Journal of
Oral Rehabilitation
Journal of Oral Rehabilitation 2009 36; 814–820
Postural and dynamic masseter and anterior temporalis muscle EMG repeatability in serial assessments T . I . S U V I N E N * , J . M A L M B E R G * , †, C . F O R S T E R ‡ & P . K E M P P A I N E N * , †
*University of
Turku, Turku, Finland, †Department of Oral and Maxillofacial Diseases, Turku University Central Hospital (TUCH), Turku, Finland and ‡
University of Erlangen-Nu¨rnberg, Erlangen, Germany
SUMMARY Electromyographic (EMG) assessment has been used as a non-invasive tool to objectively assess muscle function, although with controversial research and clinical potential. The aim of this study was to assess within-, inter-subject and betweenday repeatability of serial EMG recordings. The study sample included 10 asymptomatic subjects with no history of temporomandibular disorders or muscle parafunctions. Bilateral masseter and anterior temporalis muscle EMG parameters were assessed in two standardized serial recordings (day1 to day2) using a portable EMG equipment (ME 6000 recorder, Mega Electronics, Kuopio, Finland). The functional tasks included postural ⁄ resting activities as pre- and post-recording series of 30 s each and jaw opening ⁄ closing, intercuspal and maximal voluntary clenching activities of 5 s, repeated three times. The assessed EMG parameters included the mean amplitude, s.d. and error. In addition, the power spectrum EMG parameter
Introduction Surface electromyographic (EMG) assessment has been used as a non-invasive method to objectively record muscle activities and to evaluate the masticatory function of the stomatognathic system, although with some controversial research and clinical potential (1–3). Various EMG methods and parameters have been used to study craniofacial muscle function, such as resting or postural jaw opening and submaximal voluntary clenching and masticatory activities (4–8). EMG assessment has been applied also to study differ-
assessment included the median power frequencies and the averaged EMG spectrum data values. The results of the intraclass correlation coefficient analysis indicated reliability for nearly all of the intercuspal and all clenching EMG amplitude and power spectrum parameters. This was complemented by the repeated measures ANOVA and post hoc analyses that indicated non-significant differences between day 1 and 2 in task- and musclerelated analyses. Most variability was noted in postural and some in opening ⁄ closing tasks. In conclusion this study assessed the reliability, repeatability and limitations of postural and various dynamic masseter and temporalis EMG recordings for serial assessment. KEYWORDS: surface electromyography, masseter, temporalis, repeatability, reliability, serial assessment, power spectrum, postural, dynamic Accepted for publication 16 August 2009
ences between asymptomatic subjects and those suffering from various forms of craniofacial muscle-related dysfunctional symptoms e.g. muscle hyperactivity, bruxism, temporomandibular disorders (TMD) and ⁄ or craniofacial pain (3). The main problem to assess muscle dysfunctions or changes related to treatment interventions has been the lack of reliable and reproducible criteria and parameters that could be useful for comparative and longitudinal assessments (1–3, 9–11). In addition, a number of factors have been reported to influence the recorded EMG activity, e.g. the electrode type and positions, head position, structural
ª 2009 The Authors. Journal compilation ª 2009 Blackwell Publishing Ltd
doi: 10.1111/j.1365-2842.2009.01999.x
EMG PARAMETER REPEATABILITY IN SERIAL RECORDINGS
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Ten asymptomatic subjects (5 males, 5 females; mean age 26Æ9, range 21–50 years) participated in the study. The subjects were recruited as volunteers among the staff and students of the Institute of Dentistry, University of Turku, with the inclusion criteria as: no signs or symptoms of bruxism and ⁄ or TMD and full dentition. The Ethics Committee of the Medical Faculty of the University of Turku approved the experiments, and before the experiments the volunteers gave their informed consent in accordance with the Helsinki declaration of 1975. Bilateral masseter and anterior temporalis muscle EMG activities were assessed by one independent assessor in two serial recordings, which were conducted in a standardized way on two consecutive days. The surface electrodes were positioned according to the anatomical landmarks in masseter muscles (8, 17, 19) and in anterior temporalis muscles according to the protocol by Ferrario et al. (19). In addition, the inter-electrode distance
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Materials and methods
