We investigated the characteristics of grouped discharge (GD) waveforms obtained from long-term masseter electromyogram (EMG) recording in 6 female temporomandibular disorder (TMD) patients with myofascial pain and 6 healthy females. The EMG measurement was performed from the morning of the experiment day until the subject woke up the next day. We observed a significantly larger number of GD waveforms in the TMD group compared to the control group (p=0.002). Our results indicate that the existence of GD waveforms in masseter EMGs might be a predictor of future TMD with myofascial pain

Kawakami, Shigehisa

Kodama, Naoki

Maeda, Naoto

Manda, Yosuke

Minagi, Shogo

Oki, Kazuhiro

Okayama University Digital Information Repository

Characteristics of Grouped Discharge Waveforms Observed in Long-term Masseter Muscle Electromyographic Recording: A Preliminary Study

Okayama University Scientific Achievement Repository

A lthough temporomandibular disorder (TMD) is thought to be related to awake and/or sleep brux-ism in various stomatognathic diseases,  the cause for its occurrence has not yet been elucidated fully [1].  A cor-relation has been reported between TMD — especially myofascial pain dysfunction — and masticatory muscle activity,  which indicates the necessity of further detailed analyses of masticatory muscle activity to determine the pathophysiology of TMD by using surface electromy-ography (EMG) of the masseter muscles [2].The improvement of portable EMG devices in terms of size and accuracy has made it possible to record mas-seter EMG activity throughout the 24-h day [3].  In recent years,  close associations have been reported between masseter EMG activity (except for chewing) and various pathological conditions of the stomatog-nathic system that remain to be identified [4].  Our earlier study elucidated that intermittent jaw clenching while awake is strongly related to the collapse of occlusion [5].Bruxism,  one of the non-functional occlusal habits,  is classified as grinding,  clenching,  and other nonspe-cific mandibular movements [6].  In the analysis of bruxism activities,  it is common to set cutoff values based on maximum voluntary clenching (MVC),  and these activities are usually classified as phasic,  tonic,  and mixed episodes [6].  However,  in our previous study [5] we often observed a distinct waveform that differed from phasic,  tonic,  and mixed episodes.  This EMG waveform is similar to the grouped discharge (GD) waveform that is observed in the physiological tremor recorded from the extensor digitorum of the arm [7].  Although it is known that that physiological tremor is promoted by muscle fatigue,  the existence of a GD and/or physiological tremor in masseter muscles has not yet been elucidated [8].  We conducted the present study to analyze the characteristics of the GD waveform obtained from masseter EMG recorded throughout the 24-h day in TMD patients with myofascial pain and in healthy subjects.????????? ????????? ????????? ???? ???? ??? ???? ??????????????????? ?????????????????????????????????????????http ://escholarship.lib.okayama-u.ac.jp/amo/Short CommunicationCharacteristics of Grouped Discharge Waveforms Observed in Long-term Masseter Muscle Electromyographic Recording: A Preliminary StudyNaoto Maeda,  Naoki Kodama＊,  Yosuke Manda,  Shigehisa Kawakami,   Kazuhiro Oki,  and Shogo MinagiDepartment of Occlusal and Oral Functional Rehabilitation,  Okayama University Graduate School of Medicine,   Dentistry and Pharmaceutical Sciences,  Okayama 700-8558,  JapanWe investigated the characteristics of grouped discharge (GD) waveforms obtained from long-term masseter electromyogram (EMG) recording in 6 female temporomandibular disorder (TMD) patients with myofascial pain and 6 healthy females.  The EMG measurement was performed from the morning of the experiment day until the subject woke up the next day.  We observed a significantly larger number of GD waveforms in the TMD group compared to the control group (p= 0.002).  