Received Date: 27-Sep-2016

Accepted Article
Revised Date: 04-Feb-2017

Accepted Date: 23-Feb-2017

Article Type: Original Article

Influence of sustained submaximal clenching fatigue test on electromyographic activity and

maximum voluntary bite forces in healthy subjects and patients with temporomandibular

disorders

Running head: Jaw muscles fatigue and bite force

L . X U* , S. FAN*, B . C A I#, Z . F A N G, & X JIANG

*These authors contributed equally to this work and should be considered co-first authors. #

Correspondence: Bin Cai, Department of Rehabilitation Medicine, Shanghai Ninth People’s Hospital,

Shanghai Jiao Tong University School of Medicine, 500th. Quxi Road, Shanghai 200010, China.

E-mail: orthorehab_9th@hotmail.com

This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1111/joor.12497

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 SUMMARY This study aimed to investigate whether the fatigue induced by sustained motor task in the

jaw elevator muscles differed between healthy subjects and patients with temporomandibular disorder
Accepted Article
(TMD). Fifteen patients with TMD and thirteen age- and sex-matched healthy controls performed a

fatigue test consisting of sustained clenching contractions at 30% maximal voluntary clenching(MVC)

intensity until test failure(the criterion for terminating the fatigue test was when the biting force

decreased by 10% or more from the target force consecutively for >3 seconds). The pre- and

post-maximal bite forces (MBFs) were measured. Surface Electromyographic signals were recorded

from the superficial masseter muscles and anterior temporal muscles bilaterally, and the median

frequency at the beginning, middle, and end of the fatigue test was calculated. The duration of the

fatigue test was also quantified. Both pre- and post-MBFs were lower in TMD patients than in controls

(P < 0.01). No significant difference was found in the percentage change in MBF between groups. The

duration of the fatigue test in TMD patients was significantly shorter than that of the controls (P < 0.05).

Our results suggest that, compared to healthy subjects, TMD patients become more easily fatigued,

but the electromyographic activation process during the fatigue test is similar between healthy subjects

and TMD patients. However, the mechanisms involved in this process remain unclear and further

research is warranted.

KEYWORDS: temporomandibular disorders, muscle fatigue, bite force, surface electromyography

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 Introduction
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Masticatory muscle fatigue, pain, and weakness were frequent complaints of patients with

temporomandibular disorders (TMD) (1, 2), and have a negative impact in the patients' global quality of

life. However, the TMD-related fatigue has not been thoroughly studied and its mechanism remains

unclear. Muscle fatigue has been usually defined as a failure of the tissues to maintain the expected

force(3) or a reduction of force-producing capacity for prolonged activity (1).

In previous investigations(4, 5), bite force transducers and surface electromyography (SEMG) have

been used to analyze the masticatory muscle fatigue mechanisms in healthy and TMD subjects. In

studies employing bite force transducers, fatigue was described as in maximal bite force (MBF)(6).

While MBF is known to be lower in TMD subjects than in healthy subjects, previous studies rarely

assessed the impact of fatigue on bite force. Using a force transducer, Clark et al. (7) evaluated the

MBF immediately after the fatigue test, and found no decrease in MBF, but the changes in

electromyographic (EMG) activity are yet unknown.

The two types of characteristic changes in the EMG signal recorded from fatiguing masticatory

muscles are EMG signal amplitude increase, which is mainly caused by the recruitment of additional

motor units, and the shift of the mean power frequency toward lower frequencies, which primarily

indicates a decrease in the conduction velocity of muscle fibers (8).

During such investigations, the participants were asked to clench at sustained maximal or submaximal

force level to provoked fatigue(1, 9-13). However, a number of studies suggest that a low level of

submaximal voluntary clenching (sub-MVC) was more realistic and closely replicates activities of daily

living (ADLs) in healthy subjects (2, 14, 15). Chiarella et al. (16) showed that in healthy subjects

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 performing low-force (13kg), unilateral molar clenching, the time-related modifications in mean power

frequency decreased. Muscle fatigue is a process, rather than the state of the neuromuscular system.
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However, it remains unclear whether healthy controls and TMD subjects differ in terms of EMG signal

change over time during the low-force fatigue test.

