Journal of

Oral Rehabilitation

Journal of Oral Rehabilitation 2014 41; 353--366

Isotonic resistance jaw exercise alters jaw muscle coordination during jaw movements A. WIRIANSKI*, S. DEALL*, T. WHITTLE*, M. WONG†, G. M. MURRAY* & C . C . P E C K * *Jaw Function and Orofacial Pain Research Unit, Westmead Hospital Centre for Oral Health,

Faculty of

Dentistry, University of Sydney, Professorial Unit, Level 2, Westmead, NSW, and †School of Education, Faculty of Education, Australian Catholic University, Strathfield, NSW, Australia

SUMMARY The aim was to investigate the effects of isotonic resistance exercise on the electromyographic (EMG) activity of the jaw muscles during standardised jaw movements. In 12 asymptomatic adults surface EMG activity was recorded from the anterior temporalis and masseter muscles bilaterally and the right anterior digastric muscle during right lateral jaw movements that tracked a target. Participants were randomly assigned to a Control group or an Exercise group. Jaw movement and EMG activity were collected (i) at baseline, before the exercise task (pre-exercise); (ii) immediately after the exercise task (isotonic resistance at 60% MVC against right lateral jaw movements); (iii) after 4 weeks of a home-based exercise programme; and, (iv) at 8-weeks follow-up. There were no significant within-subject or between-group differences in the velocity and amplitude of the right lateral jaw movements either within or between data collection sessions (P > 005). However, over the 8 weeks of the study, three of

Introduction Exercise is a recognised treatment modality in the management of patients with musculoskeletal pain conditions. For example, exercise has been shown to be effective for knee pain after 6 weeks (1–4) and after 4 weeks for shoulder pain (5) and lumbar pain (6). There is also evidence that exercise is effective in the management of temporomandibular disorders (TMD; 7, 8). In particular, resistance exercises have © 2014 John Wiley & Sons Ltd

the tested EMG variables (EMG Duration, Time to Peak EMG from EMG Onset, and Time to Peak EMG activity relative to Movement Onset) showed significant (P < 005) differences in the five tested muscles. Many of the significant changes occurred in the Control group, while the Exercise group tended to maintain the majority of the tested variables at pre-exercise baseline values. The data suggest a level of variability between recording sessions in the recruitment patterns of some of the muscles of mastication for the production of the same right lateral jaw movement and that isotonic resistance exercise may reduce this variability. KEYWORDS: temporomandibular muscle and joint disorders, temporomandibular joint disorders, jaw movement, masticatory muscles, electromyography, isotonic contraction, exercise therapy, home-based exercise programme, disease management, adult Accepted for publication 20 January 2014

been claimed to improve jaw function and coordination of movements (9–11), and to reduce or eliminate temporomandibular joint (TMJ) clicking (9) and reduce jaw pain and alleviate functional impairment in patients suffering from myofascial pain syndrome (12) and internal derangement of the TMJ (13). Furthermore, recent systematic reviews have reported that jaw exercises may be effective in rehabilitation programmes for the management of TMD (14–16). Although promising, these results should be viewed doi: 10.1111/joor.12153

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A . W I R I A N S K I et al. with caution. A common finding of these systematic reviews was the difficulty of drawing clear conclusions of the effectiveness of therapeutic jaw exercises due to the heterogeneity of the selected primary studies in terms of diagnosis of TMD, participant and control selection, treatment methods and outcome measures (14–16). In addition, given that the prescribed resistance exercises were often only one part of a multifaceted approach to the management of these conditions, it is therefore also difficult to determine the contribution of the prescribed exercises to symptom resolution. Another uncertainty is that the mechanisms whereby therapeutic exercises may be effective in some TMD patients are unclear. In other musculoskeletal systems however, the mechanisms appear to be clearer. For example, participants with patellofemoral joint pain have a delay in the onset of electromyographic (EMG) activity of the vastus medialis obliquus (VMO) muscle compared with the vastus lateralis (VL) muscle. Specific strengthening of the VMO muscle results in the onset of EMG activity occurring simultaneously in both the VMO and VL muscles with a concomitant reduction in symptoms (2–4). In the oro-facial region, recent studies have reported neuroplastic changes occurring after a novel tongue-protrusion training task (17, 18) and that tooth clenching training tasks can result in shortterm (19) and long-term (20) neuroplastic adaptation of the jaw motor system. These findings are promising and tend to suggest that exercise training may lead to neuroplastic adaptions in the corticomotor pathways related to the muscles of mastication. However, there is no information as to whether there are any effects of specific therapeutic exercises on jaw muscle EMG activity patterns, whether certain types of EMG changes occur with specific jaw exercise, or how long any exercise-induced EMG effects last after the exercise programme. In light of the parallels observed in the limb and trunk motor system between EMG effects and symptom improvement, there might indeed be effects of specific therapeutic exercises on jaw muscle EMG activity patterns that might be causally related to any therapeutic effects. A detailed understanding of the EMG effects of specific jaw exercises could pave the way to enhance significantly the management of TMD in an evidence-based manner, especially if specific exercises can be tailored for specific TMD symptoms. Given