recommendations of 30 mm were observed in masseter electrode placements and a template was used to relocate electrodes (8, 16). The ground electrode ⁄ reference electrodes were placed on the chin and the forehead, respectively. All electrode sites were carefully cleaned by swabbing with 70% v ⁄ v alcohol to reduce the skin ⁄ electrode impedance before the placement of pregelled, self-adhesive and disposable bipolar paediatric ⁄ cardiac electrocardiographic electrodes (Ambu Blue Sensor; Ambu A ⁄ S, Ballerup, Denmark). Prior to the recording session the subjects were carefully and individually instructed regarding the recording schedule and protocol. Each subject was seated upright in a dental chair with the head supported and the Frankfurt horizontal plane parallel to the floor. Testing was performed in a silent and comfortable environment. During the recording the subjects were able to view the timing of each task on a computer screen. Each series of EMG recordings consisted of the following (Fig. 1): 1) Postural resting EMG activity – 30 s (total recording time). 2) Jaw opening activity – 3 · 5 s. 3) Jaw closing activity – 3 · 5 s. 4) Intercuspal activity – 3 · 5 s. 5) Maximal voluntary clenching activity – 3 · 5 s. For the analysis the following standardized recording ranges were selected:(i) postural – middle 10-s period of the 30 s recording range, (ii–v) dynamic – 2 s range in the middle of the 5 s recording range, more specifically from the beginning of the 2nd second to the end of 3rd second, apart from jaw closing, which was recorded from the beginning of 3rd second to the end of 4th second (corresponding approximately to the same vertical jaw separation as the opening range). O pe
factors, mimetic or crosstalk muscle activity and interand individual factors (1–3). Previously especially the clinical value of EMG assessment has been questioned, based on variable and controversial findings between different studies, the lack of normative data and various methodological or reliability problems (3, 9, 10). In recent years, however, more sophisticated techniques and replicable and comparative methods have again gradually increased the interest to use EMG research as a non-invasive tool ⁄ adjunct to more objectively measure and monitor craniofacial muscle function and dysfunction (1, 3, 7, 12–18). It is of importance, however, especially before assessing the diagnostic and clinical applications and use of EMG assessment in clinical research, to find most repeatable and reproducible EMG parameter ⁄ s, suitable especially for serial recordings. Therefore, the aim of this study was to test the reliability of the repeated use of a portable EMG measuring unit regarding within-subject, inter-subject and between-day differences using mean amplitude and power spectrum parameters of the EMG recordings from masseter and anterior temporalis. Standardized EMG measurements were performed during postural, jaw opening and closing, intercuspal and maximal voluntary clenching activities in asymptomatic subjects in two serial recordings.
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Fig. 1. Instructions and the standardized time sequences for dynamic task recordings (for each dynamic task the recording time = 5 s repeated three times with 5 s resting period before and after each activity and the analysed range = 2 s). A moving bar guided the subjects regarding the timing of the sequences.
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T . I . S U V I N E N et al. For the postural position (physiologic rest position) the subjects were instructed to swallow and rest their jaw with the teeth apart according to standard methods used in prosthodontics to establish freeway space (8). The rest position activities (Postural) were recorded over a 30 s period in the beginning and at the end of the recording session. For the jaw opening ⁄ closing EMG recordings the subjects were instructed to slowly open the mouth to maximal opening and slowly closing. The opening and ⁄ or closing movements (Open ⁄ Close) lasted 5 s each and were repeated in a similar manner three times, with a total recording time of 60 s. For the intercuspal position (Co) each subject was asked to put their teeth slightly together and to maintain the position with tooth contact and minimal muscular activity. For the maximal voluntary clenching (Clench) they were instructed to bite their teeth together as hard as possible. Each occlusal task lasted a minimum of 5 s and was repeated three times, with a total recording time of 60 s. The EMG activities were recorded by the recording equipment that consisted of a portable ME 6000 recorder* and PC computer for data storage. The technical characteristics included the following: the measuring band for the EMG signal was 8–500 Hz,; the measuring sensitivity from 1 to 20 000 lVs; the interference elimination coefficient for the common mode interferences, 111 dB; noise level 1.6 lV; and the total gain 305. The sampling frequency for power spectrum data was 2000 Hz. The raw EMG signals were amplified, averaged and integrated into root-mean-square values (rms) in nanovolts. The computer interface transmission was via USB cable. The computer displayed the raw EMG activity signals on the screen as a graphical data, which was saved at the end of each 30 or 60-s recording periods. For the analysis, the mean amplitude, s.d. and error for each muscle and each task were computed. The power spectrum EMG parameters included the median (MF) power frequencies and the averaged EMG (AEMG) spectrum area data values. The MF power frequency was the frequency that divided the area of the calculated spectrum in two equal areas. The AEMG was calculated from every Fast Fourier Transform algorithm frame, one averaged EMG value from the frame width in EMG data points used in calculation of *Mega Electronics, Kuopio, Finland.
spectrums. All values were calculated from the middle 10 s period of the 30 s postural data and from a 2 s period (2nd and 3rd second) during each 5 s occlusal task and in the beginning and at the end of the opening ⁄ closing circles (2 s corresponding to the same jaw opening period).
