This study evaluated the effects of visual input on surface electromyography (sEMG) of some stomathognatic and neck muscles. In patients with myogenous facial pain, visual input appears to be associated with a decrease in muscle activity.
This study evaluated the effects of visual input on surface electromyography (sEMG) of some stomathognatic and neck muscles. In patients with myogenous facial pain, visual input appears to be associated with a decrease in muscle activity.
This study evaluated the effects of visual input on surface electromyography (sEMG) of some stomathognatic and neck muscles. In patients with myogenous facial pain, visual input appears to be associated with a decrease in muscle activity.
Effects of myogenous facial pain on muscle activity of head and neck A. Monaco, A. Spadaro, R. Cattaneo, M. Giannoni: Effects of myogenous facial pain on muscle activity of head and neck. Int. J. Oral Maxillofac. Surg. 2010; 39: 767773. #2010 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. A. Monaco 1,a , A. Spadaro 1,a , R. Cattaneo 1,a , M. Giannoni 2,3,a 1 Department of Gnatology and Prostethic Dentistry, School of Dentistry, University of LAquila, Italy; 2 Department of Odontostomatological Clinic, School of Dentistry, University of LAquila, Italy; 3 Department of Surgical Science, School of Dentistry, University of LAquila, Italy 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 signicant differences were observed between closed and open eyes. In patients with myogenous facial pain, visual input appears to be associated with a signicant increase in the sEMG activity of some head and neck muscles. Key words: myogenous facial pain; muscle activity; head; neck; facial pain. Accepted for publication 19 March 2010 Available online 2 May 2010 Myogenous facial pain is dened as facial pain that originates from the musculoske- letal structures of the masticatory system. The pain is usually exacerbated by chew- ing or other jaw functions and is often accompanied, singularly or in combina- tion, by limitation of jaw movement, mus- cular and fascial tenderness or joint soreness 20 . It appears to be multifactorial, potentially involving a complex interplay of anatomic structures, biomechanical function, environmental demands and psy- chosocial responses, each capable of con- tributing to clinical manifestations and symptoms 14 . 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 7 . The aetiology and pathophysiology of myogenous facial pain are not fully under- stood. Treatment modalities are non-spe- cic and do not directly target the causative factors. Surface electromyogra- phy (sEMG) has been used to evaluate the muscle activity of patients suffering from myogenous facial pain. It has been sug- gested that the mandible elevator muscles of individuals with dental Class I pain (Angles classication) without myogen- ous facial pain signs or symptoms 3 with the mandible at rest and in the absence of exteroceptive stimuli, showed constant sEMG values ranging from 1.4 to 2.2 mV 6,25 . It is debatable whether patients suffer- ing from myogenous facial pain show higher rest sEMG values of the anterior temporalis, masseter, sternomastoid and Int. J. Oral Maxillofac. Surg. 2010; 39: 767773 doi:10.1016/j.ijom.2010.03.025, available online at http://www.sciencedirect.com a These authors contributed equally to this work. 0901-5027/080767 +07 $36.00/0 # 2010 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. 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 32 . Ocular nuclei control the eye position in the orbit; they send bres to the nuclei that control neck and head movements and receive afferent input from vestibular nuclei. It has been observed that a modication of ocular proprioception modies head and body posture 1,3,27 . The role of trigeminal affer- ences on tonic-postural regulation has been recorded 17 . In this complex system, adaptive mod- ications can be induced by sensorial dysfunction and stimulations deriving from a discrepancy of information in con- tiguous systems 24 . Information coming from well-integrated peripheral receptors may not require adaptive modications of the system. sEMG activity could show such adaptation. With the eyes open, a signicant increase in rest sEMG activity was observed in the temporal anterioris muscles 11,19,28 . The visual input effect on the sEMG activity of the sternocleidomas- toid and masseter muscles at rest has also been proved 29 . MONACO et al. 21 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 22 . 