the lack of information as to the effects of specific jaw exercises on jaw movement and jaw muscle EMG activity, an exploratory pilot study was carried out. The aims of this study were to test the following hypotheses: 1 That isotonic resistance exercise training results in significant changes in the EMG activity patterns of the jaw muscles of asymptomatic volunteers during a standardised jaw movement task; 2 That a home-based programme consisting of the same isotonic resistance exercises for a period of 4 weeks results in a facilitation or maintenance of these EMG changes. The data have been briefly reported in abstract form.

Materials and methods Participants Twelve asymptomatic adult volunteers (seven females, five males; aged 209–318 years) participated in this study. Participants with a past or current history of pain or dysfunction (e.g. TMD) in and around the oro-facial region were excluded. Participants provided informed consent. All procedures were approved by the Sydney West Area Health Service Human Research Ethics Committee and the Human Ethics Committee of the University of Sydney in accordance with the Helsinki Declaration of 1975, as revised in 2008 (21). Procedures related to the collection of EMG activity and jaw movement data have been described previously in detail (22–24). Each participant attended three sessions: (1) an Initial Training Session (ITS); (2) Testing Session 1 (TS1), 4 weeks after the ITS; and (3) Testing Session 2 (TS2), 8 weeks after the ITS (Fig. 1). The ITS consisted of a baseline section before the initial resistance exercise training (ITS Pre-Exercise), and a post-exercise section after the initial exercise training (ITS PostExercise, Fig. 1). EMG activity Bipolar silver–silver chloride (Ag–AgCl) surface electrodes (*) were placed bilaterally over the middle of the

*Duo-Trode, Myotronics, Seattle, WA, USA © 2014 John Wiley & Sons Ltd

JAW EXERCISES CHANGE EMG ACTIVITY

Fig. 1. Flowchart depicting the experimental design with sample sizes (n) in each group. MVC, Maximum voluntary contraction, EMG, electromyographic activity.

anterior temporalis and masseter muscles, and over the right anterior digastric, and aligned in the direction of the muscle fibres. To assist in the placement of temporalis and masseter electrodes in the same location on the skin between data collection sessions, the x and y coordinates of the centre of each electrode were measured in relation to the clinically determined Frankfort horizontal plane (FHP) which was taken as the x axis and with the origin of this coordinate system being the posterior part of the tragus. The EMG signals were amplified (2000–10 000 times) and filtered (low pass = 7 kHz; high pass = 70 Hz) by an isolated bio© 2014 John Wiley & Sons Ltd

electric amplifier (†), and digitised (‡) at 2 kHz with Spike2 data acquisition software (version 3.14; ‡). Jaw movement Right lateral jaw movement was recorded in six degrees of freedom with an optical jaw tracking system

† DB4-XB1 Fibre Optic; World Precision Instruments Inc., Sarasota, FL, USA. ‡

Micro 1401; Cambridge Electronic Design, Cambridge, England.

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A . W I R I A N S K I et al. (sampling rate 6725 Hz;§; 23). The light-emitting diodes (LEDs) of the tracking system were aligned parallel to the Frankfort horizontal and mid-sagittal planes, and attached to the mandibular and maxillary teeth with the use of cyanoacrylate adhesive in the canine region via lightweight titanium clutches custom fitted to the teeth with acrylic (**). This allowed for reproducible placement of the clutches during all sessions. The mandibular mid-incisor point (MIPT) was shown on a computer display for the participant. To standardise the right lateral jaw movements, participants tracked a computer-controlled target consisting of a linear bank of LEDs illuminated in sequence to generate a target to the side of the trajectory of the mandibular MIPT movement display. Each participant performed 5 trials of right laterotrusion. Maximum voluntary contraction All EMG data were normalised to the maximum EMG recorded for that muscle during a maximum voluntary contraction (MVC); participants received verbal encouragement from the experimenter (AW) to perform each MVC trial as hard as they could without causing pain or discomfort. For the masseter and temporalis muscles, participants clenched onto cotton rolls placed between their right and left molar teeth for three trials of 2 s. The use of cotton rolls between the molar teeth when obtaining recordings during MVC was chosen as this procedure has been reported to have low interindividual variability (25, 26) and provides a consistent level of muscle EMG activity over different data collection sessions (20). Furthermore, this technique also allows for participants to produce higher EMG values (27) possibly due to the cotton rolls stabilising the bite and reducing the influence of the occlusion morphology (28) as well as excluding any possible dental contact effects (25, 27, 29, 30) on the EMG activity. For the digastric, participants performed three trials of attempted mouth opening against resistance (at approximately 15 mm incisor separation). The MVC trial with the highest recorded EMG activity was then selected and the maximum EMG activity was calculated from the average EMG activity over a period of