Our results indicate that the existence of GD waveforms in masseter EMGs might be a predictor of future TMD with myofascial pain.Key words:  temporomandibular disorder,  grouped discharge,  masseter muscle,  electromyographyReceived August 28, 2018 ; accepted April 4, 2019.＊Corresponding author. Phone : +81-86-235-6687; Fax : +81-86-235-6689E-mail : naoki-k@md.okayama-u.ac.jp (N. Kodama)Conflict of Interest Disclosures: No potential conflict of interest relevant to this article was reported.Subjects and MethodsWe enrolled 6 female patients (age 64.5 ± 10.6 years) diagnosed with myofascial pain disease on the basis of Research Diagnostic Criteria for Temporomandibular Disorders classifications [9] at the Clinical Division of Occlusion and Removable Prosthodontics at Okayama University Hospital.  Six female patients (age 71.7 ± 8.3  years) who did not have TMD visiting the same hospi-tal’s Clinical Division of Preventive Dentistry for the maintenance of periodontitis were recruited as a control group.The sample size of 6 subjects in each group was determined based on the results of our preliminary measurement in the TMD and control groups.  The cal-culation was made using α = 0.05,  (1-β) = 0.8 and effect size = 1.7,  with G*Power 3.1.9.2 software.  Table 1 sum-marizes the characteristics of the TMD and control subjects.  The measurement of masseter EMG activity was performed as we described in our report by Kumazaki et al.  [3].  The portable EMG recording hard-ware consisted of analog signal processing and a differ-ential amplification-integrated hybrid circuit (NB- 6201HS; Nabtesco,  Kobe,  Japan),  which included a high-pass filter (10 Hz) and a low-pass filter (1,000 Hz),  and a two-channel digital recorder (ICR-PS004M;  Sanyo Electric,  Osaka,  Japan).An EMG was recorded using differential surface electrodes composed of three disposable Ag/AgCl sur-face electrodes (6 × 15 mm,  Vitrode F-150S;  Nihon Kohden,  Tokyo) with center-to-center distances of 15 mm.  The surface electrode was attached at the center of the subject’s left masseter muscle,  parallel to the muscle fibers.  The electrodes and cables were secured to the skin with thin biocompatible adhesive tape (Cathereep FS 1010; Nichiban,  Tokyo).  To eliminate the first-night effect,  the subjects were instructed to wear dummy electrodes and cables while sleeping on the day before the real measurement.The EMG measurement was performed from the morning of the day of the experiment to the time when the subject woke up the next day.  The subjects were instructed to perform MVC three times at the begin-ning and end of the recording.  The recorded EMG waveform was visually observed using analysis software (Sound Engine,  Coderium,  Sapporo,  Japan).  Waveforms in which the intensity of discharge was constant and maintained rhythmically were extracted as GD wave-forms.  We analyzed the total number,  frequency,  amplitude,  duration,  and total duration of GD wave-forms.  Student’s t-test was used for the evaluation of the total number of GD waveforms.  A significance level of 0.05 was used for the tests,  and two-sided tests were applied.  Data analyses were performed using SPSS 21.0 software (SPSS,  Chicago,  IL,  USA).  The study proto-col was approved by the Ethics Committee of the Okayama University Graduate School of Medicine,  Dentistry and Pharmaceutical Sciences (No. 1706-002).358 ???????????? ????????? ????????????? ???? ???? ??????? ?　 Characteristics of the TMD patients and control subjectsAge TMDtypeMusclepainNumber ofremaining teethRPDusage Dental Formula53 I Lt 24 － 765 321 |12 4567-----76 4321 |12 456772 I Rt 21 ＋ 5432 |1234-----654321 |123456751 I Lt/Rt 28 － 7654321 |1234567-----7654321 |123456764 I Lt/Rt 27 － 7654321 |1234 67-----87 54321 |123456770 I Rt 21 ＋ 76 4321 |12345-----5 321 |12345 877 I Lt 27 － 654321 |1234567-----7654321 |1234567Age TMDtypeMusclepainNumber ofremaining teethRPDusage Dental Formula67 － － 28 － 87654321 |123456-----7654321 |123456781 － － 23 ＋ 76 4321 |1234 6-----7 4321 |123456758 － － 25 － 7654321 |123456-----7 54321 |12345676 － － 25 － 654321 |123 5 7-----7654321 |123456777 － － 27 － 7654321 |1234567-----654321 |123456771 － － 26 － 76 4321 |12345-----87654321 |1234567Four of 6 TMD patients had unilateral muscle tenderness and two of 6 had bilateral muscle tenderness.ResultsFigure 1 provides a typical example of the EMG recording.  