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 adap- tive behaviour. The purpose of this study was to deter- mine 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 fullled they following inclusion cri- teria: 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 4 ; 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 difcul- ties were experienced when performing functional jaw movements. Patients with symptoms caused by trauma or surgery were not included. The control group included 20 healthy volunteers; 10 female and 10 male, ran- ging 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 4 ); absence of facial pain or other chronic pain condition (symptom free); and med- ication free. The study was approved by the Ethics Committee of the University of LAquila and signed informed consent was obtained from all subjects. At the rst visit, a trained dentist clini- cally evaluated all subjects to conrm 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 treat- ment; 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 conrmthe 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 rst 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 768 Monaco et al. Table 1. Age and sex of study and control group. 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 each trial. The mean of three consecutive recording epochs without movement arte- facts 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 oor. During the rst recording the room was silent and not illuminated; during the second recording the room was silent and softly illuminated. sEMG activity was recorded (K7-Myo- tronics-Noromed, Inc., Kent, WA, USA) using bipolar surface electrodes at single differential with an inter-electrode dis- tance of 2.1 cm. The surface electrodes were afxed with adhesive tape to the alcohol-treated skin, to reduce skin impe- dance, over the supercial areas of the right masseter (RMM), left masseter (LMM), right anterior temporalis (RTA), left anterior temporalis (LTA), right digas- tric (RDA) left digastric (LDA), right sternocleidomastoid (RSC) and left ster- nocleidomastoid (LSC) muscles. The elec- trodes were placed parallel to the muscle bres of left and right homologous mus- cles. Eight channel surface electromyo- graphy equipment was used (Myotronics-Noromed). The signals obtained were amplied, 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 per- formance. To avoid movement artefacts or spon- taneous 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 3 ; sEMG epochs present- ing swallowing were detected and deleted on-line. Blinking did not affect sEMG values because the sEMG signal was pass-band (20400 Hz) ltered. 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 signicant change of sEMG (Fig. 1) and in one case of unchan- ging 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 Effects of myogenous facial pain on muscle activity of head and neck 769 Fig. 1. Closed and open eyes sEMG for a TMD patient in the study group. Note the tonic change of anterior temporalis muscles. See text for abbreviations. The numbers on the right of the tracks represent the RMS in microvolts for each muscle. Fig. 2. Closed and open eyes sEMGfor a healthy subject in the control group. Note the unchanged tonic EMGand that blinking does not affect the anterior temporalis muscles values (LTA, left anterior temporalis, black; RTA, right anterior temporalis, red). See text for other abbreviations. The numbers on the right of the tracks represent the RMS in microvolts for each muscle. (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of the article.) the epoch on-line 2 . The sEMGvalues were examined by the same operator with no knowledge of the purpose of the record- ing. 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 depen- dent or independent groups. Differences with a value of p < 0.05 and p < 0.005 were regarded as signicant and highly signicant, respectively. The rst 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 signicant difference. In this case, the closed eyes sEMGs for the control and study groups behave in a homo- geneous way. The alternative hypothesis implies that closed eyes sEMGs for the study and control groups show signicant 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 pat- tern 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 signicant 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 sig- nicant 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 sta- tistically signicant 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 sternoclei- domastoid (p < 0.01) sEMG activity com- pared with control group. Table 3 gives the EMG results for the open eyes condition. The study group showed a statistically signicant 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. Table 4 gives the EMG values for the study group in the closed and open eye conditions. A highly signicant increase for sEMG activity in the open eye condi- tion was observed in left and right anterior temporalis (p < 0.003) and right digastric (p < 0.03). Table 5 gives the value for the control group in the closed and open eye conditions. No signicant differences were observed in the sEMG values. Discussion The purpose of this study was to determine the effects of myogenous facial pain on rest sEMG activity of head and mastica- tory muscles and the effect of visual input on rest sEMG activity in patients with myogenous facial pain. 770 Monaco et al. Fig. 3. Spontaneous dry swallowing for the TMD patient shown in Fig. 1. See text for abbreviations. The numbers on the right of the tracks represent the RMS in microvolts for each muscle. Table 3. sEMG mean values and standard deviation for study and control group in open eyes condition. Values are represented in microvolts. See text for abbreviations. Control group Study group p LTA 1.85(1.59) 3.65(1.86) 0.002 ** RTA 1.75(2.01) 3.81(1.57) 0.007 ** LMM 1.06(0.50) 1.65(1.10) 0.01 * RMM 1.03(0.45) 1.58(1.28) 0.03 * LSM 1.50(0.77) 2.71(2.68) 0.02 * RSM 1.55(0.47) 1.81(1.33) ns LDA 1.83(0.74) 1.96(1.02) ns RDA 1.72(0.76) 2.17(1.23) ns ns: non-signicant. * Signicant difference. ** Highly signicant difference. Table 2. sEMG mean values and standard deviation for study and control group in closed eyes condition. Values are represented in microvolts. See text for abbreviations. 