Abstract
Background Temporomandibular disorder (TMD) development in fibromyalgia syndrome (FMS) is not yet fully understood, but altered neuromuscular control in FMS may play a role in triggering TMD.
Objective The purpose of this study was to verify the association between neuromuscular control and chronic facial pain in groups of patients with FMS and TMD.
Design A cross-sectional study was conducted.
Methods This study involved an analysis of facial pain and electromyographic activity of the masticatory muscles in patients with FMS (n=27) and TMD (n=28). All participants were evaluated according to Research Diagnostic Criteria for Temporomandibular Disorders and surface electromyography (SEMG). Myoelectric signal calculations were performed using the root mean square and median frequency of signals.
Results The data revealed premature interruption of masticatory muscle contraction in both patient groups, but a significant correlation also was found between higher median frequency values and increased facial pain. This correlation probably was related to FMS because it was not found in patients with TMD only. Facial pain and increased SEMG activity during mandibular rest also were positively correlated.
Limitations Temporal conclusions cannot be drawn from the study. Also, the study lacked a comparison group of patients with FMS without TMD as well as a control group of individuals who were healthy.
Conclusions Altered neuromuscular control in masticatory muscles may be correlated with perceived facial pain in patients with FMS.
Fibromyalgia syndrome (FMS) is characterized by widespread chronic musculoskeletal pain and specific anatomical sites painful to palpation (tender points).1,2 The syndrome appears to be linked to central neural mediation that alters sensory processing and pain perception.3–5 Other symptoms frequently associated with FMS include sleep disturbance, fatigue, morning stiffness, anxiety, and depression.6
The coexistence of fibromyalgia and myofascial pain associated with temporomandibular disorder (TMD) also has been reported in the literature,7–11 and involvement of the masticatory muscles apparently aggravates the symptoms of FMS.7,8,12 In addition, the literature on the prevalence of TMD symptoms in people with FMS reports rates ranging from 59.3% to 80.6%.8,13–15
However, we believe these are not merely coexisting conditions but that fibromyalgia may play a role in triggering TMD, given that electromyographic studies in FMS have indicated that sensitization of muscle nociceptors is revealed by abnormal patterns of reflex motor neuron activation.16
In addition, analysis of the biceps femoris muscle in people with fibromyalgia showed spinal cord hyperexcitability,17 and analysis of the biceps brachialis muscle in people with fibromyalgia showed significantly higher muscle fiber conduction velocity,18 whereas analysis of the trapezius muscle in people with FMS showed the median frequency of the signal was reached in less time than in individuals who were healthy19 (ie, a higher number of motor units were active at the beginning of the contraction). Therefore, our hypothesis is that if these changes also occur in the masticatory muscles, this finding could represent a relevant factor contributing to the development of TMD in people with FMS.
It appears that diffuse pain originating from FMS, associated with sleep disorders, may affect the performance of the masticatory muscles, leading to an imbalance in muscle function and impaired functioning of the stomatognathic system, resulting in facial pain.20,21 These centrally generated pain conditions play a role in the onset and persistence of clinically significant TMD; however, a specific mechanism to explain this relationship has not yet been identified.10,12
Electromyography is a valuable tool for investigating neuromuscular control.22 Electromyography signal amplitude and frequency spectrum can be used to characterize muscle fatigue. Premature discontinuation of muscle contraction can be determined by examining the behavior of the median frequency over time during isometric contraction.23 In addition, median frequency values represent motor unit discharge rates, and studying the pattern of recruitment of motor units in the presence of pain may help characterize muscle response. This approach may allow us to differentiate myofascial pain from fibromyalgia or could suggest hypotheses that explain TMD in people with FMS.
Therefore, the main objective of our study was to verify the association between neuromuscular control and chronic facial pain in patients with fibromyalgia and patients with TMD. The secondary objective was to characterize facial pain in patients with fibromyalgia.
