients with varying degrees of temporomandibular disorders according to Di ( < 0.0000). e study showed an increase in the muscle fatigue of the temporal and masseter muscles correlated with the intensity of temporomandibular dysfunction symptoms in patients. e use of surface electromyography in assessing muscle fatigue is an excellent diagnostic tool for identifying patients with temporomandibular dysfunction. 1. Introduction According to various reports, the prevalence of functional disorders in the population aged 3–74 years ranges from 7% to 84% [16]. According to Luther, such a large discrepancy is probably the result of using different methodologies in assessing these types of disorders [7]. A review of epidemiological studies conducted by McNeill [1] indicates that about 75% of the population has at least one objective symptom of functional disorders, whereas only 33% reports subjective symptoms. It is also estimated that a need for treatment is expressed by only 5-6% of a large population of people with temporomandibular dysfunction. Only a 7% rate in the occurrence of subjective symptoms of temporomandibular dysfunction was reported by List et al. [8] in a group of 826 children and adolescents aged 12 to 18 years. Similar conclusions regarding the disparity between the prevalence of subjective symptoms and the recorded evidence of functional disorders were presented by Mohlin et al. [2] following a critical review of 58 studies. A significant difference in the prevalence of subjective and objective symptoms was also revealed by a meta-analysis of 51 studies in the area of temporomandibular dysfunction conducted by de Kanter et al. [9]. e incidence of subjective symptoms was found to range between 6% and 93% and the incidence of objective symptoms, confirmed by clinical examination, between 0% and 93%. A significant discrepancy between the prevalence of subjective symptoms and objective symptoms, which are clinically confirmed signs of temporomandibular dysfunction, was also observed by Suvinen et al. [10]. An analysis of this phenomenon conducted by the authors revealed a relatively weak, on the borderline of statistical significance, correlation between subjective symptoms and objective symptoms observed in routine dental examination. Luther [11] demonstrates beyond any doubt that the disparity connected with a higher incidence of objective symptoms in relation to subjective symptoms is a characteristic feature of temporomandibular dysfunction. Hindawi Publishing Corporation BioMed Research International Volume 2015, Article ID 269734, 6 pages http://dx.doi.org/10.1155/2015/269734

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Page 1: Research Article Muscle Fatigue in the Temporal and

Research ArticleMuscle Fatigue in the Temporal and Masseter Muscles inPatients with Temporomandibular Dysfunction

Krzysztof Wofniak1 Mariusz Lipski2 Damian Lichota3 and Liliana Szyszka-Sommerfeld1

1Department of Orthodontics Pomeranian Medical University of Szczecin 70111 Szczecin Poland2Department of Preclinical Conservative Dentistry and Preclinical Endodontics Pomeranian Medical University of Szczecin70111 Szczecin Poland3Department of Conservative Dentistry Pomeranian Medical University of Szczecin 70111 Szczecin Poland

Correspondence should be addressed to Krzysztof Wozniak krzysztofwozniakpumedupl

Received 8 August 2014 Revised 11 September 2014 Accepted 14 September 2014

Academic Editor Mieszko Wieckiewicz

Copyright copy 2015 Krzysztof Wozniak et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

The aim of this study is to evaluate muscle fatigue in the temporal and masseter muscles in patients with temporomandibulardysfunction (TMD) Two hundred volunteers aged 193 to 278 years (mean 2150 SD 097) participated in this studyElectromyographical (EMG) recordings were performed using a DAB-Bluetooth Instrument (Zebris Medical GmbH Germany)Muscle fatigue was evaluated on the basis of amaximum effort testThe test was performed during a 10-secondmaximum isometriccontraction (MVC) of the jaws An analysis of changes in the mean power frequency of the two pairs of temporal and massetermuscles (MPF) revealed significant differences in the groups of patients with varying degrees of temporomandibular disordersaccording to Di (119875 lt 00000) The study showed an increase in the muscle fatigue of the temporal and masseter muscles correlatedwith the intensity of temporomandibular dysfunction symptoms in patients The use of surface electromyography in assessingmuscle fatigue is an excellent diagnostic tool for identifying patients with temporomandibular dysfunction

1 Introduction

According to various reports the prevalence of functionaldisorders in the population aged 3ndash74 years ranges from 7to 84 [1ndash6] According to Luther such a large discrepancyis probably the result of using different methodologies inassessing these types of disorders [7]

A review of epidemiological studies conducted byMcNeill [1] indicates that about 75 of the population has atleast one objective symptom of functional disorders whereasonly 33 reports subjective symptoms It is also estimatedthat a need for treatment is expressed by only 5-6 of a largepopulation of people with temporomandibular dysfunctionOnly a 7 rate in the occurrence of subjective symptoms oftemporomandibular dysfunction was reported by List et al[8] in a group of 826 children and adolescents aged 12 to 18years

Similar conclusions regarding the disparity between theprevalence of subjective symptoms and the recorded evidenceof functional disorders were presented by Mohlin et al

[2] following a critical review of 58 studies A significantdifference in the prevalence of subjective and objectivesymptoms was also revealed by a meta-analysis of 51 studiesin the area of temporomandibular dysfunction conducted byde Kanter et al [9] The incidence of subjective symptomswas found to range between 6 and 93 and the incidenceof objective symptoms confirmed by clinical examinationbetween 0 and 93 A significant discrepancy between theprevalence of subjective symptoms and objective symptomswhich are clinically confirmed signs of temporomandibulardysfunction was also observed by Suvinen et al [10] Ananalysis of this phenomenon conducted by the authorsrevealed a relatively weak on the borderline of statisticalsignificance correlation between subjective symptoms andobjective symptoms observed in routine dental examinationLuther [11] demonstrates beyond any doubt that the disparityconnected with a higher incidence of objective symptoms inrelation to subjective symptoms is a characteristic feature oftemporomandibular dysfunction

Hindawi Publishing CorporationBioMed Research InternationalVolume 2015 Article ID 269734 6 pageshttpdxdoiorg1011552015269734

2 BioMed Research International

Table 1 The exclusion criteria adopted in anamnesis and thenumber of patients included in the study

Total number of patients participated in the study 200

Exclusioncriteria

Depressive disorders 0Pain in other parts of the body 4Inflammations 3Taking painkillers and antidepressants 1Periodontal diseases 1Completed treatment of masticatorymotor system dysfunctions 2

Completed orthodontic treatment 15Total number of patients included in the study 174

In the light of the evidence presented expanding therepertoire ofmodern noninvasive diagnosticmethods shouldresult in obtaining more objective research results [12ndash14]

The aim of this study is to evaluate muscle fatigue in thetemporal and masseter muscles in patients with temporo-mandibular dysfunction

2 Materials and Methods

The research was approved by the Ethics Committee of thePomeranianMedical University in Szczecin Poland (numberBN-0014507) as being consistent with the principles ofGoodClinical Practice (GCP) All the patients were informedabout the aim and research design and they gave their consentin order to participate

Twohundred volunteers (100 females and 100males) aged193 to 278 (mean 2150 SD 097) referred to the Orthodon-tic Department of the Pomeranian Medical University inSzczecin participated in this study Inclusion criteria werethat the participants should be aged between 19 and 28 yearsand express consent to participate voluntarily in the study Asa result of the application of the adopted exclusion criterialisted in Table 1 174 of these (93 females and 81 males)qualified for further examination

Anamnestic interviews which included the patientsrsquo gen-eral medical history as well as detailed information abouttheir masticatory motor systemwere conductedThe patientswere divided according to a three-point anamnestic index oftemporomandibular dysfunction (Ai)

The assessment of the function of the masticatory motorsystem included clinical as well as electromyographic exami-nations The former involved visual and auscultatory assess-ment as well as palpation andmade it possible to qualitativelyand quantitatively evaluate the function of the masticatorysystem The clinical index of temporomandibular dysfunc-tion was used for the analysis of the data obtained from theclinical study (Table 2)The interpretation of the results of theclinical index of temporomandibular dysfunction (Di) basedon the total number of points obtained during the tests wasperformed according to the followingmodel (Table 3) [15 16]

EMG recordings were performed using a DAB-BluetoothInstrument (Zebris Medical GmbH Germany) During theserecordings each patient was sitting on a comfortable chair

Table 2 Clinical index of temporomandibular dysfunction (Di)

Di SymptomsMandibular movements

0 Normal range1 Small reduction in amplitude5 Large reduction in amplitude

Temporomandibular joint function

0 Smooth noiseless abduction and adduction ofmandible trajectory asymmetry lt2mm

1 Noise in one joint or both joints during abduction andadduction of mandible trajectory asymmetry gt2mm

5 Abduction of mandible impossible andor luxationMasticatory muscle pain

0 No tenderness1 Tenderness of 1ndash3 sites5 Tenderness of 4 and more sites

Temporomandibular joint pain0 No tenderness1 Unilateral or bilateral tenderness

5 Unilateral or bilateral tenderness of the dorsal surfaceof joint

Pain during movement of mandible0 No pain1 Pain during one out of all possible movement directions

5 Pain during more than one out of all possiblemovement directions

Table 3 Interpretation of the clinical index of temporomandibulardysfunction (Di)

Range Severity of dysfunction Description0 Di 0 No dysfunction1ndash4 Di I Mild dysfunction5ndash9 Di II Moderate dysfunction10ndash25 Di III Severe dysfunction

without head support and was instructed to assume a naturalhead position during electromyographic examination

Surface EMG signals were detected by four silversilverchloride (AgAgCl) disposable self-adhesive bipolar elec-trodes (Naroxon Dual Electrode Naroxon USA) with afixed interelectrode distance of 20mm The electrodes werepositioned on the anterior temporal muscles and the super-ficial masseter on both the left and the right sides parallelto the muscular fibres for the anterior temporal musclevertically along the anterior margin of the muscle for themasseter muscle parallel to the muscular fibres with theupper pole of the electrode at the intersection between thetragus-commissura labiorum and exocanthion-gonion linesA reference electrode was placed inferior and posterior to theright ear [17]

Before the recordings in order to reduce impedance theskin was carefully cleaned with 70 ethyl alcohol and driedThe EMG procedures were performed 5 minutes later