A typical example of the masseter EMG waveform at MVC three times is shown (Fig. 1A).  Compared to the EMG waveform of MVC in Figure 1A,  a low level EMG activity was observed rhythmically with the intensity of approx.  15% MVC (Fig. 1B),  which was the so-called GD waveform.  The frequency of GD waveform seems to be approx.  15 Hz (Fig. 1C).Table 2 summarizes the characteristics of the GD waveform for each subject.  A large number of GD waveforms were observed in all 6 patients in the TMD group.  The total number of GD waveforms observed in the TMD group was 5.8 ± 2.5.  The frequency of GD waveforms was 16.0 ± 3.1 Hz,  the amplitude was 18.0 ± 6.6% MVC,  the duration was 16.0 ± 27.6 sec,  and the total duration was 93.3 ± 68.2 sec.Only one GD waveform was observed in the control group,  in one of the 6 subjects.  The frequency of the GD waveform observed in the control group was 19.0 Hz,  the amplitude was 10.0% MVC,  and the duration was 14.0 sec.  The total number of GD waveforms was sig-nificantly higher in the TMD group than in the control ??????????? ????????????????????????????????????? ???????? 359???????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????????EMG amplitude -2.5dB-2.5-6.0-6.0-12.0-lnf-12.0-2.5dB-2.55s 1s0.1s-6.0-6.0-12.0-lnf-12.0-20.5-20.5-24.0-30.0-30.0-24.0dBAEMG amplitudeBEMG amplitudeC-lnf????? ?　 Characteristics of the GD waveform for each of the 12 subjectsTMDgroupTotal number(time/day)Frequency(Hz)Amplitude(%MVC)Duration(s)Total duration(s)Subject 1 10 16.4±2.4 16.5±4.5 17.5±25.4 175.1Subject 2 6 15.5±2.2 20.8±8.4 17.4±16.5 104.4Subject 3 5 18.6±2.6 21.0±2.0 9.0±5.5 93.0Subject 4 3 20 5 2.8±1.7 8.3Subject 5 7 12.3±2.1 22.1±2.5 26.6±48.6 186.2Subject 6 4 16.3±1.9 16.3±4.1 10.1±5.1 40.4ControlgroupTotal number(time/day)Frequency(Hz)Amplitude(%MVC)Duration(s)Total duration(s)Subject 1 0 n/a n/a n/a n/aSubject 2 0 n/a n/a n/a n/aSubject 3 1 19.0 10.0 14.0 14.0Subject 4 0 n/a n/a n/a n/aSubject 5 0 n/a n/a n/a n/aSubject 6 0 n/a n/a n/a n/aTotal number,  frequency,  intensity,  duration,  and total duration of GD waveforms were analyzed in 2 groups.  Values represented as mean (±standard deviation).???? ?　 Typical example of EMG recording in a TMD patient.  The EMG recording is stored in MP3 format with 64 kbps,  and the y-axis unit is decibels (dB) [3].  A,  The MVC recording; B,  The typ-ical EMG pattern of the GD wave-form; C,  Enlarged view of the boxed part in panel b.group (p = 0.002).DiscussionOur present EMG analyses revealed significantly more GD waveforms in the TMD patients with myofas-cial pain compared to the healthy subjects.  This is the first report to show the existence of GD waveforms in the masseter muscles of TMD patients.  Earlier studies showed that the masseter and temporalis muscles in patients with TMD were more easily fatigued compared to those in healthy adults [10 , 11].  The appearance of physiological tremor is increased with muscle fatigue.  Our present results indicate that the GD waveforms observed in TMD patients with myofascial pain may be due to masseter muscle fatigue [8].The frequency of GD waveforms in our present TMD group was 16.0 ± 3.1 Hz.  It was reported that the frequency of physiological tremor was generally 8-12 Hz [12]; the frequency of GD waveforms in the present TMD patients is thus slightly higher.  This is because the frequency of EMG activity decreases in the process of muscle fatigue,  which indicates that the GD waveforms we observed herein may appear at the beginning of muscle fatigue.  In addition,  the amplitude of the GD waveforms was 18.0 ± 6.6% MVC in the TMD group and 10.0% MVC in the control group.Masticatory muscle activity while awake and sleep bruxism are both usually classified as phasic,  tonic,  and mixed episodes in accordance with a set cutoff value,  the magnitude of which is often 20% MVC.  The ampli-tude of GD waveforms in the present study was smaller than that of the cutoff value used in the present EMG analysis.  