Method
Study Design
A cross-sectional study was conducted in patients who were receiving treatment at the Clinicas Hospital of the University of São Paulo and at the teaching clinic of the Piracicaba Dental School from September 2009 to August 2010.
Participants
Female patients with FMS, clinically diagnosed according to the American College of Rheumatology (ACR) criteria of 19901,2 for the classification of FMS, were recruited from the Clinicas Hospital of the University of São Paulo. After screening using inclusion and exclusion criteria, these patients were examined and diagnosed using the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD)24 by a trained and qualified investigator.
The inclusion criteria for selection of the FMS group were sex (female) and the presence of TMD (myofascial pain). Exclusion criteria were the presence of systemic diseases, polyarthritis, exposure to macrofacial trauma, dislocated joints, use of orthodontic braces, dental pain, and the presence of sinusitis, ear infections, cancer, hormonal disorders, or morbid obesity (body mass index >40 kg/m2); the latter criterion was included because an increase in facial adipose tissue could attenuate the SEMG signal.
Additionally, a TMD group of female patients with facial pain only was recruited and investigated. The inclusion criteria for selection were sex (female) and the presence of TMD (myofascial pain). Exclusion criteria were the same as those applied for the FMS group plus the presence of FMS diagnosis.
Sample Size
The sample size for this study was calculated using the “Power Procedure” of the SAS System (release 9.2–TS Level 2M0, SAS Institute Inc, Cary, North Carolina), assuming a null correlation of .20, a theoretical Pearson correlation of .65, 80% power, and a .05 level of significance. After a pilot study,25 a sample size of 27 participants per group was estimated. After receiving a verbal presentation of the project, the volunteers signed an informed consent form prior to participating in the study.
Procedure
Intensity of facial pain was assessed by the visual analog scale (VAS), and pain was analyzed qualitatively based on the McGill Pain Questionnaire26,27 using the Pain Rating Index (PRI). The PRI was calculated based on the weighted means of the dimensions, as each category has a number of different subcategories and descriptors.
To further characterize the patients with FMS, an evaluation was performed to determine quality of life using the Fibromyalgia Impact Questionnaire (FIQ), validated for the Brazilian population.28 This questionnaire investigates the quality of life of patients with fibromyalgia, where the higher the score, the greater the impact of FMS on quality of life. Briefly, the questionnaire is scored based on the mean value of M1, which is the average of 7 items (questions 4–10) that have continuous measures (from 0 to 10) encompassing domains such as professional difficulties, well-being, pain, fatigue, morning stiffness, sleep disorders, anxiety, and depression. To assess quality of sleep, we used the Pittsburgh Sleep Quality Index (PSQI),29 validated for the Brazilian population.30 The PSQI provides a score of severity and nature of sleep disorders during the preceding months. The highest score is 21 points, and scores above 5 indicate that sleep quality has been compromised. The reliability and validity of these tools have been reported elsewhere.31–33
For TMD diagnosis, the RDC/TMD24 was used. Briefly, the RDC/TMD is divided into 2 axes. Axis I assesses joint movement, 20 sites of muscle palpation and the lateral pole of the temporomandibular joints (TMJs), and the posterior region of these joints, totaling 24 points of palpation. The RDC/TMD is proposed to classify subtypes of temporomandibular disorder into 3 groups: (1) muscle disorders-myofascial pain (group I), (2) disk displacement (group II), and (3) joint disorders (group III).