BioMed Research International 3

Table 4 Changes in mean power frequency (MPF) of muscles during 10 s of maximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction index Di

Di groupSidegender 0 I II III

119899 Mean SD 119899 Mean SD 119899 Mean SD 119899 Mean SDTemporal muscles

LeftFemales 22 minus218 699 39 minus664 513 25 minus1471 581 7 minus1044 914Males 23 minus280 354 29 minus610 534 23 minus1149 617 6 minus2783 082Total 45 minus250 545 68 minus641 519 48 minus1317 614 13 minus1847 1111

RightFemales 22 minus355 782 39 minus739 611 25 minus1503 404 7 minus1170 356Males 23 minus310 429 29 minus666 564 23 minus1114 487 6 minus2548 167Total 45 minus334 620 68 minus708 588 48 minus1317 483 13 minus1806 766

Masseter muscles

LeftFemales 22 minus189 751 39 minus1299 795 25 minus1951 481 7 minus979 1023Males 23 minus530 467 29 minus1095 414 23 minus1780 372 6 minus3677 743Total 45 minus364 639 68 minus1212 663 48 minus1869 436 13 minus2224 1647

RightFemales 22 minus335 1025 39 minus1485 880 25 minus1909 451 7 minus1477 418Males 23 minus520 590 29 minus1331 477 23 minus1766 337 6 minus3432 731Total 45 minus430 827 68 minus1419 735 48 minus1840 403 13 minus2379 1157

The DAB-Bluetooth Instrument was interfaced with acomputer which presented the data graphically and recordedit for further analysis The EMG signals were amplifieddigitized and digitally filtered

Muscle fatigue was evaluated on the basis of a maximumeffort test The test was performed during a 10-secondmaximum isometric contraction (MVC) of the jaws Analysisof themean power frequency (MPF) as a variable indepen-dent of the complex impedance of the measurement systemdid not require the use of a normalization process

The asymmetry between the activity of the left and theright jaw muscles was quantified by the Asymmetry Index(As) It ranges from 0 (total symmetry) to 100 (totalasymmetry) [18ndash20]

As =sum119873

119894=1

1003816100381610038161003816119877119894 minus 119871 1198941003816100381610038161003816

sum119873

119894=1(119877119894+ 119871119894)

sdot 100 (1)

The Kruskal-Wallis test the median and the Mann-Whitney119880 test were used to verify the hypotheses relating tothe existence or absence of differences between the mean val-ues of the independent variables The statistical significancefor verifying all the hypotheses was set at 119875 = 005

3 Results

The analysis of changes in the mean power frequency ofthe two pairs of temporal and masseter muscles (MPF)showed significant differences in the groups with varyingseverities of temporomandibular dysfunction according tothe Di index (119875 lt 00000 Table 4 Figure 1) There was asignificant tendency to increased fatigue in the testedmusclesin direct proportion to the severity of the temporomandibulardysfunction according to the Di

Weighted means

Vertical bars denote 095 confidence intervals

Temporal musclesMasseter muscles

0 I II IIIDi group

0

5

MPF

Wilks lambda = 48137 F(6336) = 24714 P = 00000

minus292

minus675

minus1317

minus1827

minus397

minus1315

minus1855

minus2302

minus35

minus30

minus25

minus20

minus15

minus10

minus5

Figure 1 Changes in mean power frequency (MPF) of musclesduring 10 s ofmaximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction

Resistance to muscle fatigue was modified at the level ofthe type of muscles examined (119875 lt 00000)There was alwaysgreater depletion of the interference signal in the case of themasseter muscles relative to the temporal muscles

Changes in the mean power frequency (MPF) of tem-poral muscles during 10 s of maximum voluntary contractionwere the lowest in the group with no symptoms of tem-poromandibular dysfunction (minus292) Significantly higher

4 BioMed Research International

depletion of the interference signal was observed in the groupwith mild dysfunction (minus675 119875 lt 00004) moderatedysfunction (minus1317 119875 lt 00000) and severe dysfunction(minus1827 119875 lt 00223) according to the Di index Therewere no significant differences in the fatigue of the right andleft temporal muscles in each group of temporomandibulardysfunction according to the Di index (119875 lt 00784)

Similar to the temporal muscles changes in the meanpower frequency of masseter muscles were the lowest inthe group with no symptoms of dysfunction (minus397)Significantly higher muscle fatigue as evidenced by a greaterreduction in the mean power frequency was found in groupswith mild dysfunction (minus1315 119875 lt 00000) moderatedysfunction (minus1855 119875 lt 00000) and severe dysfunction(minus2302 119875 lt 00341) according to the Di index As in thecase of the temporal muscles the impact of dysfunction onthe differences in fatigue between the right and left massetermuscles has not been confirmed (119875 lt 00937)

4 Discussion

Electromyography (EMG) is one of the few diagnostictools that enable direct and objective assessments of musclefunction Practitioners dealing with functional disorders ofthe masticatory motor system are particularly interested inglobal electromyography (surface electromyography (SEMG))because of the noninvasive nature of measurements that itprovides [21ndash25]

Assessing susceptibility to muscle fatigue is a crucialelement in the analysis of electromyographic examinationsFatigue is usually defined as the point beyond which aparticular level of force can no longer be maintained Meanpower frequency (MPF) and its changes linked to functionare a reliable and objective indicator of muscle resistanceto fatigue Thus changes in the frequency of the electricalactivity of muscles being a component of interference signaldepletion are a major predictor of susceptibility to musclefatigue in EMG recordings Muscle fatigue can also bedetermined by an increase in the EMG activity of musclesinvolved in generating a constant forceThis is consistent withthe view that generating a constant force as muscle fatigueincreases must be associated with an increase in the electricalactivity of muscles [26]

Our own examinations showed significant differenceswith regard to the type of muscles examined There wasa significantly greater depletion of the interference signalin respect of the changes in mean power frequency of themasseter muscles than the temporal muscles during 10 s ofmaximum isometric contraction in the intercuspal position

Changes in the interference signal with respect to themean power frequency of muscles during maximum isomet-ric contraction were also a strong predictor of functional dis-orders in the masticatory motor system Resistance to fatiguein the temporal andmassetermuscleswas significantly higherin the group with no symptoms of temporomandibular dys-function than in the group of patients with symptoms of dys-function according to the Di index There was a significantlygreater depletion of the interference signal for masseter andtemporal muscles in the group with TMD

Measurements of the mean power frequency of tempo-ral and masseter muscles also showed high discriminatoryefficiency for subjects with varying severities of temporo-mandibular dysfunctions according to the Di index Therewere significant differences in terms of fatigue betweenthe groups with varying severities of dysfunction for bothtemporal and masseter muscles

The results of the study were based on the clinical indexof temporomandibular dysfunction (Di)This index is simpleand easy to use and is extensively used in research [27]Although there are some limitations in using the Di it repre-sents a valid tool which correlates with the ResearchDiagnos-tic Criteria for Temporomandibular Disorders (RDCTMD)in identifying patients with symptoms of TMD [16 28]

In studies of masticatory muscle fatigue conducted bySforza et al [26] a muscle force sensor was used which waslocated on one side between the dental arches of ten healthysubjects This made it possible to terminate the effort test atthe precise moment when the subjects could no longer pro-duce the required bite force (127N) As in previous studiesthe endurance time ranging between 79 and 470 s in a groupof ten examined subjects was a prognostic factor for musclefatigue An analysis of mean power frequency at the begin-ning and at the end of the test showed a significant decrease inthe masseter muscles which was not confirmed with regardto the temporal muscles There was a significant decrease inthe mean power frequency of both masticatory muscles afterone minute on the side where the force sensor was placed

Hori et al [29] recorded mean power frequency (MPF)shift during fatigue and recovery of 46 healthy subjects and46 patients with craniomandibular disorder at the begin-ning and the end of fatiguing clenching and then 3 8 13and 18min following the fatiguing clenching The referenceclenching force was 80 of each subjectrsquos maximal volun-tary contraction (MVC) The results of the study showedsignificance between the healthy group and the group withcraniomandibular disorder in the three following points suchas the mean of MPF values of the masseter muscles at the endof fatiguing clenching the recovery pattern of the temporalmuscles andMPF shift induced by fatiguing clenchingTheseresults therefore suggest that measuring fatigue and recoveryMPF could be useful in the screening of craniomandibulardisorders

In studies conducted by Gay et al [30] surface EMGrecordings were made for both the masseter and anteriortemporal muscles while the subject held an incisal bite forcelevel of 10N for as long as possible The sample consisted of18 patients with symptoms of TMD and 15 patients with nosymptoms of TMD The results showed that the endurancetimes were significantly shorter for the TMD patients themasseter was not active in three of 17 TMD patients anddecreases in MPF over time were significantly greater for theTMD patients than normal subjects

A study by Castroflorio et al [31] concerned 20healthy volunteers and 18 patients with TMD An intraoralcompressive-force sensor was used to measure the voluntarycontraction forces close to the intercuspal position and toprovide visual feedback of submaximal forces to the subjectSurface EMG signals were recorded with linear electrode

BioMed Research International 5

arrays during isometric contractions at 20 40 60 and80 of the maximum voluntary contraction force during anendurance test and during the recovery phaseThe analysis ofthe results revealed that the temporal anterior and massetermuscle show the same myoelectric manifestations of fatigueand recovery and the initial values of the mean powerfrequency were lower in patients with muscle-related TMD

Liu et al [32] found significant differences in the meanpower frequency ofmasseter and temporalmuscles in a groupof 24 subjects who had at least one objective or subjectivesymptom of masticatory system dysfunction compared to agroup of 20 healthy people Although an analysis of the resultsin both the examined groups showed a similar mean powerfrequency both at the beginning and at the end of maximumcontraction in the intercuspal position over 30 s there was asignificantly greater decrease in themean power frequency ofthe temporal muscles (right 241 and left 229) and massetermuscles (right 192 and left 223) in the group with symptomsof TMD in comparison to the group with no symptoms ofTMD (temporal muscles right 134 and left 153 massetermuscles right 105 and left 109)

