Abstract
This study evaluated the effects of visual input on surface electromyography (sEMG) of some stomathognatic and neck muscles (anterior temporalis, masseter, anterior digastric and sternocleidomastoid muscles) in patients experiencing myogenous facial pain compared with healthy volunteers. All subjects kept the mandible at rest with teeth apart and underwent a 15-s sEMG recording of anterior temporalis, masseter, digastric and sternocleidomastoid muscles. Each recording was carried out with closed and then open eyes. The sEMG activity of each muscle was compared between the two groups. In the study group, anterior temporalis, masseter and sternocleidomastoid sEMG with closed eyes showed higher values compared with controls ( p < 0.05). In the study group, left and right anterior temporalis ( p < 0.003) and right digastric ( p < 0.03) sEMG with open eyes showed higher values than sEMG with closed eyes. In the control group no significant differences were observed between closed and open eyes. In patients with myogenous facial pain, visual input appears to be associated with a significant increase in the sEMG activity of some head and neck muscles.
Myogenous facial pain is defined as facial pain that originates from the musculoskeletal structures of the masticatory system. The pain is usually exacerbated by chewing or other jaw functions and is often accompanied, singularly or in combination, by limitation of jaw movement, muscular and fascial tenderness or joint soreness . It appears to be multifactorial, potentially involving a complex interplay of anatomic structures, biomechanical function, environmental demands and psychosocial responses, each capable of contributing to clinical manifestations and symptoms .
Myogenous facial pain is a common symptom of temporomandibular disorders (TMD). Myogenous facial pain affects several muscle parameters leading to reduction in maximal voluntary bite force, endurance time and extended recovery time .
The aetiology and pathophysiology of myogenous facial pain are not fully understood. Treatment modalities are non-specific and do not directly target the causative factors. Surface electromyography (sEMG) has been used to evaluate the muscle activity of patients suffering from myogenous facial pain. It has been suggested that the mandible elevator muscles of individuals with dental Class I pain (Angle’s classification) without myogenous facial pain signs or symptoms with the mandible at rest and in the absence of exteroceptive stimuli, showed constant sEMG values ranging from 1.4 to 2.2 μV .
It is debatable whether patients suffering from myogenous facial pain show higher rest sEMG values of the anterior temporalis, masseter, sternomastoid and digastric muscles compared with healthy people. A source of uncertainty could be that previous studies did not make clear whether individuals were recorded with their eyes open or closed; because vision plays an important role in the multisensory process of postural stabilisation.
Visual input can be used by oculomotor muscular systems and neck/trunk muscles to follow a moving object . Ocular nuclei control the eye position in the orbit; they send fibres to the nuclei that control neck and head movements and receive afferent input from vestibular nuclei. It has been observed that a modification of ocular proprioception modifies head and body posture . The role of trigeminal afferences on tonic-postural regulation has been recorded .
In this complex system, adaptive modifications can be induced by sensorial dysfunction and stimulations deriving from a discrepancy of information in contiguous systems . Information coming from well-integrated peripheral receptors may not require adaptive modifications of the system. sEMG activity could show such adaptation. With the eyes open, a significant increase in rest sEMG activity was observed in the temporal anterioris muscles . The visual input effect on the sEMG activity of the sternocleidomastoid and masseter muscles at rest has also been proved .
M onaco et al. found that in children presenting with myopic defects, the sEMG of the anterior temporalis muscle at rest increases when the eyes are open. Another study found positive correlations between the amount of mandibular laterodeviation, diottric defects, sEMG asymmetry and increased sEMG values of the anterior temporalis in the mandibular rest position with the eyes open .
It is possible that people suffering from muscular pain show less muscle tolerance and are more sensitive than normal healthy volunteers to variation of sEMG recording when visual input requires adaptive behaviour.
The purpose of this study was to determine the effects of myogenous facial pain on the sEMG activity of the head and masticatory muscles at rest and the effect of visual input on the sEMG activity of patients with myogenous facial pain at rest. This information could be of great interest to researchers because it could help to clarify the physiological behaviour of a dysfunctional stomatognathic system compared with a healthy one.