Axis II measures the degree of mandibular disability, depression, nonspecific physical symptoms, the presence of parafunctional habits, and the degree of interference in daily individual problems that fit into psychological and social behaviors.34 To assess oral parafunctional behavior and bruxism on RDC/TMD axis II, 2 aspects were considered: clenching and grinding.34
SEMG
The SEMG signal was recorded simultaneously by 4 electrodes attached to the skin placed in the region of the right and left temporalis and masseter muscles, following the recommendations of the International Society of Electrophysiology and Kinesiology.35 Briefly, simple active differential surface electrodes were used, composed of 2 parallel bars of pure silver, 1 mm thick and 10 mm long, with a distance of 10 mm between electrodes, a 20-fold increase (gain), an input impedance of 10 Ω,15 and a common-mode rejection ratio of 92 dB. The electrodes were connected to a MyosystemBr1-P84 (portable model) signal acquisition module (DataHominis Tecnologia Ltda, Uberlândia, Minas Gerais, Brazil). The SEMG signals were amplified 100-fold at a frequency of 2 kHz and band-pass filtered (20–1,000 Hz, Butterworth filter). The reference electrode was placed at the ulnar styloid process region and greased with gel, and the active differential electrodes were placed on the muscle bellies. Prior to attaching the electrodes, the skin was cleaned with 70% alcohol.
During the collection of the signals, the participant remained in a sitting position resting against the chair back on a Frankfurt plane parallel with the floor, eyes open, feet placed flat on the floor, and arms resting on the thighs. Three 5-second recordings of SEMG signals were collected with the mandible at rest, and three 15-second recordings were collected at maximum intercuspation (isometry), while clenching Parafilm M (Bemis Company Inc, Neenah, Wisconsin) between the premolars and molars to ensure the reliability and effectiveness of the recording.36 Data acquisition was controlled by a software program with 16-bit resolution (MyosystemBr1 software application) based on the root mean square (RMS) and the median frequency of the myoelectric signal calculations. To observe the behavior of the median frequency and RMS over time during isometric contraction, SEMG signal windows were defined using a specific software program, disregarding the first and last window of the signal, while analyzing the second, fifth, and ninth windows.
On the SEMG analysis under maximum isometric contraction, physiological muscle fatigue was evident, occurring when the median frequency shifted toward lower frequencies, which may be accompanied by an increase in the amplitude of the SEMG signal.23
The electromyographic signal was not normalized in this study because the SEMG was carried out on a single day, electrodes placed only once, and the pain reported by the participant compared with the participant's SEMG signal.37,38
Data Analysis
Calculations were performed using the SAS System, and the level of significance was set at .05. For analysis of RMS at mandibular rest, the data were subjected to an analysis of variance (ANOVA) and to Spearman correlation (R>.70=strong correlation, .70>R>.40=moderate correlation, and .40>R>.20=weak correlation).
For analysis of MNF during isometric contraction at maximal clenching, the data were subjected to an ANOVA, followed by the Tukey post hoc test. To complement the ANOVA and test the effect of windows and covariables on median frequencies, the Tukey-Kramer multiple comparison test of means was applied, maintaining a .05 level of significance. Means of the slope coefficient of the linear regression line of the electromyography signal spectrogram of the masticatory muscles were compared by applying the unpaired Student t test or Mann-Whitney U test at a .05 level of significance.
Role of the Funding Source
Financial support for the study was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Ed. #70/2009) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the 2-year postgraduate sponsorship (#2009–2010).
Results
Of the initial 82 patients, clinically diagnosed with fibromyalgia according to the ACR criteria, 41 female patients (mean age=53.2 years, SD=5.61) agreed to participate. After screening of these patients using inclusion and exclusion criteria, 31 were recruited and subsequently assessed using the RDC/TMD.24 Twenty-seven (87.1%) of these patients (FMS group) received at least one diagnosis of TMD and participated in our study (Fig. 1). Additionally, 33 female patients with facial pain were investigated, but only 28 (mean age=45 years, SD=9.53) received TMD diagnoses (Fig. 1) and agreed to participate (TMD group).
Flow diagram of participants' enrollment in the study. FMS=fibromyalgia syndrome, TMD=temporomandibular disorder, RDC/TMD=Research Diagnostic Criteria for Temporomandibular Disorders.