The studies presented whose observations are consistentwith the results of our own findings provide justificationfor using the analysis of muscle fatigue in the identificationand discrimination of subjects with symptoms of masticatorysystem dysfunction

5 Conclusions

(1) The results of the presented study showed an increasein the fatigue of temporal and masseter musclesin direct proportion to the severity of symptomsof temporomandibular dysfunction in the examinedpatients

(2) The use of surface electromyography in the assess-ment of muscle fatigue is an excellent diagnostictool for identifying patients with temporomandibulardysfunction

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C McNeill ldquoManagement of temporomandibular disordersconcepts and controversiesrdquo Journal of Prosthetic Dentistry vol77 no 5 pp 510ndash522 1997

[2] B Mohlin S Axelsson G Paulin et al ldquoTMD in relation tomalocclusion and orthodontic treatmentrdquo Angle Orthodontistvol 77 no 3 pp 542ndash548 2007

[3] M Wieckiewicz N Grychowska K Wojciechowski et alldquoPrevalence and correlation between TMD based on RDCTMDdiagnoses oral parafunctions and psychoemotional stressin Polish university studentsrdquo BioMed Research Internationalvol 2014 Article ID 472346 7 pages 2014

[4] A Anastassaki Kohler A Hugoson and T Magnusson ldquoPreva-lence of symptoms indicative of temporomandibular disorders

in adults cross-sectional epidemiological investigations cover-ing two decadesrdquo Acta Odontologica Scandinavica vol 70 no3 pp 213ndash223 2012

[5] A A Kohler A Hugoson and T Magnusson ldquoClinical signsindicative of temporomandibular disorders in adults timetrends and associated factorsrdquo Swedish Dental Journal vol 37no 1 pp 1ndash11 2013

[6] H Karibe G Goddard K Aoyagi et al ldquoComparison ofsubjective symptoms of temporomandibular disorders in youngpatients by age and genderrdquo Cranio vol 30 no 2 pp 114ndash1202012

[7] F Luther ldquoTMD and occlusion part I Damned if we doOcclusion the interface of dentistry and orthodonticsrdquo BritishDental Journal vol 202 no 1 p E2 2007

[8] T List K Wahlund B Wenneberg and S F Dworkin ldquoTMDin children and adolescents prevalence of pain gender differ-ences and perceived treatment needrdquo Journal of Orofacial Painvol 13 no 1 pp 9ndash20 1999

[9] R J A M de Kanter G J Truin R C W Burgersdijk et alldquoPrevalence in the Dutch adult population and a meta-analysisof signs and symptoms of temporomandibular disorderrdquo Jour-nal of Dental Research vol 72 no 11 pp 1509ndash1518 1993

[10] T I Suvinen M Nystrom M Evalahti E Kleemola-KujalaA Waltimo and M Kononen ldquoAn 8-year follow-up studyof temporomandibular disorder and psychosomatic symptomsfrom adolescence to young adulthoodrdquo Journal of OrofacialPain vol 18 no 2 pp 126ndash130 2004

[11] F Luther ldquoOrthodontics and the temporomandibular jointwhere are we now Part 1 Orthodontic treatment and temporo-mandibular disordersrdquo Angle Orthodontist vol 68 no 4 pp295ndash304 1998

[12] M Wieckiewicz M Zietek D Nowakowska and W Wieck-iewicz ldquoComparison of selected kinematic facebows applied tomandibular tracingrdquo BioMed Research International vol 2014Article ID 818694 5 pages 2014

[13] F Liu and A Steinkeler ldquoEpidemiology diagnosis and treat-ment of temporomandibular disordersrdquoDental Clinics of NorthAmerica vol 57 no 3 pp 465ndash479 2013

[14] M K Murphy R F MacBarb M E Wong and K A Athana-siou ldquoTemporomandibular disorders a review of etiologyclinical management and tissue engineering strategiesrdquo TheInternational Journal of Oral andMaxillofacial Implants vol 28no 6 pp e393ndashe414 2013

[15] R Napankangas A Raunio K Sipila and A Raustia ldquoEffectof mandibular advancement device therapy on the signs andsymptoms of temporomandibular disordersrdquo Journal of Oraland Maxillofacial Research vol 3 no 4 article e5 2013

[16] R A Leite J F Rodrigues M T Sakima and T Sakima ldquoRela-tionship between temporomandibular disorders and orthodon-tic treatment a literature reviewrdquo Dental Press Journal ofOrthodontics vol 18 no 1 pp 150ndash157 2013

[17] V F Ferrario C Sforza G Zanotti and G M TartaglialdquoMaximal bite forces in healthy young adults as predicted bysurface electromyographyrdquo Journal of Dentistry vol 32 no 6pp 451ndash457 2004

[18] V F Ferrario C Sforza A Colombo and V Ciusa ldquoAn elec-tromyographic investigation of masticatory muscles symmetryin normo-occlusion subjectsrdquo Journal of Oral Rehabilitationvol 27 no 1 pp 33ndash40 2000

[19] U Santana-Mora J Cudeiro M J Mora-Bermudez et alldquoChanges in EMG activity during clenching in chronic pain

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

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Page 2: Research Article Muscle Fatigue in the Temporal and

2 BioMed Research International

Table 1 The exclusion criteria adopted in anamnesis and thenumber of patients included in the study

Total number of patients participated in the study 200

Exclusioncriteria

Depressive disorders 0Pain in other parts of the body 4Inflammations 3Taking painkillers and antidepressants 1Periodontal diseases 1Completed treatment of masticatorymotor system dysfunctions 2

Completed orthodontic treatment 15Total number of patients included in the study 174

In the light of the evidence presented expanding therepertoire ofmodern noninvasive diagnosticmethods shouldresult in obtaining more objective research results [12ndash14]

The aim of this study is to evaluate muscle fatigue in thetemporal and masseter muscles in patients with temporo-mandibular dysfunction

2 Materials and Methods

The research was approved by the Ethics Committee of thePomeranianMedical University in Szczecin Poland (numberBN-0014507) as being consistent with the principles ofGoodClinical Practice (GCP) All the patients were informedabout the aim and research design and they gave their consentin order to participate

Twohundred volunteers (100 females and 100males) aged193 to 278 (mean 2150 SD 097) referred to the Orthodon-tic Department of the Pomeranian Medical University inSzczecin participated in this study Inclusion criteria werethat the participants should be aged between 19 and 28 yearsand express consent to participate voluntarily in the study Asa result of the application of the adopted exclusion criterialisted in Table 1 174 of these (93 females and 81 males)qualified for further examination

Anamnestic interviews which included the patientsrsquo gen-eral medical history as well as detailed information abouttheir masticatory motor systemwere conductedThe patientswere divided according to a three-point anamnestic index oftemporomandibular dysfunction (Ai)

The assessment of the function of the masticatory motorsystem included clinical as well as electromyographic exami-nations The former involved visual and auscultatory assess-ment as well as palpation andmade it possible to qualitativelyand quantitatively evaluate the function of the masticatorysystem The clinical index of temporomandibular dysfunc-tion was used for the analysis of the data obtained from theclinical study (Table 2)The interpretation of the results of theclinical index of temporomandibular dysfunction (Di) basedon the total number of points obtained during the tests wasperformed according to the followingmodel (Table 3) [15 16]

EMG recordings were performed using a DAB-BluetoothInstrument (Zebris Medical GmbH Germany) During theserecordings each patient was sitting on a comfortable chair

Table 2 Clinical index of temporomandibular dysfunction (Di)

Di SymptomsMandibular movements

0 Normal range1 Small reduction in amplitude5 Large reduction in amplitude

Temporomandibular joint function

0 Smooth noiseless abduction and adduction ofmandible trajectory asymmetry lt2mm

1 Noise in one joint or both joints during abduction andadduction of mandible trajectory asymmetry gt2mm

5 Abduction of mandible impossible andor luxationMasticatory muscle pain

0 No tenderness1 Tenderness of 1ndash3 sites5 Tenderness of 4 and more sites

Temporomandibular joint pain0 No tenderness1 Unilateral or bilateral tenderness

5 Unilateral or bilateral tenderness of the dorsal surfaceof joint

Pain during movement of mandible0 No pain1 Pain during one out of all possible movement directions

5 Pain during more than one out of all possiblemovement directions

Table 3 Interpretation of the clinical index of temporomandibulardysfunction (Di)

Range Severity of dysfunction Description0 Di 0 No dysfunction1ndash4 Di I Mild dysfunction5ndash9 Di II Moderate dysfunction10ndash25 Di III Severe dysfunction

without head support and was instructed to assume a naturalhead position during electromyographic examination

Surface EMG signals were detected by four silversilverchloride (AgAgCl) disposable self-adhesive bipolar elec-trodes (Naroxon Dual Electrode Naroxon USA) with afixed interelectrode distance of 20mm The electrodes werepositioned on the anterior temporal muscles and the super-ficial masseter on both the left and the right sides parallelto the muscular fibres for the anterior temporal musclevertically along the anterior margin of the muscle for themasseter muscle parallel to the muscular fibres with theupper pole of the electrode at the intersection between thetragus-commissura labiorum and exocanthion-gonion linesA reference electrode was placed inferior and posterior to theright ear [17]

Before the recordings in order to reduce impedance theskin was carefully cleaned with 70 ethyl alcohol and driedThe EMG procedures were performed 5 minutes later

BioMed Research International 3

Table 4 Changes in mean power frequency (MPF) of muscles during 10 s of maximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction index Di

Di groupSidegender 0 I II III

119899 Mean SD 119899 Mean SD 119899 Mean SD 119899 Mean SDTemporal muscles

LeftFemales 22 minus218 699 39 minus664 513 25 minus1471 581 7 minus1044 914Males 23 minus280 354 29 minus610 534 23 minus1149 617 6 minus2783 082Total 45 minus250 545 68 minus641 519 48 minus1317 614 13 minus1847 1111

RightFemales 22 minus355 782 39 minus739 611 25 minus1503 404 7 minus1170 356Males 23 minus310 429 29 minus666 564 23 minus1114 487 6 minus2548 167Total 45 minus334 620 68 minus708 588 48 minus1317 483 13 minus1806 766