In previous masticatory muscle fatigue studies, the end criteria of the fatigue tests varied, which

probably led to varied results(3), with reasons such as subjects could no longer produce the required

bite force (1), onset of discomfort or pain(12), and predetermined end time (3, 13). However, in some

studies evaluating limb muscles fatigue (17-19) , the end criterion was defined as the instant when the

produced force decreased by more than a certain percentage from the target force for consecutive

seconds. We propose that, by standardizing the end time of the test, the subjective measure of fatigue

becomes a standardized one and should provide a more accurate and reliable measure of the

endurance time.

Hence, in the current study, the participants were asked to perform a sub-MBF-level fatigue test, and

the criterion for terminating the fatigue test was when the biting force decreased by10% or more from

the target force consecutively for >3 seconds (18). The aim of the study was to evaluate the ability of

patients with TMD to sustain a submaximal biting task and associated EMG signal changes of the

involved muscles, and compare these measurements with age- and gender-matched healthy

participants.

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 Materials and methods
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Subject sample

Twenty-eight subjects participated in the study, with the TMD group comprising 15 subjects with TMD

(14 women and 1 man; age, 276 ± 71 years; height, 1641 ± 65 cm; weight, 546 ± 58 kg) and the

control group comprising 13 healthy subjects (11 women and 2 men; age, 286 ± 70 years; height,

1627 ± 63 cm; weight, 579 ± 90 kg).

The inclusion criteria for the TMD group were: diagnosis of a muscle-related TMD of type Ia

(myofascial pain) or Ib (myofascial pain with limited opening of the mouth ), according to the

Research Diagnostic Criteria for Temporomandibular Disorders Axis I (20), unilateral TMD, no current

TMD treatment, no current orthodontic treatment, mouth can be opened beyond 20 mm, pain duration

was >6 months, and no missing teeth.

The exclusion criteria for both groups were neurological or cognitive deficit, dental pain, or periodontal

problems.

All participants gave written informed consent, and the study was approved by the local ethics

committee at the Shanghai Jiao Tong University. If there was pain or discomfort in all procedures,

participants were free to stop their examination immediately.

Surface electromyography recording

SEMG recordings were performed using Noraxon 1400a (USA). The EMG signal sampling rate was

set at 1000 Hz, filtered through a band-pass of 10–500 Hz. SEMG signals were detected by four

disposable, self-adhesive, bipolar silver/silver chloride electrodes. Bipolar disposable surface

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 electrodes were positioned on the belly of the anterior temporal and masseter muscles (respectively)

on both the left and right sides. The belly of each muscle was determined by observing and palpating
Accepted Article
the muscle during clenching. The blocking hair was removed with a shaver to ensure satisfactory

electrode attachment for the belly anterior temporalis. The interelectrode distance was about 20 mm. A

common reference electrode was placed on earlobe of the clenching side. Before the recordings, the

skin was carefully cleaned with 70% ethyl alcohol and dried to reduce impedance.

Bite force measurement

The bite force transducer (linear range 0–1500 N; height, 8 mm) was placed in the unilateral premolar

position, which is defined as the clenching side (21, 22) (placed in the asymptomatic side of the TMD

group and in the dominant hand side of the control group). To keep the mandible balanced, the other

premolar side (the balancing side) was clenching a 10-mm-diameter cotton roll. The TMD subjects

were preferentially using their asymptomatic muscles (23), whereas healthy participants showed

higher masseter muscles EMG activity in the dominant side (11). Bite force was displayed on the

computer screen as visual feedback to the subject, allowing the subject to know their bite force values.

The transducer was calibrated with known weights before the experiments.

Experimental protocol

The participants were seated in a comfortable chair in an upright position, with head in a natural

position. After positioning the SEMG and bite force transducer on the participants, they were instructed

to read the bite force values on the computer screen as visual feedback. They were asked to practice

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 clenching before the experiments. Experiments were divided into three sections: i) pre-fatigue MVC

test, ii) fatigue test, iii) post-fatigue MVC test.

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The subjects were oriented on the entire experimental process before the experiments. After a training

phase, the participants was asked to produce MBF three times (pre-fatigue MVC tests), each

pre-fatigue MVC last 4 seconds with 5-min rest periods to avoid muscle fatigue. Verbal encouragement

was given to the subject in the various pre-fatigue MVC tests. Pre-fatigue MBF (pre-MBF) was defined

as the highest of the three pre-fatigue MVC tests. From that pre-MBF level, a 30% force level was

calculated for fatigue test target force.

Before the fatigue test, participants were asked to practice 30% pre-MBF. After a 10-min rest,

participants then performed the fatigue test at 30% pre-MBF guided by value displayed by the

computer and verbal encouragement when the force deviated more than 10% from the target force.