In the FMS group, participants had been diagnosed with FMS for a mean of 8.51 years (SD=6.19) and with facial pain for a mean of 4.23 years (SD=5.01). Facial pain was less intense than pain perceived in the rest of the body (Tab. 1). In this group, 62.9% of the volunteers were overweight or obese, and 96.3% had poor sleep patterns (PSQI>5), in addition to reporting a high impact of fibromyalgia on quality of life (Tab. 1). There was no association between poor sleep quality and facial pain. Oral parafunctional behavior such as clenching or grinding was reported by 74.1% of the participants with FMS (axis II of the RDC/TMD).
Mean (SD) Values of Body Mass Index (BMI) of Patients With Fibromyalgia Syndrome (n=27) and Scores Obtained on the Fibromyalgia Impact Questionnaire (FIQ), Pittsburgh Sleep Quality Index (PSQI), Visual Analog Scale (VAS), and Total Pain Rating Index (PRI) and Number of Words Chosen on the McGill Pain Questionnaire (MPQ)
The descriptors from the McGill Pain Questionnaire that best explained the facial pain of these patients were “throbbing,” “tiring,” and “sickening,” which accounted for 59.2% of the descriptions, followed by “nagging” and “pricking” (51.8%) (ie, a predominance of descriptors from the affective category). When asked to indicate the painful region of the face, participants with both TMD and fibromyalgia cited the temporalis muscle (85.2%). For the PRI of the McGill Pain Questionnaire, the categories that best described facial pain were “affective” and “evaluative” (eFigure). In the TMD group, oral parafunctional behavior was reported by all participants (axis II of the RDC/TMD), and facial pain measured by the VAS was a mean of 3.27 (SD=3.03).
There were no significant differences in facial pain, age, and weight in the sample (P>.05). However, participants with TMD showed a higher number of joint disorders than participants with FMS (Fig. 1).
Electromyographic Analysis
Mandibular rest.
In the FMS group, for the anterior temporalis muscles, a moderate positive correlation was found between heightened electromyographic activity (measured by the RMS parameter) and pain, whereas a weak correlation was found between the RMS at rest and pain for the masseter muscles (Fig. 2). In other words, the higher the activity of the anterior temporalis muscles at mandibular rest, the greater the facial pain. In the TMD group, a weak and not statistically significant correlation was found between the RMS and pain for the masseter muscles (R=.4088, P=.1654) and the anterior temporalis muscles (R=.3867, P=.1967).
Positive Spearman correlation between the pain reported by visual analog scale (VAS) and root mean square (RMS) at mandibular rest of the anterior temporalis muscles (R=.43806, P=.0223) and masseter muscles (R=.3414, P=.08) using for analysis the next higher value of RMS in participants with fibromyalgia syndrome (n=27). *P<.05.
Isometric contraction at maximal clenching.
We found a significant decrease in the median frequency values over time during isometric contraction of masticatory muscles in both study groups, but the coefficient of decrease (measured by slope) did not differ between the groups (Tab. 2). No significant variation was found among SEMG signal amplitudes (measured by the RMS parameter) in any of the muscles studied here during the 15-second isometric contraction. Therefore, we tested only the effects of the VAS covariable (facial pain) on the median frequency, with results showing that the higher the median frequency value for the left masseter and right anterior temporalis muscles, the higher the value reported on the VAS in the FMS group (Fig. 3). Furthermore, equations with a positive slope for median frequency and pain were found in the FMS group, whereas the opposite occurred in the TMD group (ie, a negative slope for median frequency and pain) (Fig. 4).
Mean (SD) Values of Median Frequency and Slope of the Linear Regression Line of the Electromyographic Signal of the Left Masseter (ML), Right Masseter (MR), Left Anterior Temporalis (TL), and Right Anterior Temporalis (TR) Muscles in Isometric Contraction (at Maximum Intercuspation) in the 3 Windows of the Surface Electomyography Signal of the Fibromyalgia Syndrome (FMS) Group (n=27) and the Temporomandibular Disorder (TMD) Group (n=28)a
Equations from the analysis of variance with repeated measures to test the effects of visual analog scale (VAS) covariable (facial pain) at maximal clenching on the median frequency of the isometric contraction of the left masseter muscle (y=7.1898x+b) and right anterior temporalis muscle (y=8.2928x+b) and the right masseter muscle (y=4.3372x+b) and left anterior temporalis muscle (y=5.2546x+b) in the electromyographic signal windowing in patients with fibromyalgia syndrome (n=27). *P<.05.