025 s centred at the peak of this rectified and Butterworth filtered EMG trace. Force data were collected (sampling rate 8 Hz) with a thin pressure sensor (††) placed between the skin overlying the mandible adjacent to the canine root tip on the right side and two fingers of the right hand that applied the resistance to the jaw movement. The force data from the Flexiforce sensor was displayed for the participant. The MVC during right lateral excursion against isometric resistance was determined initially to assist in standardising the applied force during the performance of the resistance exercises. Isotonic resistance exercise training Right lateral movement was selected as it is a relatively novel jaw movement during normal daily functions of the jaw. A unilateral movement was chosen as muscles adapt to a training intervention in a taskspecific manner directly related to the training task (31). If EMG changes were to result from the application of the right-sided resistance jaw exercise task, then it would be more likely that any changes would have been more evident when performing the test movement to the right side. This would provide a comparison between muscles that were more actively involved in producing a movement vector in the tested direction and those muscles that contributed less to that movement vector. In the isotonic resistance exercise, participants performed 10 repetitions (with a 5–10 s rest between each repetition) of right lateral movement against 60% of their MVC (the training force for that participant) during the outward and return phases of right lateral movement with no hold time at their end of range position. The same thin pressure sensor as described in the MVC determination trials above was used to provide visual feedback of the applied force to the participant during each repetition of the isotonic resistance exercise task, This was the first study to test the effect of jaw exercises on the EMG activity of the muscles of mastication. As such, this heuristic study was designed to investigate whether resistance exercises of the muscles could in fact produce immediate EMG changes. If isotonic resistance

§

JAWS3D, Metropoly AG, Zurich, Switzerland

**Duralay; Reliance Dental Mfg. Co., Worth, IL, USA

††

Flexiforce; Tekscan, South Boston, MA, USA © 2014 John Wiley & Sons Ltd

JAW EXERCISES CHANGE EMG ACTIVITY exercises resulted in immediate EMG changes as measured by the selected parameters, then this would be seen in both groups of participants following completion of the isotonic resistance exercise task during ITS. On completion of the ITS, participants were randomised into an Exercise or Control group using a blinded process (Fig. 1). Participants in the Exercise group performed 10 repetitions of the isotonic resistance exercise, three times per day (morning, afternoon and evening) for 4 weeks, with each set of 10 repetitions taking approximately 5 min to complete. To assist compliance, the experimenter (AW) contacted each participant on a weekly basis. Participants in the Control group were instructed to continue with their normal activities of daily living. This would then test the effects of a 4-weeks home-based resistance exercise programme on the calculated EMG parameters (in the Exercise group) and also whether the effects of the immediate application of the resistance exercises at ITS were maintained over the first 4-weeks period (in the Control group). At the end of 4 weeks (TS1), all participants returned for data collection of the same right lateral jaw movement trials as in the ITS. To test whether the longer term effects were maintained over the second 4-weeks period of the study, at the completion of TS1, all participants were instructed to continue with their normal activities of daily living and did not perform any jaw exercises for a further 4 weeks at which time the second testing session was performed (TS2). Data analysis

baseline level. The offset of movement was the time point at which the first data point returned to the initial baseline level. The onset of EMG activity was defined as the time point at which the normalised EMG data file deviated by more than two standard deviations from the mean of the initial baseline resting level. The offset of the EMG activity was defined as the time point at which the normalised EMG data file returned to the EMG onset value as calculated above. All statistical analyses were conducted with SPSS for Windows (––). Each data set was tested with the Kolmogorov–Smirnov Test of Normality. If the data were significantly different (P < 005) from the normal distribution, median and standard error (SE) are reported and non-parametric tests were used (Mann–Whitney test, two-tailed, and Friedman test; significance accepted at P < 005). Otherwise, mean and standard deviation (SD) are reported, and an analysis of variance (ANOVA) was used with three planned contrasts that reflected the tested conditions in terms of immediate effects (i.e. significant changes following the initial application of isotonic resistance exercise during the ITS), the training effects (i.e. significant changes in variables between ITS Pre-exercise and TS1) and whether any training effects were maintained over the longer-term (i.e. significant changes between TS1 and TS2); the Bonferroni correction determined the critical P-value for statistical significance of the contrasts tested to be 00167 (i.e. 005/3).