Masseter muscles

LeftFemales 22 minus189 751 39 minus1299 795 25 minus1951 481 7 minus979 1023Males 23 minus530 467 29 minus1095 414 23 minus1780 372 6 minus3677 743Total 45 minus364 639 68 minus1212 663 48 minus1869 436 13 minus2224 1647

RightFemales 22 minus335 1025 39 minus1485 880 25 minus1909 451 7 minus1477 418Males 23 minus520 590 29 minus1331 477 23 minus1766 337 6 minus3432 731Total 45 minus430 827 68 minus1419 735 48 minus1840 403 13 minus2379 1157

The DAB-Bluetooth Instrument was interfaced with acomputer which presented the data graphically and recordedit for further analysis The EMG signals were amplifieddigitized and digitally filtered

Muscle fatigue was evaluated on the basis of a maximumeffort test The test was performed during a 10-secondmaximum isometric contraction (MVC) of the jaws Analysisof themean power frequency (MPF) as a variable indepen-dent of the complex impedance of the measurement systemdid not require the use of a normalization process

The asymmetry between the activity of the left and theright jaw muscles was quantified by the Asymmetry Index(As) It ranges from 0 (total symmetry) to 100 (totalasymmetry) [18ndash20]

As =sum119873

119894=1

1003816100381610038161003816119877119894 minus 119871 1198941003816100381610038161003816

sum119873

119894=1(119877119894+ 119871119894)

sdot 100 (1)

The Kruskal-Wallis test the median and the Mann-Whitney119880 test were used to verify the hypotheses relating tothe existence or absence of differences between the mean val-ues of the independent variables The statistical significancefor verifying all the hypotheses was set at 119875 = 005

3 Results

The analysis of changes in the mean power frequency ofthe two pairs of temporal and masseter muscles (MPF)showed significant differences in the groups with varyingseverities of temporomandibular dysfunction according tothe Di index (119875 lt 00000 Table 4 Figure 1) There was asignificant tendency to increased fatigue in the testedmusclesin direct proportion to the severity of the temporomandibulardysfunction according to the Di

Weighted means

Vertical bars denote 095 confidence intervals

Temporal musclesMasseter muscles

0 I II IIIDi group

0

5

MPF

Wilks lambda = 48137 F(6336) = 24714 P = 00000

minus292

minus675

minus1317

minus1827

minus397

minus1315

minus1855

minus2302

minus35

minus30

minus25

minus20

minus15

minus10

minus5

Figure 1 Changes in mean power frequency (MPF) of musclesduring 10 s ofmaximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction

Resistance to muscle fatigue was modified at the level ofthe type of muscles examined (119875 lt 00000)There was alwaysgreater depletion of the interference signal in the case of themasseter muscles relative to the temporal muscles

Changes in the mean power frequency (MPF) of tem-poral muscles during 10 s of maximum voluntary contractionwere the lowest in the group with no symptoms of tem-poromandibular dysfunction (minus292) Significantly higher

4 BioMed Research International

depletion of the interference signal was observed in the groupwith mild dysfunction (minus675 119875 lt 00004) moderatedysfunction (minus1317 119875 lt 00000) and severe dysfunction(minus1827 119875 lt 00223) according to the Di index Therewere no significant differences in the fatigue of the right andleft temporal muscles in each group of temporomandibulardysfunction according to the Di index (119875 lt 00784)

Similar to the temporal muscles changes in the meanpower frequency of masseter muscles were the lowest inthe group with no symptoms of dysfunction (minus397)Significantly higher muscle fatigue as evidenced by a greaterreduction in the mean power frequency was found in groupswith mild dysfunction (minus1315 119875 lt 00000) moderatedysfunction (minus1855 119875 lt 00000) and severe dysfunction(minus2302 119875 lt 00341) according to the Di index As in thecase of the temporal muscles the impact of dysfunction onthe differences in fatigue between the right and left massetermuscles has not been confirmed (119875 lt 00937)

4 Discussion

Electromyography (EMG) is one of the few diagnostictools that enable direct and objective assessments of musclefunction Practitioners dealing with functional disorders ofthe masticatory motor system are particularly interested inglobal electromyography (surface electromyography (SEMG))because of the noninvasive nature of measurements that itprovides [21ndash25]

Assessing susceptibility to muscle fatigue is a crucialelement in the analysis of electromyographic examinationsFatigue is usually defined as the point beyond which aparticular level of force can no longer be maintained Meanpower frequency (MPF) and its changes linked to functionare a reliable and objective indicator of muscle resistanceto fatigue Thus changes in the frequency of the electricalactivity of muscles being a component of interference signaldepletion are a major predictor of susceptibility to musclefatigue in EMG recordings Muscle fatigue can also bedetermined by an increase in the EMG activity of musclesinvolved in generating a constant forceThis is consistent withthe view that generating a constant force as muscle fatigueincreases must be associated with an increase in the electricalactivity of muscles [26]

Our own examinations showed significant differenceswith regard to the type of muscles examined There wasa significantly greater depletion of the interference signalin respect of the changes in mean power frequency of themasseter muscles than the temporal muscles during 10 s ofmaximum isometric contraction in the intercuspal position

Changes in the interference signal with respect to themean power frequency of muscles during maximum isomet-ric contraction were also a strong predictor of functional dis-orders in the masticatory motor system Resistance to fatiguein the temporal andmassetermuscleswas significantly higherin the group with no symptoms of temporomandibular dys-function than in the group of patients with symptoms of dys-function according to the Di index There was a significantlygreater depletion of the interference signal for masseter andtemporal muscles in the group with TMD

Measurements of the mean power frequency of tempo-ral and masseter muscles also showed high discriminatoryefficiency for subjects with varying severities of temporo-mandibular dysfunctions according to the Di index Therewere significant differences in terms of fatigue betweenthe groups with varying severities of dysfunction for bothtemporal and masseter muscles

The results of the study were based on the clinical indexof temporomandibular dysfunction (Di)This index is simpleand easy to use and is extensively used in research [27]Although there are some limitations in using the Di it repre-sents a valid tool which correlates with the ResearchDiagnos-tic Criteria for Temporomandibular Disorders (RDCTMD)in identifying patients with symptoms of TMD [16 28]

In studies of masticatory muscle fatigue conducted bySforza et al [26] a muscle force sensor was used which waslocated on one side between the dental arches of ten healthysubjects This made it possible to terminate the effort test atthe precise moment when the subjects could no longer pro-duce the required bite force (127N) As in previous studiesthe endurance time ranging between 79 and 470 s in a groupof ten examined subjects was a prognostic factor for musclefatigue An analysis of mean power frequency at the begin-ning and at the end of the test showed a significant decrease inthe masseter muscles which was not confirmed with regardto the temporal muscles There was a significant decrease inthe mean power frequency of both masticatory muscles afterone minute on the side where the force sensor was placed

Hori et al [29] recorded mean power frequency (MPF)shift during fatigue and recovery of 46 healthy subjects and46 patients with craniomandibular disorder at the begin-ning and the end of fatiguing clenching and then 3 8 13and 18min following the fatiguing clenching The referenceclenching force was 80 of each subjectrsquos maximal volun-tary contraction (MVC) The results of the study showedsignificance between the healthy group and the group withcraniomandibular disorder in the three following points suchas the mean of MPF values of the masseter muscles at the endof fatiguing clenching the recovery pattern of the temporalmuscles andMPF shift induced by fatiguing clenchingTheseresults therefore suggest that measuring fatigue and recoveryMPF could be useful in the screening of craniomandibulardisorders

In studies conducted by Gay et al [30] surface EMGrecordings were made for both the masseter and anteriortemporal muscles while the subject held an incisal bite forcelevel of 10N for as long as possible The sample consisted of18 patients with symptoms of TMD and 15 patients with nosymptoms of TMD The results showed that the endurancetimes were significantly shorter for the TMD patients themasseter was not active in three of 17 TMD patients anddecreases in MPF over time were significantly greater for theTMD patients than normal subjects

A study by Castroflorio et al [31] concerned 20healthy volunteers and 18 patients with TMD An intraoralcompressive-force sensor was used to measure the voluntarycontraction forces close to the intercuspal position and toprovide visual feedback of submaximal forces to the subjectSurface EMG signals were recorded with linear electrode

BioMed Research International 5

arrays during isometric contractions at 20 40 60 and80 of the maximum voluntary contraction force during anendurance test and during the recovery phaseThe analysis ofthe results revealed that the temporal anterior and massetermuscle show the same myoelectric manifestations of fatigueand recovery and the initial values of the mean powerfrequency were lower in patients with muscle-related TMD

Liu et al [32] found significant differences in the meanpower frequency ofmasseter and temporalmuscles in a groupof 24 subjects who had at least one objective or subjectivesymptom of masticatory system dysfunction compared to agroup of 20 healthy people Although an analysis of the resultsin both the examined groups showed a similar mean powerfrequency both at the beginning and at the end of maximumcontraction in the intercuspal position over 30 s there was asignificantly greater decrease in themean power frequency ofthe temporal muscles (right 241 and left 229) and massetermuscles (right 192 and left 223) in the group with symptomsof TMD in comparison to the group with no symptoms ofTMD (temporal muscles right 134 and left 153 massetermuscles right 105 and left 109)

The studies presented whose observations are consistentwith the results of our own findings provide justificationfor using the analysis of muscle fatigue in the identificationand discrimination of subjects with symptoms of masticatorysystem dysfunction

5 Conclusions

(1) The results of the presented study showed an increasein the fatigue of temporal and masseter musclesin direct proportion to the severity of symptomsof temporomandibular dysfunction in the examinedpatients

(2) The use of surface electromyography in the assess-ment of muscle fatigue is an excellent diagnostictool for identifying patients with temporomandibulardysfunction

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C McNeill ldquoManagement of temporomandibular disordersconcepts and controversiesrdquo Journal of Prosthetic Dentistry vol77 no 5 pp 510ndash522 1997

[2] B Mohlin S Axelsson G Paulin et al ldquoTMD in relation tomalocclusion and orthodontic treatmentrdquo Angle Orthodontistvol 77 no 3 pp 542ndash548 2007