Equations from the analysis of variance with repeated measures to test the effects of the visual analog scale (VAS) covariable (facial pain) at maximal clenching on the median frequency of the isometric contraction of the left masseter muscle (y=−0.014x+b) and right masseter muscle (y=−0.824x+b) and the right anterior temporalis muscle (y=−25.41x+b) and left anterior temporalis muscle (y=−24.14x+b) in the electromyographic signal windowing in patients with temporomandibular disorder (n=28) (P>.05).
Discussion
The main finding of our study was that masticatory muscle fatigue occurred in both groups, reflecting the inability of both patients with TMD and patients with FMS to perform efficient muscle contractions with facial pain. However, a different pattern of muscle activation was observed in the FMS group compared with the TMD group, where electromyographic findings were correlated with facial pain.
The limitations of this study were the small number of participants and the lack of a comparison group of patients with fibromyalgia without TMD as well as a control group of individuals who were healthy, precluding comparisons with normal conditions. In addition, it remains unclear whether muscle contraction differences occurred before or after facial pain because this cross-sectional study prevented temporal conclusions from being drawn.
However, our SEMG studies showed differences in muscle recruitment among participants evaluated in the presence of facial pain, as there was a significant correlation between increase in motor unit discharge rates (higher values of median frequency) of the masticatory muscles and facial pain in the FMS group. Therefore, we suggest these are not merely coexisting comorbid conditions but that FMS may play a role in the onset of facial pain.
Because these muscles impaired by FMS could already present a condition of premature interruption of muscle contraction, contraction may have occurred, discharging the motor units at higher frequencies (tetanic contraction) in order to activate the required contraction, which is even more fatiguing, generating a cycle of muscle fatigue and pain.
The integrated pain adaptation model of Murray and Peck39 proposes that changes in muscle activity limit movement and thereby protect the sensorimotor system from further injury. With pain, a new, optimized motor unit recruitment strategy arises, leading to pain minimization in order to maintain homeostasis. In the TMD group, this strategy appeared to occur (ie, these patients' need for homeostasis is met by minimizing the generation of further pain at rest or during subsequent movement). On the other hand, in the FMS group, these patterns of recruitment were not adopted by the sensorimotor system. Perhaps there is an abnormal nociceptive response that fails to produce a protective decrease in muscle activation, even in the presence of pain. This model also proposes that under certain circumstances, if some motor units are recruited in ways they are not used to, more pain may be generated, and the pathological situation appears to occur in FMS.
Furthermore, sensitization of muscle nociceptors is revealed by abnormal patterns of reflex motor neuron activation in patients with FMS,16 and the strength and endurance of these muscle nociceptors are limited differently by nociceptive afferent feedback from exertion. Consequently, fatigue and pain occur at a lower workload in patients with FMS than in individuals who are pain-free.16,40 Muscle fatigue associated with FMS appears to be present in different muscle groups,19,22,41 including the masticatory muscles, as observed in this study, which may explain the high prevalence of TMD in people with FMS. In other words, it is possible that muscle fatigue is a predisposing factor for TMD in this patient group.
The clinical relevance of our study is the finding that a different pattern of muscle activation occurred in people with FMS, where these results may lead to new pathophysiological insights into TMD in this group of patients. We also observed that facial pain in patients with FMS was most frequently described by the affective dimension of pain perception, indicating fear of pain and activity, anxiety, and depression.31,42,43
Fibromyalgia syndrome appears to have a series of characteristics (parafunction34; muscle fatigue22; functional overload, anxiety, and stress43; sleep disorders44; allodynia and hyperalgesia4,45; and increased joint friction10) that constitute predisposing and triggering factors for TMD. Acting concomitantly, these factors could easily exceed the limit of functional adaptation to stress in the TMJ, leading to its dysfunction.