The fatigue test was ended when the participants could no longer hold the target bite force ( bite force

decreased >10% from the target continuously for more than 3 seconds) (16). All of the subjects’

endurance time was computed from the beginning to the end of the fatigue test.

Immediately (within a 3-second period) upon end of the fatigue test, participants were again asked to

produce MBF (post-MBF); the post-fatigue MVC test lasted 4 seconds, also with verbal

encouragement (7). The percentage change in MBF was calculated [={(pre-MBF) 

(post-MBF)}/(pre-MBF)  100].

Electromyographic signal analysis

The root mean square (RMS) values of the pre-fatigue MVC test EMG activity recordings were

calculated for further analysis. Three time periods of the fatigue test EMG recordings were selected for

the analysis, each lasting 5 seconds : the beginning 5 seconds of the fatigue test; the middle 5

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 seconds of the fatigue test; the end: the last 5 seconds of the fatigue test (16). The RMS and median

frequency were calculated in each period, and the RMS of each muscle EMG was normalized as a
Accepted Article
percentage of its RMS value during the pre-fatigue MVC test.

Statistical analysis

All statistical analyses were performed using SPSS package (version 170; IBM, Armonk, NY, USA).

The independent t test assessed general subject characteristics such as age, height, and weight. The

differences between pre-MBF and post-MBF (identical group) were examined with paired t test. The

differences in endurance time, pre-MBF, post-MBF, and percentage change in MBF between the TMD

and control groups were assessed by independent t test. A one-way analysis of variance (ANOVA) of

median frequency and normalized RMS obtained at beginning, middle and end period during fatigue

test was performed separately for each muscle, and Tukey’s post hoc tests were used to adjust for

multiple comparisons. The two-way factorial ANOVA was used to compare groups (TMD vs. control)

and sides (clenching side vs. balancing side) on median frequency and normalized RMS. Statistical

significance was set at P < 005. Data were described as mean and standard deviation.

Results

Endurance times

The endurance time was significantly longer for the control group (ranged from 78 to 166 seconds)

than for the TMD group (ranged from 29 to 116 seconds), P < 005 (Table 1).

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 Maximum bite force
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The pre-MBF was significantly higher in the control group (700 ± 147 N ) than in the TMD group (380 ±

206 N) (P < 001); the post-MBF was also significantly higher in the control group (493 ± 159 N) than in

the TMD group (223 ± 162 N) (P < 001). The MBFs were significantly decreased in the period from

before to after the fatigue test in the control group (decreased from 700 ± 147 to 493 ± 159 N, P < 001)

and the TMD group (decreased from 380 ± 206 to 223 ± 162 N, P < 001). The percentage of change in

MBF was greater in the TMD group (41 ± 20%) than in the control group (30 ± 16%), but the difference

was not statistically significant (P = 0138) (Table 1).

Surface electromyography

Normalized root mean square. ANOVA shows that only in the clenching side of the anterior temporal

muscles of the healthy controls, whose normalized RMS significantly increased at the end compared

with the beginning (P < 005, tested by Tukey’s post hoc tests). (Table 2)

The two-way factorial ANOVA indicated a significant effect (P < 005) of the group (for the masseter

muscles and anterior temporal muscles during the beginning; masseter muscles during the middle;

and anterior temporal muscles during the end of the fatigue test) and side (only for anterior temporal

muscles during the middle of the fatigue test) The TMD patients showed higher normalized RMS than

the healthy subjects (P < 005).

Median frequency. Both in the TMD patients and healthy control, ANOVA showed a significant

decrease in the median frequency for the clenching side of the masseter muscles (P < 001). In the

TMD patients, ANOVA showed a significant decrease in the median frequency for clenching side of the

masseter muscles (P < 001) and anterior temporal muscles (P < 001) and balancing side of the

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 masseter muscles (P < 001) during fatigue test (at the beginning, middle, and end). Tukey’s post hoc

tests indicated a significant difference between the beginning period and ending period in the
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clenching side of the masseter muscles and anterior temporal muscles and balancing side of the

masseter muscles. (Table 2)

The two-way factorial ANOVA indicated no significant effect of group, side, or group  side interaction

in any of the muscles.