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 ns: non-signicant. * Signicant difference. ** Highly signicant difference. Masticatory muscle activity, controlled by the trigeminal nerve, is regulated by several inputs coming from the proprio- ception of neuromuscular spindles. These inputs have an important role in mainte- nance and in modication of muscular base tone: a non-physiologic trigeminal proprioception can induce an altered mas- ticatory muscle efferent activity. There is a convergence of nociceptive and proprio- ceptive afferences in the sensorial nuclei of the trigeminal nerve 12 , including neck and C1C3 proprioception. It is possible that nociceptive stimuli, such as myogen- ous facial pain, can induce an alteration of masticatory muscle resting tone. The sig- nicant difference of LTA, RTA, LMM, RMM, LSM sEMGactivity between study and control groups with eyes closed seems to conrm this hypothesis. Proprioception messages from the neck muscles are integrated in the central ner- vous system and contribute to control balance and body orientation 10 . Centripe- tal impulses from neck proprioceptors cooperate with the labyrinth impulses to promote oculomotor muscular activity through the cervicalvestibularocular reex 9 . Some important encephalic nuclei (tri- geminal nuclei, oculomotor nuclei, vestib- ular nuclei, accessorial nerve nuclei) are integrated in the medial longitudinal fas- ciculus. Ocular proprioceptive receptors send afferent signals to trigeminal and cuneate nuclei. The anatomic and physio- logic links of these anatomical structures imply a co-ordinated integration of pro- prioceptive ocular and stomatognathic afferences. Some studies suggest that mandible elevator muscles of individuals with class I pain (according with Angles classica- tion) without TMD signs or symptoms have constant sEMG values in the man- dibular rest position and in the absence of exteroceptive stimuli 6,25 . There is heated discussion about the usefulness of sEMG in the diagnosis and study of TMD but most reviews suggest some cautions. It is generally thought that the physiological variables that have to be taken into account are age, sex, skeletal morphology and psychological factors. The authors agree with this, so to improve their data they screened the study and control group for the criteria given in the Materials and Methods section. They think that doing this could overcome the problem. There is no agreement on the actual effect of morphology on the anterior tem- poralis muscle. Some authors (specially during the 1980s) suggested some kind of relation 15,33 , but others (in the late 1990s and more recently) propose that there is no correlation 5,23,30,31 . The same argument could be made for psychological factors. There is some evi- dence about the incidence of depression and anxiety, especially cognitive symp- toms, in myogenous facial pain, but there is no clear evidence in the literature that these factors could inuence the sEMG values of stomatognathic muscles. For example, RISSE ` N et al. 26 showed no sig- nicant correlation between the psycho- physiological stress reaction and sEMG, and no association was found between sEMG activity and pain, and between negative stress rating and pain. Others have reported that patients with pain had higher anxiety, especially cognitive symp- toms, and feelings of muscle tension than did controls. These authors stated that EMG activity in the masseter regions was not signicantly different between the pain and control groups 16,18 . Many sEMG studies are concerned with functional activity, such as clenching, and few of them have studied the rest position. None of them used the present strict inclu- sive criteria, and none studied the differ- ence between the anterior temporalis sEMG in open and closed eye conditions. The present work is not concerned with the rest activity of one muscle, isometric activity during clenching or other func- tional and specic activities of the stoma- tognathic system. It tries to show through sEMG activity that changing the physio- logical status (open versus closed eyes), in some way, could be considered a non- specic stimulus requiring orientation activity. The results of sEMG activity at rest observed in the healthy group, comparing closed and