This result indicated that the GD waveform might fall outside the scope of the analysis.A GD waveform was observed in one of our 6 con-trol subjects without myofascial pain,  demonstrating that the GD waveform is not present only in patients with myofascial pain.  However,  the frequency of GD waveforms observed in the control group (19.0 Hz) was slightly higher than that of the GD waveform in the TMD group (～16.0 Hz),  indicating that this was in the early stage of muscle fatigue.  Therefore,  the occurrence of the GD waveform might be an indicator of the risk of the development of TMD with myofascial pain.There were several limitations in this study.  First,  the number of subjects was small; investigations with more subjects are needed to test our findings.  Second,  the GD waveform in masticatory muscles has not yet been clearly defined,  and further studies are necessary to establish a clear definition of the GD waveform.This is the first report to demonstrate the existence of the GD waveform on masseter EMG.  If the GD wave-form is an indicator of muscle fatigue in the masseter muscle,  our findings offer researchers the advantage of not needing to fatigue subjects intentionally by giving them experimental tasks for their muscles.  Our results indicate that the existence of the GD waveform in mas-seter EMG might be used as a predictor of future TMD patients with myofascial pain.References 1. Reissmann DR,  John MT,  Aigner A,  Schon G,  Sierwald I and Schiﬀman EL: Interaction Between Awake and Sleep Bruxism Is Associated with Increased Presence of Painful Temporomandibular Disorder.  J Oral Facial Pain Headache (2017) 31: 299-305. 2. Glaros AG,  Marszalek JM and Williams KB: Longitudinal Multilevel Modeling of Facial Pain,  Muscle Tension,  and Stress.  J Dent Res (2016) 95: 416-422. 3. Kumazaki Y,  Naito M,  Kawakami S,  Hirata A,  Oki K and Minagi S:  Development of a speech-discriminating electromyogram system for routine ambulatory recordings for the low-level masseter muscle activity.  J Oral Rehabil (2014) 41: 266-274. 4. Manfredini D,  De Laat A,  Winocur E and Ahlberg J: Why not stop looking at bruxism as a black/white condition? Aetiology could be unrelated to clinical consequences.  J Oral Rehabil (2016) 43: 799-801. 5. Kawakami S,  Kumazaki Y,  Manda Y,  Oki K and Minagi S: Speciﬁc diurnal EMG activity pattern observed in occlusal collapse patients:  relationship between diurnal bruxism and tooth loss progression.  PLoS One (2014) 9: e101882. 6. Lavigne GJ,  Rompre PH and Montplaisir JY: Sleep bruxism: valid-ity of clinical research diagnostic criteria in a controlled polysom-nographic study.  J Dent Res (1996) 75: 546-552. 7. Morrison S,  Kavanagh J,  Obst SJ,  Irwin J and Haseler LJ: The eﬀects of unilateral muscle fatigue on bilateral physiological tremor.  Exp Brain Res (2005) 167: 609-621. 8. Köster B,  Lauk M,  Timmer J,  Winter T,  Guschlbauer B,  Glocker FX,  Danek A,  Deuschl G and Lücking CH: Central mechanisms in human enhanced physiological tremor.  Neurosci Lett (1998) 241:  135-138. 9. Dworkin SF and LeResche L: Research diagnostic criteria for temporomandibular disorders: review,  criteria,  examinations and speciﬁcations,  critique.  J Craniomandib Disord (1992) 6: 301-355.10. Pitta NC,  Nitsch GS,  Machado MB and de Oliveira AS: Activation time analysis and electromyographic fatigue in patients with tem-poromandibular disorders during clenching.  J Electromyogr Kinesiol (2015) 25: 653-657.11. Woźniak K,  Lipski M,  Lichota D and Szyszka-Sommerfeld L: Muscle fatigue in the temporal and masseter muscles in patients with tem-poromandibular dysfunction.  Biomed Res Int (2015) 269734.12. Novak T and Newell KM:  Physiological tremor (8-12 Hz compo-nent) in isometric force control.  Neurosci Lett (2017) 641: 87-93.360 ???????????? ????????? ????????????? ???? ???? ??

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Characteristics of Grouped Discharge Waveforms Observed in Long-term Masseter Muscle Electromyographic Recording: A Preliminary Study

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