Material and methods
The study included 40 individuals divided into a study and a control group. The study group included 20 patients with myogenic craniomandibular dysfunction; 12 women and 8 men, ranging in age from 19 to 41 years (mean 30.6, SD 8.2 years; Table 1 ). The study subjects were selected from patients with myogenous facial pain from the TMD centre at the authors’ institution, who fulfilled they following inclusion criteria: absence of visual defects; natural dentition and bilateral molar support; absence of any previous orthodontic or gnathologic treatment; recent history of pain in or around the temporomandibular joint (TMJ) (preauricolar area, cheek area, parietal area, temporal area, periorbital area) according to a research diagnostic criteria (RDC) questionnaire ; presence of spontaneous muscle pain (exacerbated by meteorological changes, certain weather conditions or palpation in the cervical and masticatory muscles); self-reported teeth clenching during the day; and if difficulties were experienced when performing functional jaw movements. Patients with symptoms caused by trauma or surgery were not included.
| Study group | Control group | ||||
|---|---|---|---|---|---|
| Patients | Sex | Age | Patients | Sex | Age |
| 1 | Male | 27 | 1 | Male | 23 |
| 2 | Male | 46 | 2 | Female | 21 |
| 3 | Female | 18 | 3 | Female | 23 |
| 4 | Male | 30 | 4 | Female | 26 |
| 5 | Male | 37 | 5 | Male | 28 |
| 6 | Male | 38 | 6 | Female | 37 |
| 7 | Female | 21 | 7 | Female | 27 |
| 8 | Female | 22 | 8 | Female | 23 |
| 9 | Female | 27 | 9 | Male | 20 |
| 10 | Male | 20 | 10 | Male | 21 |
| 11 | Female | 27 | 11 | Female | 18 |
| 12 | Female | 24 | 12 | Female | 19 |
| 13 | Female | 19 | 13 | Male | 24 |
| 14 | Female | 24 | 14 | Female | 19 |
| 15 | Female | 21 | 15 | Male | 18 |
| 16 | Male | 26 | 16 | Male | 23 |
| 17 | Male | 41 | 17 | Male | 23 |
| 18 | Female | 19 | 18 | Female | 23 |
| 19 | Female | 24 | 19 | Male | 30 |
| 20 | Female | 22 | 20 | Male | 27 |
The control group included 20 healthy volunteers; 10 female and 10 male, ranging in age from 18 to 37 years (mean 27.8, SD 9.1 years). They were volunteers selected from medical and dental students and people referred to the dental department for conservative or hygiene treatment according to the following inclusion criteria: absence of visual defects; natural dentition and bilateral molar support; absence of any previous orthodontic or gnathologic treatment; no history of pain in or around the TMJ (according to RDC questionnaire ); absence of facial pain or other chronic pain condition (symptom free); and medication free.
The study was approved by the Ethics Committee of the University of L’Aquila and signed informed consent was obtained from all subjects.
At the first visit, a trained dentist clinically evaluated all subjects to confirm that they complied with the inclusion criteria. For the study subjects these were: natural dentition and bilateral molar support; absence of any previous orthodontic or gnathologic treatment; recent history of pain in or around TMJ; and presence of spontaneous muscle pain. For the control group they were: natural dentition and bilateral molar support; absence of any previous orthodontic or gnathologic treatment; no history of pain in or around the TMJ. At the second visit, a trained ophthalmologist gave each participant a complete ophthalmological and orthoptic evaluation to confirm the absence of visual defects. At the third visit, all subjects were investigated by sEMG.
Each individual was submitted to two sEMG recordings in the mandibular rest position (lips in normal soft contact, no occlusal contact), one with closed and one with open eyes. During the first recording the subjects were asked to keep their eyes closed for 5 min in a dark room to avoid visual information. 15 s of sEMG were recorded for each trial. During the second recording the subjects were asked to keep their eyes open while looking straight ahead. 15 s of sEMG were recorded for each trial. The mean of three consecutive recording epochs without movement artefacts was chosen for statistical analysis. The sEMG values were processed in amplitude domain using the root mean square (RMS) measured in microvolts.
sEMG measurement
The subjects were seated upright on a comfortable wooden chair. The head was positioned with the Frankfort plan parallel to the floor. During the first recording the room was silent and not illuminated; during the second recording the room was silent and softly illuminated.