[3] M Wieckiewicz N Grychowska K Wojciechowski et alldquoPrevalence and correlation between TMD based on RDCTMDdiagnoses oral parafunctions and psychoemotional stressin Polish university studentsrdquo BioMed Research Internationalvol 2014 Article ID 472346 7 pages 2014

[4] A Anastassaki Kohler A Hugoson and T Magnusson ldquoPreva-lence of symptoms indicative of temporomandibular disorders

in adults cross-sectional epidemiological investigations cover-ing two decadesrdquo Acta Odontologica Scandinavica vol 70 no3 pp 213ndash223 2012

[5] A A Kohler A Hugoson and T Magnusson ldquoClinical signsindicative of temporomandibular disorders in adults timetrends and associated factorsrdquo Swedish Dental Journal vol 37no 1 pp 1ndash11 2013

[6] H Karibe G Goddard K Aoyagi et al ldquoComparison ofsubjective symptoms of temporomandibular disorders in youngpatients by age and genderrdquo Cranio vol 30 no 2 pp 114ndash1202012

[7] F Luther ldquoTMD and occlusion part I Damned if we doOcclusion the interface of dentistry and orthodonticsrdquo BritishDental Journal vol 202 no 1 p E2 2007

[8] T List K Wahlund B Wenneberg and S F Dworkin ldquoTMDin children and adolescents prevalence of pain gender differ-ences and perceived treatment needrdquo Journal of Orofacial Painvol 13 no 1 pp 9ndash20 1999

[9] R J A M de Kanter G J Truin R C W Burgersdijk et alldquoPrevalence in the Dutch adult population and a meta-analysisof signs and symptoms of temporomandibular disorderrdquo Jour-nal of Dental Research vol 72 no 11 pp 1509ndash1518 1993

[10] T I Suvinen M Nystrom M Evalahti E Kleemola-KujalaA Waltimo and M Kononen ldquoAn 8-year follow-up studyof temporomandibular disorder and psychosomatic symptomsfrom adolescence to young adulthoodrdquo Journal of OrofacialPain vol 18 no 2 pp 126ndash130 2004

[11] F Luther ldquoOrthodontics and the temporomandibular jointwhere are we now Part 1 Orthodontic treatment and temporo-mandibular disordersrdquo Angle Orthodontist vol 68 no 4 pp295ndash304 1998

[12] M Wieckiewicz M Zietek D Nowakowska and W Wieck-iewicz ldquoComparison of selected kinematic facebows applied tomandibular tracingrdquo BioMed Research International vol 2014Article ID 818694 5 pages 2014

[13] F Liu and A Steinkeler ldquoEpidemiology diagnosis and treat-ment of temporomandibular disordersrdquoDental Clinics of NorthAmerica vol 57 no 3 pp 465ndash479 2013

[14] M K Murphy R F MacBarb M E Wong and K A Athana-siou ldquoTemporomandibular disorders a review of etiologyclinical management and tissue engineering strategiesrdquo TheInternational Journal of Oral andMaxillofacial Implants vol 28no 6 pp e393ndashe414 2013

[15] R Napankangas A Raunio K Sipila and A Raustia ldquoEffectof mandibular advancement device therapy on the signs andsymptoms of temporomandibular disordersrdquo Journal of Oraland Maxillofacial Research vol 3 no 4 article e5 2013

[16] R A Leite J F Rodrigues M T Sakima and T Sakima ldquoRela-tionship between temporomandibular disorders and orthodon-tic treatment a literature reviewrdquo Dental Press Journal ofOrthodontics vol 18 no 1 pp 150ndash157 2013

[17] V F Ferrario C Sforza G Zanotti and G M TartaglialdquoMaximal bite forces in healthy young adults as predicted bysurface electromyographyrdquo Journal of Dentistry vol 32 no 6pp 451ndash457 2004

[18] V F Ferrario C Sforza A Colombo and V Ciusa ldquoAn elec-tromyographic investigation of masticatory muscles symmetryin normo-occlusion subjectsrdquo Journal of Oral Rehabilitationvol 27 no 1 pp 33ndash40 2000

[19] U Santana-Mora J Cudeiro M J Mora-Bermudez et alldquoChanges in EMG activity during clenching in chronic pain

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

Submit your manuscripts athttpwwwhindawicom

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Disease Markers

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Research Article Muscle Fatigue in the Temporal and

BioMed Research International 3

Table 4 Changes in mean power frequency (MPF) of muscles during 10 s of maximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction index Di

Di groupSidegender 0 I II III

119899 Mean SD 119899 Mean SD 119899 Mean SD 119899 Mean SDTemporal muscles

LeftFemales 22 minus218 699 39 minus664 513 25 minus1471 581 7 minus1044 914Males 23 minus280 354 29 minus610 534 23 minus1149 617 6 minus2783 082Total 45 minus250 545 68 minus641 519 48 minus1317 614 13 minus1847 1111

RightFemales 22 minus355 782 39 minus739 611 25 minus1503 404 7 minus1170 356Males 23 minus310 429 29 minus666 564 23 minus1114 487 6 minus2548 167Total 45 minus334 620 68 minus708 588 48 minus1317 483 13 minus1806 766

Masseter muscles

LeftFemales 22 minus189 751 39 minus1299 795 25 minus1951 481 7 minus979 1023Males 23 minus530 467 29 minus1095 414 23 minus1780 372 6 minus3677 743Total 45 minus364 639 68 minus1212 663 48 minus1869 436 13 minus2224 1647

RightFemales 22 minus335 1025 39 minus1485 880 25 minus1909 451 7 minus1477 418Males 23 minus520 590 29 minus1331 477 23 minus1766 337 6 minus3432 731Total 45 minus430 827 68 minus1419 735 48 minus1840 403 13 minus2379 1157

The DAB-Bluetooth Instrument was interfaced with acomputer which presented the data graphically and recordedit for further analysis The EMG signals were amplifieddigitized and digitally filtered

Muscle fatigue was evaluated on the basis of a maximumeffort test The test was performed during a 10-secondmaximum isometric contraction (MVC) of the jaws Analysisof themean power frequency (MPF) as a variable indepen-dent of the complex impedance of the measurement systemdid not require the use of a normalization process

The asymmetry between the activity of the left and theright jaw muscles was quantified by the Asymmetry Index(As) It ranges from 0 (total symmetry) to 100 (totalasymmetry) [18ndash20]

As =sum119873

119894=1

1003816100381610038161003816119877119894 minus 119871 1198941003816100381610038161003816

sum119873

119894=1(119877119894+ 119871119894)

sdot 100 (1)

The Kruskal-Wallis test the median and the Mann-Whitney119880 test were used to verify the hypotheses relating tothe existence or absence of differences between the mean val-ues of the independent variables The statistical significancefor verifying all the hypotheses was set at 119875 = 005

3 Results

The analysis of changes in the mean power frequency ofthe two pairs of temporal and masseter muscles (MPF)showed significant differences in the groups with varyingseverities of temporomandibular dysfunction according tothe Di index (119875 lt 00000 Table 4 Figure 1) There was asignificant tendency to increased fatigue in the testedmusclesin direct proportion to the severity of the temporomandibulardysfunction according to the Di

Weighted means

Vertical bars denote 095 confidence intervals

Temporal musclesMasseter muscles

0 I II IIIDi group

0

5

MPF

Wilks lambda = 48137 F(6336) = 24714 P = 00000

minus292

minus675

minus1317

minus1827

minus397

minus1315

minus1855

minus2302

minus35

minus30

minus25

minus20

minus15

minus10

minus5

Figure 1 Changes in mean power frequency (MPF) of musclesduring 10 s ofmaximal voluntary contraction in intercuspal positiondepending on the temporomandibular dysfunction

Resistance to muscle fatigue was modified at the level ofthe type of muscles examined (119875 lt 00000)There was alwaysgreater depletion of the interference signal in the case of themasseter muscles relative to the temporal muscles

Changes in the mean power frequency (MPF) of tem-poral muscles during 10 s of maximum voluntary contractionwere the lowest in the group with no symptoms of tem-poromandibular dysfunction (minus292) Significantly higher

4 BioMed Research International

depletion of the interference signal was observed in the groupwith mild dysfunction (minus675 119875 lt 00004) moderatedysfunction (minus1317 119875 lt 00000) and severe dysfunction(minus1827 119875 lt 00223) according to the Di index Therewere no significant differences in the fatigue of the right andleft temporal muscles in each group of temporomandibulardysfunction according to the Di index (119875 lt 00784)

Similar to the temporal muscles changes in the meanpower frequency of masseter muscles were the lowest inthe group with no symptoms of dysfunction (minus397)Significantly higher muscle fatigue as evidenced by a greaterreduction in the mean power frequency was found in groupswith mild dysfunction (minus1315 119875 lt 00000) moderatedysfunction (minus1855 119875 lt 00000) and severe dysfunction(minus2302 119875 lt 00341) according to the Di index As in thecase of the temporal muscles the impact of dysfunction onthe differences in fatigue between the right and left massetermuscles has not been confirmed (119875 lt 00937)

4 Discussion

Electromyography (EMG) is one of the few diagnostictools that enable direct and objective assessments of musclefunction Practitioners dealing with functional disorders ofthe masticatory motor system are particularly interested inglobal electromyography (surface electromyography (SEMG))because of the noninvasive nature of measurements that itprovides [21ndash25]

Assessing susceptibility to muscle fatigue is a crucialelement in the analysis of electromyographic examinationsFatigue is usually defined as the point beyond which aparticular level of force can no longer be maintained Meanpower frequency (MPF) and its changes linked to functionare a reliable and objective indicator of muscle resistanceto fatigue Thus changes in the frequency of the electricalactivity of muscles being a component of interference signaldepletion are a major predictor of susceptibility to musclefatigue in EMG recordings Muscle fatigue can also bedetermined by an increase in the EMG activity of musclesinvolved in generating a constant forceThis is consistent withthe view that generating a constant force as muscle fatigueincreases must be associated with an increase in the electricalactivity of muscles [26]

Our own examinations showed significant differenceswith regard to the type of muscles examined There wasa significantly greater depletion of the interference signalin respect of the changes in mean power frequency of themasseter muscles than the temporal muscles during 10 s ofmaximum isometric contraction in the intercuspal position