Results Eleven participants (n = 5 for the control group, n = 6 for the exercise group) completed all three data collection sessions, ITS, TS1 and TS2 (Table 1).

Raw EMG and movement data were processed with customised programs developed with Agilent VEE Pro 6.0 (‡‡ Appendix 1). Raw EMG data were digitally rectified and Butterworth filtered (Cutoff frequency = 1 Hz, order = 3) and normalised to the maximum EMG. The coordinates of the movement of the mandibular MIPT in the lateral direction (i.e. y-direction (right is positive) of the JAWS3D system) were extracted. Figure 2 and Appendix 2 show the measured variables and the methods of calculating them. The onset of movement was defined as the time point where the first data point deviated in the positive y-direction from the initial

There were no qualitative differences in the right lateral movement traces between the four sessions (Fig. 3). There were no significant differences in mean square error between movement trials, either within subjects (Friedman test, chi-square v2F = 42, P = 0241) or between the Control group and the Exercise group across all testing sessions (Mann–Whitney test, P > 005 for all four testing sessions).

‡‡

––

Agilent Technologies, Santa Clara, CA, USA

© 2014 John Wiley & Sons Ltd

Effects of resistance exercise on right lateral jaw movement

version 15: SPSS Inc, Chicago, IL, USA

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Fig. 2. An example of a typical right lateral movement trace (top panel) and a single rectified and Butterworth-filtered EMG trace (bottom panel) as taken from one movement trial from one participant. These traces depict some of the reference points and calculated variables that were used in this study. See text for details. Three calculated variables showed significant changes following the application of isotonic resistance exercise as described in the text: EMG Duration (ED); Time to Peak EMG activity (ETPk); and, Time to Peak EMG activity relative to jaw Movement Onset (ETPm).

Effects of resistance exercise on EMG activity The maximum mean peak EMG activity (EPk) during the right lateral jaw movement trials was 170% of MVC (SD = 286) and the minimum mean EPk was 43% of MVC (SD = 32; Table 2). The EPk was 078 (43). These power analyses are supportive that the majority of the significant between-group effects occurred as a result of the isotonic resistance exercise programme. Future studies also need to investigate a patient population. Given the small sample size, it is possible that recruiting both males and females into the study may have affected the results; however, testing for the effects of gender differences was not the aim of the study. This study was a within-subject design aiming to investigate exercise effects over time. The limited sample size is a limitation of this study, and in future studies with larger sample sizes, it might be possible to tease out any possible gender differences, although previous literature suggests that there are no differences (19, 20). The training effects on the EMG activities of the masticatory muscles has previously been investigated in mixed gender samples (19, 20). Gender differences were neither reported (19) nor found (20) in either of these studies. Both these studies had components in there methodologies that were similar to the current study, for example, measurement of MVC and EMG activities from the masseter and temporal muscles. It was therefore considered appropriate to pool the data of both female and male participants.

Conclusions and clinical relevance The present findings suggest that it may be possible to retrain the human masticatory system so as to change the EMG activity of some of the muscles of mastication in the production of jaw movements. Some of the data were suggestive that isotonic resistance exercise resulted in a maintenance of pre-exercise EMG activity timing and levels that may indicate a reduction of the variability of the EMG activity over time. This reduction in variability may indicate the utilisation of a more stable motor recruitment pattern in the production of the movement task. Whether these effects are indicative of an improvement in the motor performance of the human masticatory system remains to be determined. Nonetheless, elucidating the mechanisms involved may help facilitate the development and the appropriate application of safe and relatively inexpensive rehabilitation programmes © 2014 John Wiley & Sons Ltd

JAW EXERCISES CHANGE EMG ACTIVITY to reduce the impact of TMD and return symptomatic individuals to more normal jaw function.

Acknowledgments The authors would like to thank Mr Kamal Wanigaratne, Ms Anna Forte and Mr David Armour for their assistance with data collection and technical aspects of the project.

Ethical approvals All procedures were approved by the Sydney West Area Health Service Human Research Ethics Committee and the Human Ethics Committee of the University of Sydney in accordance with the Helsinki Declaration of 1975, as revised in 2008 (21).

Source of funding This study was supported by a Grant from the Australian Dental Research Foundation (ADRF Research Grant No: 73/2006).

Conflict of interest The authors report no conflict of interests related to this study.

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Supporting Information Additional Supporting Information may be found in the online version of this article: Appendix 1. Data processing flowchart of the VEE Pro 6 Program. Appendix 2. Equations used to calculate the measured variables.

© 2014 John Wiley & Sons Ltd

Isotonic resistance jaw exercise alters jaw muscle coordination during jaw movements.

The aim was to investigate the effects of isotonic resistance exercise on the electro-myographic (EMG) activity of the jaw muscles during standardised...
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