Moreover, because these factors are inherent to FMS, they also act as perpetuating factors and may increase the progression and chronicity of the dysfunction. According to Cairns,46 the physiopathology of TMD involves the association of these mechanical factors, which, when exceeding adaptive capacity, generate hypoxia, leading rapidly to the production of proinflammatory cytokines and hence to degradation of the articular cartilage. Clearly, more research is needed to unravel the relationship among muscle activation, central motor control failure, and central sensitization to pain in the clinical picture of FMS.
In conclusion, the current study demonstrated that the intensity of facial pain in people with FMS is moderate and best characterized by the affective dimension of the McGill Pain Questionnaire. The masticatory muscles present muscular fatigue in patients with TMD and FMS; however, different patterns of muscle activation are associated with pain in people with FMS. In the present study, we put forward the hypothesis that FMS can play a role in triggering TMD. It appears that the sensorimotor system fails to inhibit muscle contraction with pain in people with FMS.
The Bottom Line
What do we already know about this topic?
Myofascial pain associated with temporomandibular disorder (TMD) has been related to fibromyalgia syndrome (FMS), and fibromyalgia symptoms precede facial pain in patients with FMS. However, a specific mechanism explaining these coexisting conditions has not been identified.
What new information does this study offer?
In this article, the authors hypothesize that FMS may play a role in triggering TMD, because patients with FMS experience facial pain associated with a different surface electromyographic response. According to the results of the study, it appears that the sensorimotor system fails to inhibit muscle contraction with pain in FMS; however, it remains unclear whether muscle contraction differences occurred before or after facial pain.
If you're a patient/caregiver, what might these findings mean for you?
Fibromyalgia syndrome appears to have a series of characteristics that could constitute predisposing or triggering factors for facial pain associated with TMD in patients with FMS.
Footnotes
Professor Gui, Professor Pedroni, Dr Aquino, Dr Pimentel, Dr Reimão, Professor Berzin, and Professor Rizzatti-Barbosa provided concept/idea/research design. Professor Gui, Professor Pedroni, and Professor Rizzatti-Barbosa provided writing. Professor Gui, Dr Aquino, and Dr Pimentel provided data collection. Professor Gui, Professor Pedroni, Dr Aquino, Dr Pimentel, Dr Alves, Dr Reimão, Professor Berzin, Dr Marques, and Professor Rizzatti-Barbosa provided data analysis. Dr Rossini, Professor Berzin, and Professor Rizzatti-Barbosa provided project management. Dr Pimentel, Dr Reimão, Professor Berzin, and Professor Rizzatti-Barbosa provided study participants. Professor Berzin and Professor Rizzatti-Barbosa provided facilities/equipment. Professor Berzin and Dr Marques provided institutional liaisons. Professor Gui, Professor Pedroni, Dr Aquino, Dr Pimentel, Dr Rossini, Dr Reimão, and Professor Rizzatti-Barbosa provided consultation (including review of manuscript before submission).
This study was approved by the Ethics Committee on Research Involving Human Subjects of the Piracicaba School of Dentistry, State University of Campinas–UNICAMP, Brazil, under protocol number 103/2009. The study is registered in the International Clinical Trial Registry under identification number ACTRN12610000517077, according to the criteria established by the World Health Organization and the International Committee of Medical Journal Editors.
An abstract of the manuscript was presented at ESB2010: 17th Congress of the European Society of Biomechanics; July 4–8, 2010; Edinburgh, United Kingdom.
Financial support for the study was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Ed. #70/2009) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the 2-year postgraduate sponsorship (#2009–2010).
- Received August 28, 2012.
- Accepted April 12, 2013.
- © 2013 American Physical Therapy Association
References
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