Discussion

In this study, we used bilateral clenching with 30% MBF to induce jaw muscle fatigue and terminated

the fatigue test when bite force was decreased by 10% from the target force for more than 3

consecutive seconds. We compared the endurance times, MBF, and EMG signal characteristics of

healthy and TMD subjects. The results show that i) the endurance time was significantly shorter for

TMD subjects; ii) the MBFs before and immediately after the fatigue test were significantly higher in the

control group than in the TMD group; iii) significant decreases in MBF after fatigue test were similar for

the two groups; iv) the median frequency decreases over time in both groups, with no significant

differences between healthy and TMD subjects.

To reduce the effects of pain, discomfort, and fear on the fatigue test, we chose 30% MBF in the

current study. This force was closer to the force used during ADLs, and according to a former study

(15), the chewing force was <25 kg (33% MVC, or 245 N) during the occlusion phase and the

swallowing force was <30 kg (40% MVC, or 294 N) in healthy subjects. A similar consideration can be

found in other research (7, 16).

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 The endurance time of healthy subjects was inversely proportional to their bite force (5, 24). For similar

loads, Sforza et al. (16) reported that healthy subjects could hold a unilateral 47% MVC (127 N), which
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ended when the subjects could no longer produce the required bite force for 79–470 seconds (226 ±

142 seconds). Clark et al. (7) show that the endurance time for subjects with myofascial pain to reach

pain tolerance with a sustained 30% MVC was 24 ± 5 seconds (compared to 177 ± 23 seconds in

healthy controls). In the study of Michelotti et al. (2), healthy subjects with muscle pain induced by

glutamate injections were asked to clench at 25% MVC for 20 minutes. These various endurance times

may have been caused by differences in subjects, absolute target force levers, pain levels, end criteria

of the fatigue test, and so on.

A large number of previous studies have shown that the mean MBF values was higher in healthy

subjects (varied from 115 to 777 N) than in TMD patients (varied from 50 to 250 N) (1, 7, 10, 25-27)).

We observed a similar difference in MBF in the two groups (700 vs. 380 N) before the fatigue test. The

MBF after fatigue test similarly decreased both in healthy and TMD subjects. However, Clark et al. (7)

reported that MBF did not decrease in either healthy or myofascial pain subjects after sustained

clenching at 30% MBF; a similar observation (i.e., no decrease in MBF) was reported in healthy

subjects after sustained clenching at 25%, 50%, 75%, and 100% MBF(28). On the other hand, similar

with our observation, Svensson et al. (1) showed that the MVC determined before (777 ± 73 N) and

after (652 ± 115 N) the 10% MVC (80 N) clenching task decreased significantly in healthy subjects.

The discrepancy may be due to differences in end criteria of the fatigue test. In the studies of Clark and

colleagues (7, 28), subjects stopped clenching because of pain tolerance. In the research of Svensson

et al. (1), healthy participants were asked to sustain for 60 min, which suggests that fatigue increased

progressively over time and the sensation of fatigue was stronger than the sensation of pain during the

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 test. Thus, it could be conjectured that fatigue test at the end of the two different senses (pain or

fatigue) maybe lead to different results (no decrease or decrease). Another possibility is that patients
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with TMD have more fatigable masticatory muscles, since the TMD subjects had reduced pre-MBF,

the target bite force during the fatigue test was lower (30% pre-MBF), and the endurance time was

significantly shorter..

Our present study found that there were similar decreases in MBF after fatigue test for healthy and

TMD subjects. In a limb fatigue study, Neyroud et al. (29) observed different times to fatigue when

sustaining sub-MVC ends when 50% MVC could not be maintained for more than 3 consecutive

seconds in four different limb muscles; however, the MVC loss immediately after the end of the test

was similar for diverse muscle groups. Neyroud et al. (29) suggested that the degree of muscle fatigue

was not affected by endurance time, but rather the result of the etiology of fatigue. This opinion also

supports our research.

EMG is painless, noninvasive, and inexpensive (30), and according to previous muscle fatigue studies

(1, 8, 9), median frequency decrease was mainly due to the reduction in the conduction velocity of the

muscle fibers and RMS increase was primary to the recruitment of additional motor units. Our EMG

data were in agreement with Park et al. (9) and Maton et al. (24), who found significant decreases in

the MF and that the RMSs were highly variable across individual subjects. In our study, the normalized

RMS slightly increased, the normalized RMS of the anterior temporal muscles slightly increased over

time (beginning to end), and the masseter muscles normalized the RMS, (beginning to middle)

increasing at first and then (middle to end) decreasing. However, the change in normalized RMS was

not significant. The discrepancy between the SEMG RMS behavior of the masseter muscles and

anterior temporal muscles is potentially related to sources of activity artifacts from the epicranius (31).