Statistical analyses To test for reliability of the repetition of the EMG measurements intraclass correlation coefficients (ICC two-way random models (20) were calculated for each pair of EMG parameters from day 1 versus day 2. The repetitions of the same measurement (e.g. three values of an open-task) were averaged and these mean values were used for this ICC analysis. ANOVA with repeated measures design was used as a complementary analysis. The factors of the effects within a subject were stimulus repetition (3 times) and day (2 days). In addition the type of muscle (4 muscles) was included as a categorical factor for the ANOVA. Post hoc tests (Fisher’s least significant difference) were performed on significant effects regarding the type of muscle. Each EMG parameter and each
Table 1. The intraclass correlation coefficients of the various EMG parameters between day 1 and day 2 Left Right Left Right masseter masseter temporalis temporalis Postural
Mean s.d. MF AEMG Open Mean s.d. MF AEMG Close Mean s.d. MF AEMG Intercuspal Mean (Co) s.d. MF AEMG Clench Mean s.d. MF AEMG
0Æ069 0Æ251 0Æ258 0Æ069 0Æ730 0Æ861 0Æ971 0Æ735 0Æ340 0Æ510 0Æ374 0Æ335 0Æ608 0Æ322 0Æ876 0Æ609 0Æ877 0Æ854 0Æ912 0Æ879
)0Æ004 )0Æ036 0Æ540 0Æ008 0Æ803 0Æ690 0Æ941 0Æ794 0Æ186 0Æ095 0Æ802 0Æ138 0Æ728 0Æ422 0Æ639 0Æ717 0Æ882 0Æ804 0Æ904 0Æ881
0Æ303 0Æ240 0Æ768 0Æ299 0Æ949 0Æ802 0Æ805 0Æ952 0Æ933 0Æ477 0Æ625 0Æ936 0Æ595 0Æ383 0Æ939 0Æ604 0Æ899 0Æ610 0Æ939 0Æ895
0Æ444 0Æ388 0Æ506 0Æ434 0Æ455 0Æ209 0Æ751 0Æ500 0Æ554 0Æ868 0Æ804 0Æ530 0Æ705 0Æ246 0Æ854 0Æ736 0Æ880 0Æ916 0Æ920 0Æ876
EMG, electromyographic; AEMG, averaged EMG; MF, median. All values which are not significant (P > 0Æ05) are printed in bold. ª 2009 The Authors. Journal compilation ª 2009 Blackwell Publishing Ltd
EMG PARAMETER REPEATABILITY IN SERIAL RECORDINGS task were analysed separately. Statistical values with P < 0Æ05 were considered as significant.
Results
Discussion The general aim of this study was to assess repeatable methods to obtain data for serial and comparative clinical evaluations. For this purpose several tests were
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As shown in Table 1 the ICCs were significant for most intercuspal (Mean, MF, AEMG) and all clenching EMG parameters indicating reliability for those parameters. This was further confirmed by the ANOVA where the between-day effects showed no differences (P > 0Æ05). Figures 2–3 illustrate the between-day repeatability of the power spectrum MF values and the mean EMG values (which showed similar results as the AEMG power spectrum data).
Most postural and some opening ⁄ closing data values showed non-significant ICCs and in the ANOVA significant differences between day1 and day2 (Table 1, Figs 4–6). These results indicated that the opening ⁄ closing tasks were most sensitive of the dynamic recordings for between-day differences and that the pre- and post-recording postural activities showed more effect for between-day versus within-day recordings.
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Fig. 2. The between-day effects in relation to intercuspal task and electromyographic parameters from all four muscles at day 1 and day 2 (MF and mean s.e.m.). MF, median.
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Fig. 3. The between-day effects in relation to clenching task and electromyographic parameters from all four muscles at day 1 and day 2 (MF and mean s.e.m.). MF, median.
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Fig. 4. The between-day effects in relation to open task and electromyographic parameters (MF and mean s.e.m.) from all four muscles at day 1 and day 2. MF, median. ª 2009 The Authors. Journal compilation ª 2009 Blackwell Publishing Ltd
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Fig. 5. The between-day effects in relation to close task and electromyographic parameters from all four muscles at day 1 and day 2 (MF and mean s.e.m.). MF, median.