Changes in the interference signal with respect to themean power frequency of muscles during maximum isomet-ric contraction were also a strong predictor of functional dis-orders in the masticatory motor system Resistance to fatiguein the temporal andmassetermuscleswas significantly higherin the group with no symptoms of temporomandibular dys-function than in the group of patients with symptoms of dys-function according to the Di index There was a significantlygreater depletion of the interference signal for masseter andtemporal muscles in the group with TMD

Measurements of the mean power frequency of tempo-ral and masseter muscles also showed high discriminatoryefficiency for subjects with varying severities of temporo-mandibular dysfunctions according to the Di index Therewere significant differences in terms of fatigue betweenthe groups with varying severities of dysfunction for bothtemporal and masseter muscles

The results of the study were based on the clinical indexof temporomandibular dysfunction (Di)This index is simpleand easy to use and is extensively used in research [27]Although there are some limitations in using the Di it repre-sents a valid tool which correlates with the ResearchDiagnos-tic Criteria for Temporomandibular Disorders (RDCTMD)in identifying patients with symptoms of TMD [16 28]

In studies of masticatory muscle fatigue conducted bySforza et al [26] a muscle force sensor was used which waslocated on one side between the dental arches of ten healthysubjects This made it possible to terminate the effort test atthe precise moment when the subjects could no longer pro-duce the required bite force (127N) As in previous studiesthe endurance time ranging between 79 and 470 s in a groupof ten examined subjects was a prognostic factor for musclefatigue An analysis of mean power frequency at the begin-ning and at the end of the test showed a significant decrease inthe masseter muscles which was not confirmed with regardto the temporal muscles There was a significant decrease inthe mean power frequency of both masticatory muscles afterone minute on the side where the force sensor was placed

Hori et al [29] recorded mean power frequency (MPF)shift during fatigue and recovery of 46 healthy subjects and46 patients with craniomandibular disorder at the begin-ning and the end of fatiguing clenching and then 3 8 13and 18min following the fatiguing clenching The referenceclenching force was 80 of each subjectrsquos maximal volun-tary contraction (MVC) The results of the study showedsignificance between the healthy group and the group withcraniomandibular disorder in the three following points suchas the mean of MPF values of the masseter muscles at the endof fatiguing clenching the recovery pattern of the temporalmuscles andMPF shift induced by fatiguing clenchingTheseresults therefore suggest that measuring fatigue and recoveryMPF could be useful in the screening of craniomandibulardisorders

In studies conducted by Gay et al [30] surface EMGrecordings were made for both the masseter and anteriortemporal muscles while the subject held an incisal bite forcelevel of 10N for as long as possible The sample consisted of18 patients with symptoms of TMD and 15 patients with nosymptoms of TMD The results showed that the endurancetimes were significantly shorter for the TMD patients themasseter was not active in three of 17 TMD patients anddecreases in MPF over time were significantly greater for theTMD patients than normal subjects

A study by Castroflorio et al [31] concerned 20healthy volunteers and 18 patients with TMD An intraoralcompressive-force sensor was used to measure the voluntarycontraction forces close to the intercuspal position and toprovide visual feedback of submaximal forces to the subjectSurface EMG signals were recorded with linear electrode

BioMed Research International 5

arrays during isometric contractions at 20 40 60 and80 of the maximum voluntary contraction force during anendurance test and during the recovery phaseThe analysis ofthe results revealed that the temporal anterior and massetermuscle show the same myoelectric manifestations of fatigueand recovery and the initial values of the mean powerfrequency were lower in patients with muscle-related TMD

Liu et al [32] found significant differences in the meanpower frequency ofmasseter and temporalmuscles in a groupof 24 subjects who had at least one objective or subjectivesymptom of masticatory system dysfunction compared to agroup of 20 healthy people Although an analysis of the resultsin both the examined groups showed a similar mean powerfrequency both at the beginning and at the end of maximumcontraction in the intercuspal position over 30 s there was asignificantly greater decrease in themean power frequency ofthe temporal muscles (right 241 and left 229) and massetermuscles (right 192 and left 223) in the group with symptomsof TMD in comparison to the group with no symptoms ofTMD (temporal muscles right 134 and left 153 massetermuscles right 105 and left 109)

The studies presented whose observations are consistentwith the results of our own findings provide justificationfor using the analysis of muscle fatigue in the identificationand discrimination of subjects with symptoms of masticatorysystem dysfunction

5 Conclusions

(1) The results of the presented study showed an increasein the fatigue of temporal and masseter musclesin direct proportion to the severity of symptomsof temporomandibular dysfunction in the examinedpatients

(2) The use of surface electromyography in the assess-ment of muscle fatigue is an excellent diagnostictool for identifying patients with temporomandibulardysfunction

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C McNeill ldquoManagement of temporomandibular disordersconcepts and controversiesrdquo Journal of Prosthetic Dentistry vol77 no 5 pp 510ndash522 1997

[2] B Mohlin S Axelsson G Paulin et al ldquoTMD in relation tomalocclusion and orthodontic treatmentrdquo Angle Orthodontistvol 77 no 3 pp 542ndash548 2007

[3] M Wieckiewicz N Grychowska K Wojciechowski et alldquoPrevalence and correlation between TMD based on RDCTMDdiagnoses oral parafunctions and psychoemotional stressin Polish university studentsrdquo BioMed Research Internationalvol 2014 Article ID 472346 7 pages 2014

[4] A Anastassaki Kohler A Hugoson and T Magnusson ldquoPreva-lence of symptoms indicative of temporomandibular disorders

in adults cross-sectional epidemiological investigations cover-ing two decadesrdquo Acta Odontologica Scandinavica vol 70 no3 pp 213ndash223 2012

[5] A A Kohler A Hugoson and T Magnusson ldquoClinical signsindicative of temporomandibular disorders in adults timetrends and associated factorsrdquo Swedish Dental Journal vol 37no 1 pp 1ndash11 2013

[6] H Karibe G Goddard K Aoyagi et al ldquoComparison ofsubjective symptoms of temporomandibular disorders in youngpatients by age and genderrdquo Cranio vol 30 no 2 pp 114ndash1202012

[7] F Luther ldquoTMD and occlusion part I Damned if we doOcclusion the interface of dentistry and orthodonticsrdquo BritishDental Journal vol 202 no 1 p E2 2007

[8] T List K Wahlund B Wenneberg and S F Dworkin ldquoTMDin children and adolescents prevalence of pain gender differ-ences and perceived treatment needrdquo Journal of Orofacial Painvol 13 no 1 pp 9ndash20 1999

[9] R J A M de Kanter G J Truin R C W Burgersdijk et alldquoPrevalence in the Dutch adult population and a meta-analysisof signs and symptoms of temporomandibular disorderrdquo Jour-nal of Dental Research vol 72 no 11 pp 1509ndash1518 1993

[10] T I Suvinen M Nystrom M Evalahti E Kleemola-KujalaA Waltimo and M Kononen ldquoAn 8-year follow-up studyof temporomandibular disorder and psychosomatic symptomsfrom adolescence to young adulthoodrdquo Journal of OrofacialPain vol 18 no 2 pp 126ndash130 2004

[11] F Luther ldquoOrthodontics and the temporomandibular jointwhere are we now Part 1 Orthodontic treatment and temporo-mandibular disordersrdquo Angle Orthodontist vol 68 no 4 pp295ndash304 1998

[12] M Wieckiewicz M Zietek D Nowakowska and W Wieck-iewicz ldquoComparison of selected kinematic facebows applied tomandibular tracingrdquo BioMed Research International vol 2014Article ID 818694 5 pages 2014

[13] F Liu and A Steinkeler ldquoEpidemiology diagnosis and treat-ment of temporomandibular disordersrdquoDental Clinics of NorthAmerica vol 57 no 3 pp 465ndash479 2013

[14] M K Murphy R F MacBarb M E Wong and K A Athana-siou ldquoTemporomandibular disorders a review of etiologyclinical management and tissue engineering strategiesrdquo TheInternational Journal of Oral andMaxillofacial Implants vol 28no 6 pp e393ndashe414 2013

[15] R Napankangas A Raunio K Sipila and A Raustia ldquoEffectof mandibular advancement device therapy on the signs andsymptoms of temporomandibular disordersrdquo Journal of Oraland Maxillofacial Research vol 3 no 4 article e5 2013

[16] R A Leite J F Rodrigues M T Sakima and T Sakima ldquoRela-tionship between temporomandibular disorders and orthodon-tic treatment a literature reviewrdquo Dental Press Journal ofOrthodontics vol 18 no 1 pp 150ndash157 2013

[17] V F Ferrario C Sforza G Zanotti and G M TartaglialdquoMaximal bite forces in healthy young adults as predicted bysurface electromyographyrdquo Journal of Dentistry vol 32 no 6pp 451ndash457 2004

[18] V F Ferrario C Sforza A Colombo and V Ciusa ldquoAn elec-tromyographic investigation of masticatory muscles symmetryin normo-occlusion subjectsrdquo Journal of Oral Rehabilitationvol 27 no 1 pp 33ndash40 2000

[19] U Santana-Mora J Cudeiro M J Mora-Bermudez et alldquoChanges in EMG activity during clenching in chronic pain

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Research Article Muscle Fatigue in the Temporal and

4 BioMed Research International

depletion of the interference signal was observed in the groupwith mild dysfunction (minus675 119875 lt 00004) moderatedysfunction (minus1317 119875 lt 00000) and severe dysfunction(minus1827 119875 lt 00223) according to the Di index Therewere no significant differences in the fatigue of the right andleft temporal muscles in each group of temporomandibulardysfunction according to the Di index (119875 lt 00784)

Similar to the temporal muscles changes in the meanpower frequency of masseter muscles were the lowest inthe group with no symptoms of dysfunction (minus397)Significantly higher muscle fatigue as evidenced by a greaterreduction in the mean power frequency was found in groupswith mild dysfunction (minus1315 119875 lt 00000) moderatedysfunction (minus1855 119875 lt 00000) and severe dysfunction(minus2302 119875 lt 00341) according to the Di index As in thecase of the temporal muscles the impact of dysfunction onthe differences in fatigue between the right and left massetermuscles has not been confirmed (119875 lt 00937)