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 However, we believe that the experimental setup minimized this source of errors. For that EMG

characteristic in our study, we hypothesized that masticatory muscle fatigue was primarily due to the
Accepted Article
obvious muscle fiber conduction velocity decrease, which is compensated for by the loss of tension in

some of the fatigue units through the recruitment of fresh and non-fatigued motor units rather than the

addition of more recruitment motor units (8). The TMD and healthy groups showed similar median

frequency decrease and slight RMS increase, which might be the result of the similar etiology of

fatigue of the two groups. Other hypotheses for no statistical significance in the two groups is the lack

of relationship between mean power frequency and bite force, in accordance with the observation of

Maton et al. (24) and the large standard deviation of mean values in median frequency and RMS (10).

There are some limitations in our study. First, we placed a 10-mm cotton roll on the balancing side to

minimize joint unbalance and awkward sensation resulting from unilateral biting for a long period of

time. However, the cotton roll was soft and malleable, which may have introduced additional variations

in the collected data. Second, although we asked the study participants regarding their sensation of

muscle fatigue and pain during the fatigue test, we did not quantify this information using specialized

scoring scales. Therefore, we can only judge the muscle fatigue in terms of electromyographic

activities (median frequency ), and may not quantify the level of fatigue. The third potential limitation

refers to the relatively small sample size, which may have resulted in overlooking certain associations

in the final analysis

Overall, our present findings that TMD subjects have lower MBFs and shorter endurance time indicate

a significantly reduced performance of the jaw elevator muscles and increased fatigability. On the

other hand, the electromyographic activity during the fatigue test varied in a similar manner for TMD

and healthy subjects (i.e., the median frequency decreased ), and both groups experienced a

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 significant decrease in MBF after the test, indicating the possibility that fatigue proceeds similarly in

healthy and TMD subjects. However, the mechanisms involved in this process remain unclear and
Accepted Article
further research is warranted.

Acknowledgments

This study was supported by Key Developing Disciplines Construction Program of Shanghai Municipal

Commission of Health and Family Planning(2015ZB0404). The participation of volunteers is greatly

appreciated.

Conflicts of interest

The authors have stated explicitly that there are no conflicts of interest in connection with this article.

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Accepted Article
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Table 1. Endurance time and Maximum bite force(MBF)

Endurance Change in
Pr-MBF(N) Post-MBF(N)
time(s) MBF(%)

TMD 75.9±29.3 380 ±206 223±162# 41±20

Control 100.3±26.2* 700±147** 493±159**# 30±16

Pr-MBF: Pre-fatigue Maximum bite force

Post-MBF: post- fatigue Maximum bite force

Change in MBF(%)=(pre-MBF)-(post-MBF) divided by (pre-MBF)*100

*: indicates significant difference(p<0.05) between TMD group and control group; **: indicates great

significant difference(p<0.01) between TMD group and control group

#: indicates significant difference(p<0.05) between pre-MBF and post-MBF

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 Table 2. Normalized RMS and Median Frequency of the fatigue test
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RMS(%) Median Frequency (Hz)

Muscle Time

TMD Control TMD Control

CMM beg 54.5±13.5 49.5 ±6.4 127±27 130±31

mid 59±13.6 49.8±11.2 110±26 109±32

end 57.5±18.8 47.3±13.8 88±27* 86±29*

BMM beg 53.9±15.3 47.5±13 136±23 130±32

mid 57.7±16 50.8±14 1119±25 108±3

end 56.4±18.6 51.6±20 97±31* 86±28*

CAT beg 58±16.8 49.8±5.9 128±32 131±23

mid 63.8±17 58.6±10.8 115±25 115±27

end 67.5±16.7 59.6±10.5* 98±26* 94±25*

BAT beg 52.8±12.8 42±14.9 127±31 125±29

mid 57.7±15.3 48.6±14.5 115±21 119±22

end 61.1±16.4 49.7±16.5 107±23 105±19

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 RMS: Root Mean Square; MF: Median Frequency
Accepted Article
beg: the beginning 5 seconds of the fatigue test; mid :the middle 5 seconds of the fatigue test; end: the

end 5 seconds of the fatigue test

CMM: clenching side of masseter muscles

BMM: balancing side of masseter muscles

CAT: clenching side of anterior temporal

BAT: balancing side of anterior temporal

*: indicates significant difference(p<0.05) between beg and end

This article is protected by copyright. All rights reserved.