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Fig. 6. The between-day effects in relation to postural task and electromyographic parameters from all four muscles at day 1 and day 2 (MF and mean s.e.m.) – within- and in-between-day differences (a = pre-postural, b = post-postural series). MF, median.
conducted in asymptomatic individuals. Especially the assessment of various functional and resting tasks and the relative value of various measured EMG parameters for repeated serial assessments were of interest. The results indicated that maximum voluntary clenching (MVC) and intercuspal biting could be reproduced from day 1 to day 2 and therefore were most repeatable of the dynamic tasks compared with opening and closing movement data. These results were also supported by the literature as several studies had used especially MVC activities as a useful method to obtain reliable data (3, 7, 21, 22). Ferrario et al. (18) and Tartaglia et al. (23) have further suggested that the method of normalized EMG indices using MVC values could further improve reliability, but this method is yet to be tested by other investigators. The opening and especially closing movements and their effect on EMG muscle activities are not often used in serial assessment studies. Of special interest are the studies by Lindauer et al. (5) that indicated a relationship between EMGforce characteristics and vertical dimension of jaw opening. Other studies have similarly reported variations in EMG patterns in relation to the degree of mandibular opening (8, 24–28). More studies are required to further test jaw opening and closing movement reliability and other aspects related to these, but
the basic protocol in this study design appeared repeatable in terms of serial assessment of functional tasks. Of special interest in this study was also to assess preand post-recording resting data values using within-day and between-day postural recordings. These data were used partly to test how the resting ⁄ postural values were affected by the study protocol i.e. by the series of various functional tests. Based on the results of this study it appeared that asymptomatic muscles behaved in a repeatable fashion within 1 day. Similar results have been reported by Castroflorio et al. (16). Many past studies have also reported variability and method sensitivity regarding the reliability of postural recordings (3, 6, 8, 19, 29). To obtain reliable comparative data for serial recordings it is therefore important that the conditions are standardized regarding the timing of the recordings (e.g. morning versus afternoon) and situational factors (e.g. familiarity with the recording series, other stressful events during the day), which may all cause unwanted or additional artefacts. Overall, to reduce the general individual bias special attention for the standardization of the protocol needs to be given in both research and clinical settings. One of the criticisms expressed against past EMG research has been the lack of repeatable standardized study design methods between various centres of
ª 2009 The Authors. Journal compilation ª 2009 Blackwell Publishing Ltd
EMG PARAMETER REPEATABILITY IN SERIAL RECORDINGS evaluations. Therefore in this study some of the methods used by Ferrario et al. (19) and Castroflorio et al. (16) were partially tested. In our design similar electrode placement in the temporalis muscle was used as Ferrario et al. (19) and the inter-electrode distance recommendations of 30 mm was observed in masseter electrode placements (8, 16). Also a template was used for electrode relocation (16). The used pre-gelled cardiac disposable electrodes were well tolerated and reported comfortable by the subjects. As the standardization of the electrode location and replacement between sessions has been reported as one of the major technical features causing variability (2), the tested methodology used in this study appeared reliable. Further studies and evaluations are still recommended to reach acceptable standards for these recordings, e.g. in terms of the innervation zones (16, 30). Most previous EMG studies have used the assessment of mean amplitude measurements (2, 3, 31). In more recent studies increasingly, power spectrum characteristics have been used also in dental literature and some previous studies have assessed their reliability (32–34). The assessment of the various EMG parameters in this study indicated that the power spectrum data (MF) appeared to be of value in addition to mean amplitude data (Mean; s.d.). Whilst the results of this study indicated that several issues in serial recordings were of value to be considered, it also raised questions. It is also noteworthy that until further research is available no real conclusions can be made regarding the general value of EMG assessment in diagnostics or clinical conditions. It is, however, recommended that the general protocol and standardization methods used in this study are of interest and value for further comparative studies and serial evaluations of e.g. therapeutic measures.
Conclusions 1) A task-related, between-day, comparison in asymptomatic subjects showed some variability in the postural and opening ⁄ closing tasks in comparison with intercuspal and clenching tasks which showed least significant differences in serial recordings. 2) The postural EMG signal data were the least appropriate of the tested tasks in serial assessments. Overall the results of this study assessed the reliability, repeatability and limitations of the EMG recordings for serial assessments.
Acknowledgments The authors wish to thank Alon Cohen and Tero Nordlund for their assistance in the subject recruitment and assessments. This study was supported by the Academy of Finland.
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Correspondence: Tuija I Suvinen, Department of Stomatognathic Physiology, Institute of Dentistry, University of Turku, Lemminka¨isenkatu 2, Turku, FIN-20520, Finland; Fax: c ⁄ o Annikki Vaisto +3582-3338356. Email:
[email protected]
ª 2009 The Authors. Journal compilation ª 2009 Blackwell Publishing Ltd