4 Discussion

Electromyography (EMG) is one of the few diagnostictools that enable direct and objective assessments of musclefunction Practitioners dealing with functional disorders ofthe masticatory motor system are particularly interested inglobal electromyography (surface electromyography (SEMG))because of the noninvasive nature of measurements that itprovides [21ndash25]

Assessing susceptibility to muscle fatigue is a crucialelement in the analysis of electromyographic examinationsFatigue is usually defined as the point beyond which aparticular level of force can no longer be maintained Meanpower frequency (MPF) and its changes linked to functionare a reliable and objective indicator of muscle resistanceto fatigue Thus changes in the frequency of the electricalactivity of muscles being a component of interference signaldepletion are a major predictor of susceptibility to musclefatigue in EMG recordings Muscle fatigue can also bedetermined by an increase in the EMG activity of musclesinvolved in generating a constant forceThis is consistent withthe view that generating a constant force as muscle fatigueincreases must be associated with an increase in the electricalactivity of muscles [26]

Our own examinations showed significant differenceswith regard to the type of muscles examined There wasa significantly greater depletion of the interference signalin respect of the changes in mean power frequency of themasseter muscles than the temporal muscles during 10 s ofmaximum isometric contraction in the intercuspal position

Changes in the interference signal with respect to themean power frequency of muscles during maximum isomet-ric contraction were also a strong predictor of functional dis-orders in the masticatory motor system Resistance to fatiguein the temporal andmassetermuscleswas significantly higherin the group with no symptoms of temporomandibular dys-function than in the group of patients with symptoms of dys-function according to the Di index There was a significantlygreater depletion of the interference signal for masseter andtemporal muscles in the group with TMD

Measurements of the mean power frequency of tempo-ral and masseter muscles also showed high discriminatoryefficiency for subjects with varying severities of temporo-mandibular dysfunctions according to the Di index Therewere significant differences in terms of fatigue betweenthe groups with varying severities of dysfunction for bothtemporal and masseter muscles

The results of the study were based on the clinical indexof temporomandibular dysfunction (Di)This index is simpleand easy to use and is extensively used in research [27]Although there are some limitations in using the Di it repre-sents a valid tool which correlates with the ResearchDiagnos-tic Criteria for Temporomandibular Disorders (RDCTMD)in identifying patients with symptoms of TMD [16 28]

In studies of masticatory muscle fatigue conducted bySforza et al [26] a muscle force sensor was used which waslocated on one side between the dental arches of ten healthysubjects This made it possible to terminate the effort test atthe precise moment when the subjects could no longer pro-duce the required bite force (127N) As in previous studiesthe endurance time ranging between 79 and 470 s in a groupof ten examined subjects was a prognostic factor for musclefatigue An analysis of mean power frequency at the begin-ning and at the end of the test showed a significant decrease inthe masseter muscles which was not confirmed with regardto the temporal muscles There was a significant decrease inthe mean power frequency of both masticatory muscles afterone minute on the side where the force sensor was placed

Hori et al [29] recorded mean power frequency (MPF)shift during fatigue and recovery of 46 healthy subjects and46 patients with craniomandibular disorder at the begin-ning and the end of fatiguing clenching and then 3 8 13and 18min following the fatiguing clenching The referenceclenching force was 80 of each subjectrsquos maximal volun-tary contraction (MVC) The results of the study showedsignificance between the healthy group and the group withcraniomandibular disorder in the three following points suchas the mean of MPF values of the masseter muscles at the endof fatiguing clenching the recovery pattern of the temporalmuscles andMPF shift induced by fatiguing clenchingTheseresults therefore suggest that measuring fatigue and recoveryMPF could be useful in the screening of craniomandibulardisorders

In studies conducted by Gay et al [30] surface EMGrecordings were made for both the masseter and anteriortemporal muscles while the subject held an incisal bite forcelevel of 10N for as long as possible The sample consisted of18 patients with symptoms of TMD and 15 patients with nosymptoms of TMD The results showed that the endurancetimes were significantly shorter for the TMD patients themasseter was not active in three of 17 TMD patients anddecreases in MPF over time were significantly greater for theTMD patients than normal subjects

A study by Castroflorio et al [31] concerned 20healthy volunteers and 18 patients with TMD An intraoralcompressive-force sensor was used to measure the voluntarycontraction forces close to the intercuspal position and toprovide visual feedback of submaximal forces to the subjectSurface EMG signals were recorded with linear electrode

BioMed Research International 5

arrays during isometric contractions at 20 40 60 and80 of the maximum voluntary contraction force during anendurance test and during the recovery phaseThe analysis ofthe results revealed that the temporal anterior and massetermuscle show the same myoelectric manifestations of fatigueand recovery and the initial values of the mean powerfrequency were lower in patients with muscle-related TMD

Liu et al [32] found significant differences in the meanpower frequency ofmasseter and temporalmuscles in a groupof 24 subjects who had at least one objective or subjectivesymptom of masticatory system dysfunction compared to agroup of 20 healthy people Although an analysis of the resultsin both the examined groups showed a similar mean powerfrequency both at the beginning and at the end of maximumcontraction in the intercuspal position over 30 s there was asignificantly greater decrease in themean power frequency ofthe temporal muscles (right 241 and left 229) and massetermuscles (right 192 and left 223) in the group with symptomsof TMD in comparison to the group with no symptoms ofTMD (temporal muscles right 134 and left 153 massetermuscles right 105 and left 109)

The studies presented whose observations are consistentwith the results of our own findings provide justificationfor using the analysis of muscle fatigue in the identificationand discrimination of subjects with symptoms of masticatorysystem dysfunction

5 Conclusions

(1) The results of the presented study showed an increasein the fatigue of temporal and masseter musclesin direct proportion to the severity of symptomsof temporomandibular dysfunction in the examinedpatients

(2) The use of surface electromyography in the assess-ment of muscle fatigue is an excellent diagnostictool for identifying patients with temporomandibulardysfunction

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C McNeill ldquoManagement of temporomandibular disordersconcepts and controversiesrdquo Journal of Prosthetic Dentistry vol77 no 5 pp 510ndash522 1997

[2] B Mohlin S Axelsson G Paulin et al ldquoTMD in relation tomalocclusion and orthodontic treatmentrdquo Angle Orthodontistvol 77 no 3 pp 542ndash548 2007

[3] M Wieckiewicz N Grychowska K Wojciechowski et alldquoPrevalence and correlation between TMD based on RDCTMDdiagnoses oral parafunctions and psychoemotional stressin Polish university studentsrdquo BioMed Research Internationalvol 2014 Article ID 472346 7 pages 2014

[4] A Anastassaki Kohler A Hugoson and T Magnusson ldquoPreva-lence of symptoms indicative of temporomandibular disorders

in adults cross-sectional epidemiological investigations cover-ing two decadesrdquo Acta Odontologica Scandinavica vol 70 no3 pp 213ndash223 2012

[5] A A Kohler A Hugoson and T Magnusson ldquoClinical signsindicative of temporomandibular disorders in adults timetrends and associated factorsrdquo Swedish Dental Journal vol 37no 1 pp 1ndash11 2013

[6] H Karibe G Goddard K Aoyagi et al ldquoComparison ofsubjective symptoms of temporomandibular disorders in youngpatients by age and genderrdquo Cranio vol 30 no 2 pp 114ndash1202012

[7] F Luther ldquoTMD and occlusion part I Damned if we doOcclusion the interface of dentistry and orthodonticsrdquo BritishDental Journal vol 202 no 1 p E2 2007

[8] T List K Wahlund B Wenneberg and S F Dworkin ldquoTMDin children and adolescents prevalence of pain gender differ-ences and perceived treatment needrdquo Journal of Orofacial Painvol 13 no 1 pp 9ndash20 1999

[9] R J A M de Kanter G J Truin R C W Burgersdijk et alldquoPrevalence in the Dutch adult population and a meta-analysisof signs and symptoms of temporomandibular disorderrdquo Jour-nal of Dental Research vol 72 no 11 pp 1509ndash1518 1993

[10] T I Suvinen M Nystrom M Evalahti E Kleemola-KujalaA Waltimo and M Kononen ldquoAn 8-year follow-up studyof temporomandibular disorder and psychosomatic symptomsfrom adolescence to young adulthoodrdquo Journal of OrofacialPain vol 18 no 2 pp 126ndash130 2004

[11] F Luther ldquoOrthodontics and the temporomandibular jointwhere are we now Part 1 Orthodontic treatment and temporo-mandibular disordersrdquo Angle Orthodontist vol 68 no 4 pp295ndash304 1998

[12] M Wieckiewicz M Zietek D Nowakowska and W Wieck-iewicz ldquoComparison of selected kinematic facebows applied tomandibular tracingrdquo BioMed Research International vol 2014Article ID 818694 5 pages 2014

[13] F Liu and A Steinkeler ldquoEpidemiology diagnosis and treat-ment of temporomandibular disordersrdquoDental Clinics of NorthAmerica vol 57 no 3 pp 465ndash479 2013

[14] M K Murphy R F MacBarb M E Wong and K A Athana-siou ldquoTemporomandibular disorders a review of etiologyclinical management and tissue engineering strategiesrdquo TheInternational Journal of Oral andMaxillofacial Implants vol 28no 6 pp e393ndashe414 2013

[15] R Napankangas A Raunio K Sipila and A Raustia ldquoEffectof mandibular advancement device therapy on the signs andsymptoms of temporomandibular disordersrdquo Journal of Oraland Maxillofacial Research vol 3 no 4 article e5 2013

[16] R A Leite J F Rodrigues M T Sakima and T Sakima ldquoRela-tionship between temporomandibular disorders and orthodon-tic treatment a literature reviewrdquo Dental Press Journal ofOrthodontics vol 18 no 1 pp 150ndash157 2013

[17] V F Ferrario C Sforza G Zanotti and G M TartaglialdquoMaximal bite forces in healthy young adults as predicted bysurface electromyographyrdquo Journal of Dentistry vol 32 no 6pp 451ndash457 2004