open eye conditions, agree with those of HOLMGREN et al. 8 who did not nd any signicant change in resting masseter activity when visual input was varied, and disagree with the studies of MIRALLES that found a signicant decrease in sEMG values of the above mentioned muscles in the closed eye condition 19 . Different methods could explain the discrepancy between the present results and those of MIRALLES. The selection criteria in the HOLMGREN and MIRALLES studies differ from the pre- sent ones. The authors strict inclusion criteria for the control group included, among the others, a complete ophthalmol- ogist and orthoptist evaluation to conrm absence of visual defects. MIRALLES work focused on EMG activity of the sterno- cleidomastoid and masseter muscles in the supine and lateral decubitus positions. The Effects of myogenous facial pain on muscle activity of head and neck 771 Table 4. sEMG mean values and standard deviation for study group in closed and open eyes conditions. Values are represented in microvolts. See text for abbreviations. Closed eyes Open eyes p LTA 2.39(1.64) 3.65(1.86) 0.003 ** RTA 2.24(1.32) 3.81(1.57) 0.003 ** LMM 1.52(0.95) 1.65(1.10) ns RMM 1.69(1.54) 1.58(1.28) ns LSM 2.34(1.93) 2.71(2.68) ns RSM 1.63(1.28) 1.81(1.33) ns LDA 2.00(1.17) 1.96(1.02) ns RDA 1.96(1.25) 2.17(1.23) 0.03 * ns: non-signicant. * Signicant difference. ** Highly signicant difference. Table 5. sEMG mean values and standard deviation for control group in closed and open eyes conditions. Values are represented in microvolts. See text for abbreviations. Closed eyes Open eyes p LTA 1.43(0.83) 1.85(1.59) ns RTA 1.25(0.63) 1.75(2.01) ns LMM 1.40(0.46) 1.06(0.50) ns RMM 1.06(0.45) 1.03(0.45) ns LSM 1.50(0.56) 1.50(0.77) ns RSM 1.57(0.54) 1.55(0.47) ns LDA 1.85(0.82) 1.83(0.74) ns RDA 1.69(0.80) 1.72(0.76) ns ns: non-signicant. * Signicant difference. ** Highly signicant difference. present results concern the anterior tem- poralis muscle, in the upright seated posi- tion, with the head in a neutral position. One result quoted by the authors was that after 5 min in lateral decubitus in a dark room and in the rest position, the sEMG of the sternomastoid and masseter was reduced in both groups: 22 patients with myogenic cranio-cervical-mandibular dysfunction and 18 healthy subjects. MIRALLES rest position is difcult to consider as a reference point. The author concluded by saying that the signicant change in EMG activity, mainly observed at rest, suggests that the visual input effect is weak. But it is possible that after 5 min in decubitus, in a dark room, people, if they are healthy, fall asleep, resulting in this change in sEMG activity. Moreover, the change between waking and the rst sleep stage (sleep onset latency), detect- able only with a polysomnograph record, range from 3 to 15 min in the healthy. HOLMGRENs work did not compare patients with healthy controls, did not take into account visual defects, data were not consistent regarding open or closed eyes and concentrated attention on the sEMG (anterior temporalis and masseter mus- cles) effects of splint therapy. The present data, in part, conrm those of HOLMGREN, but extend the observation because what the authors have seen seems to be an effect due to myogenous facial pain and does not seem related simply to opening the eyes. MIRALLES considered open eyes the reference condition and closed eyes the test condition. On the contrary, according to WIDMALM et al. 34 , in order to avoid or signicantly reduce artefacts on the scalp muscles, the present study considered closed eyes the reference condition and open eyes the test condition. The present study showed a signicant inuence of visual input on LTA, RTA and LDA sEMG activity in the study group subjects, as previously con- rmed 21,22 . This suggests that ocular pro- prioceptive stimuli, in patients with myogenous facial pain, are an important input that could lead to tonic muscular adjustments of mandibular posture. Patients with myogenous facial pain, once their physiological adaptation mechan- isms have been overridden, represent an alarmed postural system that suffers the changes of environmental demands. The present ndings indicate that in patients with myogenous facial pain, the open eyes condition, compared with the closed eyes one, is associated with a change in the head and neck sEMG activ- ity in the mandibular rest position. 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Address: Annalisa Monaco Gnatology Clinic and Prosthetic Department University of LAquila Via Vetoio Delta 6 CAP 67100 LAquila Italy Tel: +39 0862 433837 Fax: +39 0862 433826 E-mail: annalisamonaco@yahoo.it Effects of myogenous facial pain on muscle activity of head and neck 773
Gloria Pfoltzer Theresa Morris, an Infant, by Mother and Next Friend Christopher Morris, an Infant, by Mother and Next Friend Randy Morris, an Infant, by Mother and Next Friend v. Fairfax County Department of Human Development Susan Manzo Paulette Byrd Florence Hannigan, and Louis Villafane, 966 F.2d 1443, 4th Cir. (1992)