sEMG activity was recorded (K7-Myotronics-Noromed, Inc., Kent, WA, USA) using bipolar surface electrodes at single differential with an inter-electrode distance of 2.1 cm. The surface electrodes were affixed with adhesive tape to the alcohol-treated skin, to reduce skin impedance, over the superficial areas of the right masseter (RMM), left masseter (LMM), right anterior temporalis (RTA), left anterior temporalis (LTA), right digastric (RDA) left digastric (LDA), right sternocleidomastoid (RSC) and left sternocleidomastoid (LSC) muscles. The electrodes were placed parallel to the muscle fibres of left and right homologous muscles. Eight channel surface electromyography equipment was used (Myotronics-Noromed). The signals obtained were amplified, recorded and computed using software for the clinical environment (K7-Myotronics-Noromed); RMS, expressed in microvolts, was used as amplitude indicator of the signal. Three 15 s epochs were recorded for each performance.
To avoid movement artefacts or spontaneous activity (swallowing or blinking) the sEMG epochs were evaluated on-line and recorded only if they were artefact free. The sEMG pattern of swallowing is simple to detect ; sEMG epochs presenting swallowing were detected and deleted on-line. Blinking did not affect sEMG values because the sEMG signal was pass-band (20–400 Hz) filtered. Blinking is characterized by a frequency lower than 20 Hz.
Figures 1 and 2 show the sEMG with closed (on the left) and open (on the right) eyes in one case of significant change of sEMG ( Fig. 1 ) and in one case of unchanging sEMG ( Fig. 2 ). In Fig. 2 two episodes of blinking can be discerned. Electrode position, equipment, head position and subject were not changed during the test, so the results are probably due to visual input. Figure 3 shows an episode of dry spontaneous saliva swallowing. The event is simple to detect and the operator deleted the epoch on-line . The sEMG values were examined by the same operator with no knowledge of the purpose of the recording.
Statistical analysis
A paired t -test was performed using Stata statistics package to obtain a comparison between mean and variance values of electromyography data between dependent or independent groups. Differences with a value of p < 0.05 and p < 0.005 were regarded as significant and highly significant, respectively.
The first step was to make a paired t -test for independent samples to compare the closed eyes condition between study and control group. The null hypothesis implies that for closed eyes, the study and control group show no significant difference. In this case, the closed eyes sEMGs for the control and study groups behave in a homogeneous way. The alternative hypothesis implies that closed eyes sEMGs for the study and control groups show significant difference. In this case, the two groups are different in the rest closed eyes sEMGs.
The second step was to perform a paired t -test for dependent samples to compare sEMG data, in closed and open eyes, in study and control groups separately. The null hypothesis suggests that the open eyes condition does not change the sEMG pattern of the closed eyes condition. The alternative hypothesis suggests that the open eyes condition changes the sEMG pattern compared with the closed eyes condition, implying a significant effect of visual input on sEMG data.
Results
Table 1 shows the age and sex of all participants. Comparison according to the age of the individual showed no significant differences between the groups. Table 2 gives the EMG mean values and standard deviation (in parenthesis) for the study and control groups in the closed eyes condition. The study group showed a statistically significant increase in left ( p < 0.01) and right masseter ( p < 0.03), in left ( p < 0.01) and right ( p < 0.0003) anterior temporalis and in left sternocleidomastoid ( p < 0.01) sEMG activity compared with control group. Table 3 gives the EMG results for the open eyes condition. The study group showed a statistically significant increase in left ( p < 0.01) and right ( p < 0.03) masseter, in left ( p < 0.002) and right ( p < 0.007) anterior temporalis and in left sternocleidomastoid ( p < 0.02) sEMG activity compared with the control group.
| Control group | Study group | p | |
|---|---|---|---|
| LTA | 1.43 (0.83) |
2.39 (1.64) |
0.01 * |
| RTA | 1.25 (0.63) |
2.24 (1.32) |
0.0003 ** |
| LMM | 1.04 (0.46) |
1.52 (0.95) |
0.01 * |
| RMM | 1.06 (0.45) |
1.69 (1.54) |
0.03 * |
| LSM | 1.50 (0.56) |
2.34 (1.93) |
0.01 * |
| RSM | 1.57 (0.54) |
1.63 (1.28) |
ns |
| LDA | 1.85 (0.82) |
2.00 (1.17) |
ns |
| RDA | 1.69 (0.80) |
1.96 (1.25) |
ns |
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