[18] V F Ferrario C Sforza A Colombo and V Ciusa ldquoAn elec-tromyographic investigation of masticatory muscles symmetryin normo-occlusion subjectsrdquo Journal of Oral Rehabilitationvol 27 no 1 pp 33ndash40 2000

[19] U Santana-Mora J Cudeiro M J Mora-Bermudez et alldquoChanges in EMG activity during clenching in chronic pain

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Research Article Muscle Fatigue in the Temporal and

BioMed Research International 5

arrays during isometric contractions at 20 40 60 and80 of the maximum voluntary contraction force during anendurance test and during the recovery phaseThe analysis ofthe results revealed that the temporal anterior and massetermuscle show the same myoelectric manifestations of fatigueand recovery and the initial values of the mean powerfrequency were lower in patients with muscle-related TMD

Liu et al [32] found significant differences in the meanpower frequency ofmasseter and temporalmuscles in a groupof 24 subjects who had at least one objective or subjectivesymptom of masticatory system dysfunction compared to agroup of 20 healthy people Although an analysis of the resultsin both the examined groups showed a similar mean powerfrequency both at the beginning and at the end of maximumcontraction in the intercuspal position over 30 s there was asignificantly greater decrease in themean power frequency ofthe temporal muscles (right 241 and left 229) and massetermuscles (right 192 and left 223) in the group with symptomsof TMD in comparison to the group with no symptoms ofTMD (temporal muscles right 134 and left 153 massetermuscles right 105 and left 109)

The studies presented whose observations are consistentwith the results of our own findings provide justificationfor using the analysis of muscle fatigue in the identificationand discrimination of subjects with symptoms of masticatorysystem dysfunction

5 Conclusions

(1) The results of the presented study showed an increasein the fatigue of temporal and masseter musclesin direct proportion to the severity of symptomsof temporomandibular dysfunction in the examinedpatients

(2) The use of surface electromyography in the assess-ment of muscle fatigue is an excellent diagnostictool for identifying patients with temporomandibulardysfunction

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] C McNeill ldquoManagement of temporomandibular disordersconcepts and controversiesrdquo Journal of Prosthetic Dentistry vol77 no 5 pp 510ndash522 1997

[2] B Mohlin S Axelsson G Paulin et al ldquoTMD in relation tomalocclusion and orthodontic treatmentrdquo Angle Orthodontistvol 77 no 3 pp 542ndash548 2007

[3] M Wieckiewicz N Grychowska K Wojciechowski et alldquoPrevalence and correlation between TMD based on RDCTMDdiagnoses oral parafunctions and psychoemotional stressin Polish university studentsrdquo BioMed Research Internationalvol 2014 Article ID 472346 7 pages 2014

[4] A Anastassaki Kohler A Hugoson and T Magnusson ldquoPreva-lence of symptoms indicative of temporomandibular disorders

in adults cross-sectional epidemiological investigations cover-ing two decadesrdquo Acta Odontologica Scandinavica vol 70 no3 pp 213ndash223 2012

[5] A A Kohler A Hugoson and T Magnusson ldquoClinical signsindicative of temporomandibular disorders in adults timetrends and associated factorsrdquo Swedish Dental Journal vol 37no 1 pp 1ndash11 2013

[6] H Karibe G Goddard K Aoyagi et al ldquoComparison ofsubjective symptoms of temporomandibular disorders in youngpatients by age and genderrdquo Cranio vol 30 no 2 pp 114ndash1202012

[7] F Luther ldquoTMD and occlusion part I Damned if we doOcclusion the interface of dentistry and orthodonticsrdquo BritishDental Journal vol 202 no 1 p E2 2007

[8] T List K Wahlund B Wenneberg and S F Dworkin ldquoTMDin children and adolescents prevalence of pain gender differ-ences and perceived treatment needrdquo Journal of Orofacial Painvol 13 no 1 pp 9ndash20 1999

[9] R J A M de Kanter G J Truin R C W Burgersdijk et alldquoPrevalence in the Dutch adult population and a meta-analysisof signs and symptoms of temporomandibular disorderrdquo Jour-nal of Dental Research vol 72 no 11 pp 1509ndash1518 1993

[10] T I Suvinen M Nystrom M Evalahti E Kleemola-KujalaA Waltimo and M Kononen ldquoAn 8-year follow-up studyof temporomandibular disorder and psychosomatic symptomsfrom adolescence to young adulthoodrdquo Journal of OrofacialPain vol 18 no 2 pp 126ndash130 2004

[11] F Luther ldquoOrthodontics and the temporomandibular jointwhere are we now Part 1 Orthodontic treatment and temporo-mandibular disordersrdquo Angle Orthodontist vol 68 no 4 pp295ndash304 1998

[12] M Wieckiewicz M Zietek D Nowakowska and W Wieck-iewicz ldquoComparison of selected kinematic facebows applied tomandibular tracingrdquo BioMed Research International vol 2014Article ID 818694 5 pages 2014

[13] F Liu and A Steinkeler ldquoEpidemiology diagnosis and treat-ment of temporomandibular disordersrdquoDental Clinics of NorthAmerica vol 57 no 3 pp 465ndash479 2013

[14] M K Murphy R F MacBarb M E Wong and K A Athana-siou ldquoTemporomandibular disorders a review of etiologyclinical management and tissue engineering strategiesrdquo TheInternational Journal of Oral andMaxillofacial Implants vol 28no 6 pp e393ndashe414 2013

[15] R Napankangas A Raunio K Sipila and A Raustia ldquoEffectof mandibular advancement device therapy on the signs andsymptoms of temporomandibular disordersrdquo Journal of Oraland Maxillofacial Research vol 3 no 4 article e5 2013

[16] R A Leite J F Rodrigues M T Sakima and T Sakima ldquoRela-tionship between temporomandibular disorders and orthodon-tic treatment a literature reviewrdquo Dental Press Journal ofOrthodontics vol 18 no 1 pp 150ndash157 2013

[17] V F Ferrario C Sforza G Zanotti and G M TartaglialdquoMaximal bite forces in healthy young adults as predicted bysurface electromyographyrdquo Journal of Dentistry vol 32 no 6pp 451ndash457 2004

[18] V F Ferrario C Sforza A Colombo and V Ciusa ldquoAn elec-tromyographic investigation of masticatory muscles symmetryin normo-occlusion subjectsrdquo Journal of Oral Rehabilitationvol 27 no 1 pp 33ndash40 2000

[19] U Santana-Mora J Cudeiro M J Mora-Bermudez et alldquoChanges in EMG activity during clenching in chronic pain

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Research Article Muscle Fatigue in the Temporal and

6 BioMed Research International

patients with unilateral temporomandibular disordersrdquo Journalof Electromyography and Kinesiology vol 19 no 6 pp e543ndashe549 2009

[20] D Rodrigues Bigaton K C S Berni A F N Almeida and MT Silva ldquoActivity and asymmetry index of masticatory musclesin women with and without dysfunction temporomandibularrdquoElectromyography and Clinical Neurophysiology vol 50 no 7-8pp 333ndash338 2010

[21] F Bosman and H W van der Glas ldquoElectromyography Aid indiagnosis therapy and therapy evaluation in temporomandibu-lar dysfunctionrdquoNederlands Tijdschrift voor Tandheelkunde vol103 no 7 pp 254ndash257 1996

[22] L B Goldstein ldquoThe use of surface electromyography inobjective measurement of the muscle function in facialpaintemporomandibular dysfunction patientsrdquoThe FunctionalOrthodontist vol 17 no 3 pp 26ndash29 2000

[23] B C Cooper ldquoMore about TMD and SEMGrdquo Journal of theAmerican Dental Association vol 137 no 10 p 1366 2006

[24] T I Suvinen and P Kemppainen ldquoReview of clinical EMGstudies related to muscle and occlusal factors in healthy andTMD subjectsrdquo Journal of Oral Rehabilitation vol 34 no 9 pp631ndash644 2007

[25] V F Ferrario G M Tartaglia F E Luraghi and C SforzaldquoThe use of surface electromyography as a tool in differentiatingtemporomandibular disorders from neck disordersrdquo ManualTherapy vol 12 no 4 pp 372ndash379 2007

[26] C Sforza G Zanotti E Mantovani and V F Ferrario ldquoFatiguein the masseter and temporalis muscles at constant loadrdquoCranio vol 25 no 1 pp 30ndash36 2007

[27] C M De Felicio M De Oliveira Melchior and M A M R DaSilva ldquoClinical validity of the protocol for multi-professionalcenters for the determination of signs and symptoms of tem-poromandibular disorders Part IIrdquo CraniomdashJournal of Cran-iomandibular Practice vol 27 no 1 pp 62ndash67 2009

[28] J Pehling E Schiffman J Look J Shaefer P Lenton andJ Fricton ldquoInterexaminer reliability and clinical validity ofthe temporomandibular index a new outcome measure fortemporomandibular disordersrdquo Journal of Orofacial Pain vol16 no 4 pp 296ndash304 2002

[29] H Hori H Kobayashi T Hayashi and S Kohno ldquoMean powerfrequency shift during fatigue and recovery in patients withcraniomandibular disordersrdquo Journal of Oral Rehabilitation vol22 no 2 pp 159ndash165 1995

[30] T Gay B Maton J Rendell and A Majourau ldquoCharacteristicsof muscle fatigue in patients with myofascial pain-dysfunctionsyndromerdquo Archives of Oral Biology vol 39 no 10 pp 847ndash8521994

[31] T Castroflorio D Falla G M Tartaglia C Sforza and ADeregibus ldquoMyoelectric manifestations of jaw elevator musclefatigue and recovery in healthy and TMD subjectsrdquo Journal ofOral Rehabilitation vol 39 no 9 pp 648ndash658 2012

[32] Z J Liu K Yamagata Y Kasahara and G Ito ldquoElectromyo-graphic examination of jaw muscles in relation to symptomsand occlusion of patients with temporomandibular joint dis-ordersrdquo Journal of Oral Rehabilitation vol 26 no 1 pp 33ndash471999

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Research Article Muscle Fatigue in the Temporal and

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom