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An investigation of the simultaneously recorded occlusal contact and surface electromyographic activity of jaw-closing muscles for patients with temporomandibular disorders and a scissors-bite relationship
Journal of Electromyography and Kinesiology 28 (2016) 114–122
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An investigation of the simultaneously recorded occlusal contact and surface electromyographic activity of jaw-closing muscles for patients with temporomandibular disorders and a scissors-bite relationship Kun Qi, Shao-Xiong Guo, YiFei Xu, Qi Deng, Lu Liu, Baoyong Li, Mei-Qing Wang ⇑ State Key Laboratory of Military Stomatology, Dept. Oral Anatomy and Physiology and TMD, School of Stomatology, Fourth Military Medical University, Xi’an, PR China
a r t i c l e
i n f o
Article history: Received 5 February 2016 Received in revised form 3 April 2016 Accepted 12 April 2016
Keywords: Scissors-bite TMD symptom Surface electromyographic activity T-scan
a b s t r a c t Surface electromyographic (SEMG) activity of the masseter and anterior temporalis (TA) muscles has been reported to be associated with occlusion and orofacial pain. However, our recent report did not reveal an association between the side of orofacial pain and the side showing higher or lower level of SEMG activity of masseter or TA. The present purpose was to re-test this association in patients who had unilateral scissors-bite relationship. Thirty-two unilateral scissors-bite femalepatients complaining of unilateral orofacial pain (n = 15) or TMJ sounds (n = 17) were enrolled to simultaneously record contacts, force distribution of occlusion, and SEMG activity of masseter and TA during centric maximal voluntary clenching (MVC). The results indicated that neither orofacial pain nor the TMJ sounds had an association with the masseter’s SEMG values, while scissors-bite had (P < 0.05). A lower SEMG value for masseter was found on the scissors-bite side where there was a smaller number of contacts and a lower biting force distribution (P < 0.05). No such association was revealed in TA. In conclusion, in patients with unilateral TMD symptom(s) and scissors-bite, the jawclosing muscles’ SEMG activity during centric MVC was associated with the scissors-bite rather than the symptoms of orofacial pain or TMJ sounds. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction Posterior scissors-bite, a transversal malocclusion, is defined as maxillary posterior teeth/tooth completely displaced from the buccal aspect, either not occluding the mandibular antagonist teeth/tooth or contact being made between the lingual surface of the maxillary lingual cusp(s) and the buccal surface of the mandibular buccal cusp(s) (Lambourne et al., 2007). Posterior scissors-bite is caused by labial eruption of the upper posterior tooth/teeth, lingual tipping of the mandibular posterior tooth/teeth or any combination of these conditions. The prevalence of scissorsbite malocclusion is approximately 1.1% in Icelandic children and 0.4–2.7% in the Icelandic adult population (Jonsson et al., 2007). Scissors-bite can cause occlusal interference by restricting lateral jaw movement and disturbing the function of the masticatory muscles. Thus, it has been suggested that scissors-bite leads to functional disorders, such as temporomandibular disorders ⇑ Corresponding author at: Department of Oral Anatomy and Physiology and TMD, School of Stomatology, Fourth Military Medical University, 145 West Changle Road, Xi’an 710032, PR China. E-mail address: [email protected] (M.-Q. Wang). http://dx.doi.org/10.1016/j.jelekin.2016.04.004 1050-6411/Ó 2016 Elsevier Ltd. All rights reserved.
(TMD) (Türp and Schindler, 2012). Tomonari et al. (2014) reported that when chewing on the scissors-bite side, the working side masseter (MM) and anterior temporalis (TA) muscles’ surface electromyographic (SEMG) activities were significantly lower than when chewing on the non-scissors-bite side. This asymmetrical muscle recruitment was suggested as a compensatory mechanism for protecting the muscle tissues against further damage and allowing for time to heal the damage (Lobbezzo et al., 2006). However, the unbalanced contractile activity of the MM and TA has been associated with TMD symptoms (Felício et al., 2012; Nielsen et al., 1990; Santana-Mora et al., 2009). The values of the maximum SEMG activity of the TA and MM were reportedly lower in patients with TMD pain than in pain-free subjects (Fogle and Glaros, 1995). Then, whether the unbalanced SEMG activity is a sign of failure of the muscular functional compensation as suggested by Santana-Mora et al. (2009), or a sign of masticatory muscular responses to occlusion, such as scissor bite, remains unclear. The T-Scan system was designed to record the distribution of tooth contacts and relative biting force. Although the T-Scan system’s 60- to 100-lm-thick sensor may produce an artifact on occlusion detection, it can be linked with SEMG activity. With this combined system, the separate diagnostic data for occlusal force
K. Qi et al. / Journal of Electromyography and Kinesiology 28 (2016) 114–122
distribution, tooth contacts and SEMG can be recorded and played back simultaneously for further analysis (Kerstein, 2004; Kerstein and Radke, 2006; Wang et al., 2013). In a recent publication (Li et al., 2016), we examined occlusal contact and SEMG activity of MM and TA simultaneously with that system. In that paper we could not find an association between the side of orofacial pain and any regular changes of the jaw-closing muscles’ SEMG activity in a group of patients with morphologically normal occlusion. It is thus necessary to investigate a group of patients with both pain and scissors-bite to clarify whether there is an altered SEMG activity of jaw-closing muscles in orofacial pain and scissors-bite patients and whether the altered SEMG activity associated with scissors-bite occlusion rather than orofacial pain. In the current study, we enrolled patients with unilateral orofacial pain and also with unilateral posterior scissors-bite. The patients with unilateral TMJ sounds and unilateral posterior scissors-bite were included as symptom controls. The purpose of our study was to detect whether the SEMG activity of the bilateral MM and TA during centric maximal voluntary clenching (MVC) was consistently higher or lower on the symptom side and/or on the scissors-bite side. The null hypothesis was no side difference of the jaw-closing muscles’ SEMG activity during centric clenching in view of either scissorsbite or TMD symptom(s).
2. Materials and methods 2.1. Subjects The study population consisted of a consecutive sample of patients with either orofacial pain or TMJ sound who visited the department of TMD and Orofacial Pain, Stomatology Hospital, the Fourth Military Medical University, Xi’an, China during the period from January 2013 to January 2015. The inclusion criteria were as follows: (1) unilateral posterior scissors-bite in at least one pair of posterior teeth; (2) chief complaint of either orofacial pain (myalgia) that had lasted for at least 1 month or TMJ sound(s); (3) complete permanent dentition except for missing third molars; and (4) Skeletal Class I and a mesofacial growth pattern (according to lateral cephalograms). The exclusion criteria were as follows: (1) an orofacial trauma history, (2) skeletal asymmetries, (3) previous or current orthodontic treatment, (4) prosthetic restorations, (5) obvious periodontal disease, and (6) the presence of neurological disturbances. Thirty-two females, with a mean age of 23.4 ± 3.04 years (range 18–28 years), satisfied all of the criteria. Fifteen of the 32 patients complained of orofacial pain, and the other 17 patients complained of TMJ sounds. In patients with orofacial pain, 6 of the patients had pain on the right side, and the other 9 patients had pain on the left side. In the patients with TMJ sounds, 6 of the patients had sounds on the right side, and the other 11 patients had sounds on the left side (Table 1). Nine of the 32 patients had scissors-bite on the left side, and the other 23 patients had scissors-bite on the right side. Two of 15 patients with orofacial pain were limited in opening their mouth; their mouth opening lengths were 28 mm and 29 mm, respectively. The orofacial pain and TMJ sounds were confirmed by patients’ complaints and by palpations performed by one of the authors (Xu). In the group of patients with myalgia, 3 of 15 patients complained of pain in the temple, and 12 patients had pain in front of the ear. The palpation of the temporalis and master muscle was performed by one of the authors (Xu) in the manner described in the RDC/TMD criteria (Dworkin and Leresche, 1992). The TMJ sounds included a clicking and/or a popping sound (without crepitus) examined by palpation by the same author (Xu). Using a visual analog scale (VAS), all patients were asked to mark one point that represented the intensity of
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self-reported pain on a non-graded straight line of 10 cm, from no pain to the worst pain imaginable (Carlsson, 1983). The mean value of the VAS for the patients in pain was 3.33 ± 0.82 cm. Each of the 32 patients signed an informed consent form, and the study was approved by the local ethical committee of the Fourth Military Medical University. 2.2. Testing task Each subject was comfortably seated with back support and feet placed flat on the floor, with their eyes directed at a mark 2 m away at eye level and their head postured with the Frankfort horizontal plane parallel to the floor. The subjects were encouraged to close their jaw as fast as possible from rest to their intercuspal position (ICP) and clench with maximal effort. The task was demonstrated and explained to each subject using dental casts. The subjects were instructed to repeat the task at least five times in front of a mirror prior to the recordings. The task was performed twice, and each recording lasted for 10 s. A two-minute rest period was allowed between each recording to avoid muscle fatigue. The total recording time was approximately 10 min. 2.3. Recordings of occlusion and SEMG The occluding features and SEMG activity of the bilateral MM and TA were recorded simultaneously using the T-Scan III occlusal analysis system (Tekscan, Inc., Boston, MA, USA) and the BioEMG III electromyographic recording system (BioPAK system, version 6.0, Bioresearch Associates, Inc., Milwaukee, WI, USA) with the aid of the T-Scan/BioPAK linking software (Tekscan, Inc./Bioresearch Associates, Inc. technology partnership), as described in a recent publication (Li et al., 2016). The analog EMG signal was amplified differentially with a fixed gain of 5000, within a peak-to-peak input range ±2000 lV, and digitized with 16-bit resolution at a 1000 Hz A/D sampling frequency. The theoretical resolution is 0.03 lV using a differential amplifier with a high common mode rejection ratio (CMRR > 130 dB at 50/60 Hz [either line frequency], input impedance 1012 X, and maximum signal to noise ratio 106 to 1) and filtered bandwidth in the frequency range of 20–500 Hz (low pass = 6 dB/octave, high pass = 12 dB/octave); an additional 20 dB band-stop for common 50/60 Hz interference was available with an intelligent software digital filter. Surface electrodes (BioFLEX; Bioresearch Associates, Inc., Milwaukee, WI, USA, 2 conductive polyester adhesive rectangular contacts of 144 square millimeters with 20 mm center-to-center spacing) were placed after cleaning the skin with 95% alcohol, according to generally accepted standards (Hellmann et al., 2012). A common electrode (38 mm by 32 mm; Bioresearch Associates, Inc., Milwaukee, WI, USA) was placed on the back of the neck as a reference. The electromyographic contractile activity was recorded simultaneously with the T-Scan III relative force data during acquisition. The T-Scan III occlusion analysis system with software version 6.0 was used to record occlusal contact locations, timings and relative biting forces. The sheet sensor (HD recording sensor, Tekscan Inc. Boston, MA, USA) was 60-lm-thick when compressed (Kerstein, 2004; Kerstein and Radke, 2006). The recordings were made in Turbo Mode, when the sensor was scanned in 0.003-s increments to maximize the timing resolution of the recorded occlusal contact data. Sensor sensitivity adjustment was performed following the operators manual before formal recording to fit the individual’s bite force level within the sensor’s responsiveness. Briefly, this was done by adjusting the number of red color-coded sensels, which represented the highest magnitude of the contact force, to be less than five (Kerstein and Radke, 2006).
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Table 1 Clinical information of the patients. Patients number
Age
Teeth with scissors-bite relation
Side with orofacial pain
Side with TMJ sound(s)
Duration of the disease (Month)
VAS value of pain
Mouth opening length (mm)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
19 21 22 26 23 20 26 28 24 22 23 28 27 20 27 18 21 22 19 26 24 28 19 22 21 25 26 23 21 27 27 24
A5/C5 A7/C7 A7/C7 A5/C5 A4/C4 A7/C7 A7/C7 A7/C7 A4/C4 A7/C7 B5/D5 B7/D7 B7/D7 B4/D4 B7/D7 A5/C5 A7/C7 A5/C5 A7/C7 A7/C7 A7/C7 A4/C4 A7/C7 A7/C7 A7/C7 A7/C7 A5/C5 A7/C7 B7/D7 B7/D7 B4/D4 B7/D7
Left Right Left Left Left Left Right Right Left Left Right Right Left Right Left / / / / / / / / / / / / / / / / /
/ / / / / / / / / / / / / / / Left Left Right Left Left Left Left Right Left Left Left Right Right Right Left Right Left
2 1 1 2 2 2 1 4 1 2 4 2 3 3 2 3 6 4 5 6 2 4 4 6 8 6 4 5 6 6 3 3
3 3 5 3 4 4 3 2 4 3 3 4 3 2 4 / / / / / / / / / / / / / / / / /
38 40 28 36 35 36 38 43 29 34 42 38 37 44 34 41 44 42 44 43 46 40 38 37 41 44 43 45 41 42 40 38
2.4. Parameters For each recording, the following parameters were provided automatically by the software of the T-Scan III system (Tekscan, Inc.) and the BioPAK Electrognathography software (Maruyama et al., 1986; Radke et al., 2014). (i) The Numbers of occlusal contacts: including red, yellow, green and blue colored sensels. The sum of all four color-coded sensels was represented as one contact number. If more than one color displayed in the same site, the contact number of this site was taken as one. (ii) The biting force spatial distribution: a percentage of the biting force in different dental sections, such as the right side or left side of the dental arch. (iii) The root-mean-square (in lV) SEMG activity. The time points selected for statistical analysis were when the relative force reached 25% and 50% of the maximal force and also the earliest time point at which maximal force was achieved; these time points were recorded as 25%-ICP, 50%-ICP and MVC-ICP, respectively. In the case that no point could be located on the graphs that matched the exact values of 25% and 50% relative force, the point closest to the corresponding value was selected. Finally, the selected minimum points were 21.6% and 46.2%, respectively, for the 25%-ICP and the 50%-ICP values; the selected maximums were 27.2% and 53.8%, accordingly, for the 25%-ICP and 50%-ICP values. 2.5. Statistical analysis Data from patients with pains and sounds were analyzed separately using the SPSS 13.0 package. Three-way analysis of the variance (ANOVA) was used to compare the influence of the following three factors on the occlusal contact number, biting force distribution and SEMG values. These three factors included (1) the biting force level, (2) the side of the scissors-bite and (3) the side with
orofacial pain or TMJ sounds. The Student–Newman–Keuls posttest was performed if significant differences between the groups were found. The level of significance was set at P < 0.05 for all statistical tests. For all of the comparisons, a = 0.05. 3. Results The time required for the biting force to increase from 25%-ICP to ICP-MVC was 2.17 ± 0.94 s. The three-way ANOVA data indicated that in both the group with pain and the group with TMJ sounds there were not any interactional effects of the three factors i.e., the biting-force level, the side of the scissors-bite and the side with TMD symptoms on the occlusal contact number, biting force distribution and the SEMG activity levels of the MM and TA. The factors of the biting force level and scissors-bite side showed an association with the occlusal contact number, the biting force distribution and the values of the SEMG activity of the MM (P < 0.05), while the factor of the symptom side, either the orofacial pain or the TMJ sounds, did not show such an association. The biting force level also showed an association with the value of the TA SEMG activity (P < 0.05), but neither the factor of scissors-bite side nor the factor of the symptom side, including orofacial pain and TMJ sound, showed any significant association (Tables 2 and 3). The occlusal contact number gradually increased in both sides as the biting force increased (P < 0.05; Fig. 1 and Tables 2–4). The contact number on the scissors-bite side was smaller than that on the non-scissors-bite side at all three biting force levels (P < 0.05; Fig. 1a and b). The non-scissors-bite side sustained a larger percentage of bite force (Fig. 2a and b). At the level of 100%-ICP, the scissors-bite side was 54.35% and non-scissors-bite side was 45.65% of the total bite force. When the biting force level increased from 25% to 50%, the activity of both the TA and MM significantly
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Table 2 P values disclosed by three-way ANOVA analysis for the association of the factors of biting-force level, scissors-bite side and/or orofacial pain side with the Tooth Contact Number and Biting Force Distribution disclosed by T-Scan System, and on the values of surface electromyographic (SEMG) of masseter (MM) and anterior temporalis (TA) during centric maximal voluntary clenching (MVC). Pain patients
Tooth contact number Biting force distribution SEMG value of TA SEMG value of MM
Force level
Scissorsbite
Orofacial pain
Interaction Force level & scissors-bite
Force level & orofacial pain
Scissors-bite & orofacial pain
Force level & scissors-bite & orofacial pain
0.000
0.001
0.415
0.957
0.905
0.810
0.905
1.000
0.000
0.056
0.995
0.244
0.910
0.985
0.038 0.038
0.264 0.017
0.985 0.998
0.819 0.984
0.877 0.930
0.815 0.442
0.787 0.708
Table 3 P values disclosed by three-way ANOVA analysis for the association of the factors of biting-force level, scissors-bite side and/or TMJ sound(s) side on with the Tooth Contact Number and Biting Force Distribution disclosed by T-Scan System, and on the values of surface electromyographic (SEMG) of masseter (MM) and anterior temporalis (TA) during centric maximal voluntary clenching (MVC). TMJ sound(s) patients
Force level
Scissors bite
TMJ sound (s)
Interaction Force level & scissors bite
Force level & TMJ sound(s)
Scissors bite & TMJ sound(s)
Tooth contact number Biting force distribution SEMG value of TA SEMG value of MM
0.000
0.000
.364
.827
.726
.496
.981
1.000
0.000
.837
.893
.402
.999
1.000
0.009 0.039
.153 0.004
.154 .527
.983 .820
.656 .927
.151 .082
.843 .599
Force level & scissors bite & TMJ sound(s)
Fig. 1. Comparison of the mean (±SD) of the Number of contacts between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
increased (P < 0.05; Figs. 3 and 4). When the force increased from 50% to 100% of the maximum, however, the SEMG activity of both the TA and MM did not show further changes (Figs. 3 and 4).
At the 100%-ICP force level, the scissors-bite side for the MM showed lower SEMG activity than that of the non-scissors-bite side (P < 0.05; Fig. 4a and b). This side difference was not found at the
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Table 4 Comparison of occlusion contact numbers at different force levels between sides. Force level
Side
Red (highest level)
Yellow (high level)
Green (middle level)
Blue (low level)
Total
25% (pain patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
0.20 0.40 0.20 0.40
0.07 0.20 0.20 0.20
3.33 3.87 3.73 3.53
0.53 0.60 0.40 0.53
4.13 5.07 4.53 4.67
25% (sound patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
0.24 0.35 0.29 0.29
0.12 0.29 0.12 0.29
3.59 4 3.88 3.71
0.53 0.94 0.71 0.76
4.59 5.59 5 5.06
50%(Pain Patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
0.40 0.53 0.47 0.47
0.53 0.93 0.93 1.07
4.00 4.73 4.53 5.00
1.73 1.53 1.20 1.00
6.66 7.72 7.13 7.54
50%(Sound Patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
0.35 0.47 0.41 0.41
0.59 0.77 0.65 0.71
4.12 4.76 4.47 4.41
0.77 0.88 0.76 0.88
5.82 6.88 6.29 6.41
100%(Pain Patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
1.00 1.60 1.20 0.60
1.00 1.20 1.33 1.67
4.47 4.27 4.67 4.33
2.00 2.27 1.67 2.33
8.47 9.34 8.87 8.93
100%(Sound Patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
1.12 1.06 1.06 1.12
1.18 1.29 1.35 1.12
4.65 5.06 4.76 4.94
2.12 2.71 2.35 2.47
9.06 10.12 9.53 9.65
Note: Biting force level is ordered as red > yellow > green > blue.
Fig. 2. Comparison of the mean (±SD) of the biting force distribution between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
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Fig. 3. Comparison of the mean (±SD) of the SEMG of TA between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels.
other two biting force levels. There were also no symptom side differences of MM activity at any biting force levels in patients with orofacial pain or patients with TMJ sounds (Fig. 4c and d).
4. Discussion The present results showed that in this group of unilateral scissors-bite patients with unilateral orofacial pain or TMJ sounds, it was the scissors-bite relation rather than the TMD symptoms that was associated with MM SEMG activity during centric MVC. Compared to the non-scissors-side, the scissors-bite side showed a lower level of MM SEMG activity together with a smaller occlusal contact number and less biting force distribution. No such an occlusion association was noticed with TA SEMG activity. Biting force during MVC is influenced by occlusion (Bakke, 2006; English et al., 2002). Using a polynomial regression model, Bakke et al. (1990) indicated that 10–20% of the variation of maximum bite force in adults was determined by occlusal contact. Scissors-bite results in a reduced occlusal contact area because of reduced intercuspation of the maxillary and mandibular teeth (Maeda et al., 2008). Thus, patients with scissors-bite have a lower level of bite force (Sonnesen et al., 2001). Biting force is ascribed to the contraction of the jaw-closing muscles. The present lower level of MM SEMG activity at the scissors-bite side during centric MVC agrees with the detected data of lower biting force and smaller contact number at the scissors-bite side. This decrease of SEMG activity was not observed in the TA which differs from what was reported by Tomonari et al. (2014) who found both TA and MM on the scissors-bite side had lower SEMG activity than on the non-scissors-bite side, but agrees with the fact that there is a functional difference between MM and TA. For example, when clenched
with unilateral occlusal support, which causes a less symmetric load of the jaw and TMJ tissues (Van der Bilt et al., 2008), the MM contributes to keep the mandible in balance by lowering its activity at the working side, while the TA more likely provides clenching power at the working side (Wang et al., 2010). In agreement with this muscle’s functional difference, a less balanced occlusion, such as the scissors-bite in the current study and posterior cross-bite in other reports (Alarcón et al., 2000; Piancino et al., 2009), has demonstrated an association with a lower level of MM SEMG activity. As for the TA, its SEMG activity was increased when the biting force increases, having least association with the contact number. In addition to biting force (Baba et al., 1996; Christensen and Rassouli, 1995; Naeije et al., 1989) and the number of occlusal contacts (Kerstein, 2004; Ferrario et al., 2002), the SEMG activity of jaw-closing muscles during clenching is also influenced by many other factors, such as jaw position (Baba et al., 2000) and the contact locations (Bakke, 1993). Thus, the SEMG activity is an outcome of the summation of many factors. Some subsets of SEMG activity are responsible for stabilizing the mandibular bone during clenching (Wang et al., 2013). Our previous report indicated that in healthy subjects, when the number of the occlusal contacts increased to the MVC level, the requirement for moving the mandible to a stable condition is reduced, leading to a decrease in the MM SEMG activity at the MVC level compared to that at 50% of the MVC level (Wang et al., 2013). However, in the present scissors-bite orofacial pain patients, this decrease in MM SEMG activity was not observed, implying a functional increase of this muscle in these patients. Moreover, the MM SEMG activity from 25%-ICP to 50%-ICP in healthy individuals showed no difference (Wang et al., 2013), while this activity value was increased in patients. Specifically, the patients with an unstable scissors-bite
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Fig. 4. Comparison of the mean (±SD) of the SEMG of MM between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
relation tended to perform a modified MVC, possibly to prevent potential harm; It took 2.17 ± 0.94 s from 25% to MVC when the patients were required to perform a fast close, while healthy individuals took 1.55 ± 0.84 s to complete this movement (Wang et al., 2013). Orofacial pain and TMJ sounds are two of the most common signs of TMD. Nowdays, there remains no consensus on the association of TMD and the jaw muscles’ EMG activity. Nielsen et al. (1990) reported that there were no significant differences of MM SEMG values during clenching between TMD patients and healthy controls. However, pain and sounds may have different effects on the masticatory muscles. Santana-Mora et al. (2009) reported that the MM SEMG activity of patients with unilateral TMD pain symptoms for over 6 months (VAS: 4.76 ± 1.70) was lower on the pain side than on the pain-free side. In addition, Liu et al. (1989) stated that TMJ sounds were related to the function of the lateral pterygoid muscles, but less related to the SEMG activity of the MM and TA in centric clenching. However, no occlusion details were provided in these reports, and the differences in patient homogenization and study methodology make precise comparison between reports impossible. The inclusion criteria for the present study were carefully implemented by choosing patients with not only unilateral symptoms, pains or sounds but also with unilateral scissor-bite relations. In this way, we were able to compare the side differences and to disclose the association of SEMG activity of the jaw-closing muscles with occlusion and/or symptoms. Our results indicate that not only did the sound side show no association with the jaw-closing muscles’ SEMG activity, as was reported (Liu et al., 1989), but also that the pain side showed no such association, which is in agreement with our recent report (Li et al.,
2016). In considering the present results, the number of subjects was too small to be a reflection of a specific population. Furthermore, there could have been an effect from the T-Scan sensor that was inserted between the dentitions, although it was only 60–100 lm in thickness (Kerstein, 2004; Kerstein and Radke, 2006). Indeed, a previous study on interocclusal thickness discrimination showed that aluminum foil as thin as 20 lm could impact the bite-disturbing proprioceptive information for a subject (Kampe et al., 1987). Thus, the data from this type of instrument only provide a general idea of the occlusal contacts. Overall, the present data from a small number of subjects indicate, in patients with unilateral TMD symptom(s) and scissors-bite, that the jaw-closing muscles’ SEMG activity during centric MVC was more associated with the scissors-bite rather than the symptoms of orofacial pain or TMJ sounds. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgments The study was supported by the National Nature Science Foundation of China (NSFC) No. 81470762. Thanks to John Radke, Chairman of BioResearch Associates, Inc., for his advice regarding the using of the software and analyzing program, and also a proof reading. The statistics assistance of Lin Sun was gratefully acknowledged. The participation of patients was greatly appreciated.
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References Alarcón, J.A., Martín, C., Palma, J.C., 2000. Effect of unilateral posterior crossbite on the electromyographic activity of human masticatory muscles. Am. J. Orthod. Dentofac. Orthop. 118 (3), 328–334. Baba, K., Ai, M., Mizutani, H., Enosawa, S., 1996. Influence of experimental occlusal discrepancy on masticatory muscle activity during clenching. J. Oral Rehabil. 23 (1), 55–60. Baba, K., Yugami, K., Akishige, S., Ai, M., 2000. Immediate effect of occlusal contact pattern in lateral jaw position on the EMG activity in jaw-elevator muscles in humans. Int. J. Prosthodont. 13 (6), 500–505. Bakke, M., 1993. Mandibular elevator muscles: physiology, action, and effect of dental occlusion. Scand. J. Dent. Res. 101 (5), 314–331. Bakke, M., 2006. Bite force and occlusion. Semin. Orthod. 12 (2), 120–126. Bakke, M., Holm, B., Jensen, B.L., Lars, M., Eigild, M., 1990. Unilateral, isometric bite force in 8–68-year-old women and men related to occlusal factors. Scand. J. Dent. Res. 98 (2), 149–158. Carlsson, A.M., 1983. Assessment of chronic pain. I. Aspects of the reliability and validity of the visual analogue scale. Pain 16 (1), 87–101. Christensen, L.V., Rassouli, N.M., 1995. Experimental occlusal interferences. Part II. Masseteric EMG responses to an intercuspal interference. J. Oral Rehabil. 22 (7), 521–531. Dworkin, S.F., Leresche, L., 1992. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J. Craniomandib. Disord. 6 (4), 301–355. English, J.D., Buschang, P.H., Throckmorton, G.S., 2002. Does malocclusion affect masticatory performance? Angle Orthod. 72 (1), 21–27. Felício, C.M.D., Ferreira, C.L.P., Medeiros, A.P.M., Tartaglia, G.M., Sforza, C., 2012. Electromyographic indices, orofacial myofunctional status and temporomandibular disorders severity: a correlation study. J. Electromyogr. Kinesiol. 22 (2), 266–272. Ferrario, V.F., Serrao, G., Dellavia, C., Caruso, E., Sforza, C., 2002. Relationship between the number of occlusal contacts and masticatory muscle activity in healthy young adults. Cranio 20 (20), 91–98. Fogle, L.L., Glaros, A.G., 1995. Contributions of facial morphology, age, and gender to EMG activity under biting and resting conditions: a canonical correlation analysis. J. Dent. Res. 74 (8), 1496–1500. Hellmann, D., Giannakopoulos, N.N., Schmitter, M., Lenz, J., Schindler, H.J., 2012. Anterior and posterior neck muscle activation during a variety of biting tasks. Eur. J. Oral Sci. 120 (4), 326–334. Jonsson, T., Arnlaugsson, S., Karlsson, K.O., 2007. Orthodontic treatment experience and prevalence of malocclusion traits in an Icelandic adult population. Am. J. Orthod. Dentofac. Orthop. 131 (1), 8.e11–8.e18. Kampe, T., Haraldson, T., Hannerz, H., Carlsson, G.E., 1987. Occlusal perception and bite force in young subjects with and without dental fillings. Acta Odontol. Scand. 45 (2), 101–107. Kerstein, R.B., 2004. Combining technologies: a computerized occlusal analysis system synchronized with a computerized electromyography system. Cranio 22 (2), 96–109. Kerstein, R.B., Radke, J., 2006. The effect of disclusion time reduction on maximal clench muscle activity levels. Cranio 24 (3), 156–165. Lambourne, C., Lampasso, J., William, C., Buchanan, J., Dunford, R., Mccall, W., 2007. Malocclusion as a risk factor in the etiology of headaches in children and adolescents. Am. J. Orthod. Dentofac. Orthop. 132 (6), 754–761. Li, B.Y., Zhou, L.J., Guo, S.X., Zhang, Y., Lu, L., Wang, M.Q., 2016. An investigation on the simultaneously recorded occlusion contact and surface electromyographic activity for patients with unilateral temporomandibular disorders pain. J. Electromyogr. Kinesiol. 28, 199–207. Liu, Z.J., Wang, H.Y., Pu, W.Y., 1989. A comparative electromyographic study of the lateral pterygoid muscle and arthrography in patients with temporomandibular joint disturbance syndrome sounds. J. Prosthet. Dent. 62 (2), 229–233. Lobbezzo, F., van Selms, M.K.A., Naeije, M., 2006. Masticatory muscle pain and disordered jaw motor behaviour: literature review over the past decade. Arch. Oral Biol. 51 (9), 713–720. Maeda, A., Soejima, K., Ogura, M., Ohmure, H., Sugihara, K., Miyawaki, S., 2008. Orthodontic treatment combined with mandibular distraction osteogenesis and changes in stomatognathic function. Angle Orthod. 78 (6), 1125–1132. Maruyama, T., Kuwabara, T., Mizumori, T., Miyauchi, S., Kuroda, T., 1986. The effect of TMJ abnormalities on chewing movements. J. Osaka Univ. Dent. Sch. 25, 63–77. Naeije, M., McCarroll, R.S., Weijs, W.A., 1989. Electromyographic activity of the human masticatory muscles during submaximal clenching in the intercuspal position. J. Oral Rehabil. 16 (1), 63–70. Nielsen, I.L., McNeill, C., Danzig, W., Goldman, S., Levy, J., Miller, A.J., 1990. Adaptation of craniofacial muscles in subjects with craniomandibular disorders. Am. J. Orthod. Dentofac. Orthop. 97 (1), 20–34. Piancino, M.G., Farina, D., Talpone, F., Merlo, A., Bracco, P., 2009. Muscular activation during reverse and non-reverse chewing cycles in unilateral posterior crossbite. Eur. J. Oral Sci. 117 (2), 122–128. Radke, J.C., Kull, R.S., Sethi, M.S., 2014. Chewing movements altered in the presence of temporomandibular joint internal derangements. Cranio 32 (3), 187–192. Santana-Mora, U., Cudeiro, J., Mora-Bermúdez, M.J., 2009. Changes in EMG activity during clenching in chronic pain patients with unilateral temporomandibular disorders. J. Electromyogr. Kinesiol. 19 (6), e543–e549. Sonnesen, L., Bakke, M., Solow, B., 2001. Bite force in pre-orthodontic children with unilateral crossbite. Eur. J. Orthod. 23 (6), 741–749.
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Tomonari, H., Kubota, T., Yagi, T., Kuninori, T., Kitashima, F., Uehara, S., Miyamaki, S., 2014. Posterior scissors-bite: masticatory jaw movement and muscle activity. J. Oral Rehabil. 41 (4), 257–265. Türp, J.C., Schindler, H., 2012. The dental occlusion as a suspected cause for TMDs: epidemiological and etiological considerations. J. Oral Rehabil. 39 (7), 502–512. Van der Bilt, A., Tekamp, A., Van der Glas, H., Abbink, J., 2008. Bite force and electromyography during maximum unilateral and bilateral clenching. Eur. J. Oral Sci. 116 (3), 217–222. Wang, M.Q., He, J.J., Zhang, J.H., Wang, K., Svensson, P., Widmalm, S.E., 2010. SEMG activity of jaw-closing muscles during biting with different unilateral occlusal supports. J. Oral Rehabil. 37 (9), 719–725. Wang, X.R., Zhang, Y., Xu, Y.F., Wang, M.Q., 2013. Stable tooth contacts in intercuspal occlusion makes for utilities of the jaw elevators during maximal voluntary clenching. J. Oral Rehabil. 40 (5), 319–328.
Kun Qi received the B.S. (2005) and the M.S. degree (2008) in Medical Science from the Xi’an Jiaotong University. He is currently attending to his Ph.D. in Oral Anatomy and Physiology at the Fourth Military Medical University. His clinical and research interests are correlations between occlusion and temporomandibular disorders.
Shaoxiong Guo received the B.S. (2012) in Medical Science from Xi’an Medical University and the M.S. degree (2015) in the Fourth Military Medical University. He is currently attending to his Ph.D. in Oral Anatomy and Physiology at the Fourth Military Medical University. He has focused significant part of his research activity on the correlations between the masticatory system and cervical system and evidence-based dentistry.
YiFei Xu received the B.S. (2007) and the M.S. degree (2010) in Medical Science from the Xi’an Jiaotong University. She is currently Attending Dentist in Oral Anatomy and Physiology at the Fourth Military Medical University. Her clinical and research interests are correlations between othodontics and temporomandibular disorders.
Qi Deng received the B.S. (2012) and she is a clinical research member and physical therapist in the Fourth Military Medical University. She has cured about 300 oral-facial pain patients. Her clinical and research interests are health care of Temporomandibular Disorders and SEMG of masticatory muscle.
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K. Qi et al. / Journal of Electromyography and Kinesiology 28 (2016) 114–122 Lu Liu received the B.S. (2013) and she is a clinical research member and physical therapist in the Fourth Military Medical University. She has cured about 400 oral-facial pain patients. Her clinical and research interests are health care of Temporomandibular Disorders and laser therapy of masticatory muscle disorder.
Baoyong Li received the B.S. (2003) and the M.S. degree (2007) in Medical Science from the Fourth Military Medical University. He is currently attending to his Ph. D. in Oral Anatomy and Physiology at the Fourth Military Medical University. His clinical and research interests are correlations between occlusion and temporomandibular disorders.
Dr. Meiqing Wang is the Chief Professor in Dept. Oral Anatomy and Physiology and TMJ, College of Stomatology, Fourth Military Medical University. She is an occlusionist and specialist in Temporomandibular Disorders (TMD). She treats over 30 TMD patients per week from 1997. She have published more than 200 papers, including over 40 English papers to expression her scientific view point that occlusion takes a role in TMD. She has also edited and published 4 books in Chinese on Oral Anatomy and Physiology and Occlusion. She has supervised more than 50 postgraduate students. She has won the awards of Education Progress in Military (1997), the Science and Technology Progress in Military (Second Class, 2003) and in Shanxi Province (First Class, 2005). She was honoured as the Excellent Teacher of Chinese Military Schools (1998, 2006 and 2010). She is now the vice president of the Society of TMD and Occlusion and the president of Occlusion Branch, Chinese Stomatological Association (CSA). She is now the editorial board member of J Bone Mineral Res, J Oral Rehabil and CRANIO.
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Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
An investigation of the simultaneously recorded occlusal contact and surface electromyographic activity of jaw-closing muscles for patients with temporomandibular disorders and a scissors-bite relationship Kun Qi, Shao-Xiong Guo, YiFei Xu, Qi Deng, Lu Liu, Baoyong Li, Mei-Qing Wang ⇑ State Key Laboratory of Military Stomatology, Dept. Oral Anatomy and Physiology and TMD, School of Stomatology, Fourth Military Medical University, Xi’an, PR China
a r t i c l e
i n f o
Article history: Received 5 February 2016 Received in revised form 3 April 2016 Accepted 12 April 2016
Keywords: Scissors-bite TMD symptom Surface electromyographic activity T-scan
a b s t r a c t Surface electromyographic (SEMG) activity of the masseter and anterior temporalis (TA) muscles has been reported to be associated with occlusion and orofacial pain. However, our recent report did not reveal an association between the side of orofacial pain and the side showing higher or lower level of SEMG activity of masseter or TA. The present purpose was to re-test this association in patients who had unilateral scissors-bite relationship. Thirty-two unilateral scissors-bite femalepatients complaining of unilateral orofacial pain (n = 15) or TMJ sounds (n = 17) were enrolled to simultaneously record contacts, force distribution of occlusion, and SEMG activity of masseter and TA during centric maximal voluntary clenching (MVC). The results indicated that neither orofacial pain nor the TMJ sounds had an association with the masseter’s SEMG values, while scissors-bite had (P < 0.05). A lower SEMG value for masseter was found on the scissors-bite side where there was a smaller number of contacts and a lower biting force distribution (P < 0.05). No such association was revealed in TA. In conclusion, in patients with unilateral TMD symptom(s) and scissors-bite, the jawclosing muscles’ SEMG activity during centric MVC was associated with the scissors-bite rather than the symptoms of orofacial pain or TMJ sounds. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction Posterior scissors-bite, a transversal malocclusion, is defined as maxillary posterior teeth/tooth completely displaced from the buccal aspect, either not occluding the mandibular antagonist teeth/tooth or contact being made between the lingual surface of the maxillary lingual cusp(s) and the buccal surface of the mandibular buccal cusp(s) (Lambourne et al., 2007). Posterior scissors-bite is caused by labial eruption of the upper posterior tooth/teeth, lingual tipping of the mandibular posterior tooth/teeth or any combination of these conditions. The prevalence of scissorsbite malocclusion is approximately 1.1% in Icelandic children and 0.4–2.7% in the Icelandic adult population (Jonsson et al., 2007). Scissors-bite can cause occlusal interference by restricting lateral jaw movement and disturbing the function of the masticatory muscles. Thus, it has been suggested that scissors-bite leads to functional disorders, such as temporomandibular disorders ⇑ Corresponding author at: Department of Oral Anatomy and Physiology and TMD, School of Stomatology, Fourth Military Medical University, 145 West Changle Road, Xi’an 710032, PR China. E-mail address: [email protected] (M.-Q. Wang). http://dx.doi.org/10.1016/j.jelekin.2016.04.004 1050-6411/Ó 2016 Elsevier Ltd. All rights reserved.
(TMD) (Türp and Schindler, 2012). Tomonari et al. (2014) reported that when chewing on the scissors-bite side, the working side masseter (MM) and anterior temporalis (TA) muscles’ surface electromyographic (SEMG) activities were significantly lower than when chewing on the non-scissors-bite side. This asymmetrical muscle recruitment was suggested as a compensatory mechanism for protecting the muscle tissues against further damage and allowing for time to heal the damage (Lobbezzo et al., 2006). However, the unbalanced contractile activity of the MM and TA has been associated with TMD symptoms (Felício et al., 2012; Nielsen et al., 1990; Santana-Mora et al., 2009). The values of the maximum SEMG activity of the TA and MM were reportedly lower in patients with TMD pain than in pain-free subjects (Fogle and Glaros, 1995). Then, whether the unbalanced SEMG activity is a sign of failure of the muscular functional compensation as suggested by Santana-Mora et al. (2009), or a sign of masticatory muscular responses to occlusion, such as scissor bite, remains unclear. The T-Scan system was designed to record the distribution of tooth contacts and relative biting force. Although the T-Scan system’s 60- to 100-lm-thick sensor may produce an artifact on occlusion detection, it can be linked with SEMG activity. With this combined system, the separate diagnostic data for occlusal force
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distribution, tooth contacts and SEMG can be recorded and played back simultaneously for further analysis (Kerstein, 2004; Kerstein and Radke, 2006; Wang et al., 2013). In a recent publication (Li et al., 2016), we examined occlusal contact and SEMG activity of MM and TA simultaneously with that system. In that paper we could not find an association between the side of orofacial pain and any regular changes of the jaw-closing muscles’ SEMG activity in a group of patients with morphologically normal occlusion. It is thus necessary to investigate a group of patients with both pain and scissors-bite to clarify whether there is an altered SEMG activity of jaw-closing muscles in orofacial pain and scissors-bite patients and whether the altered SEMG activity associated with scissors-bite occlusion rather than orofacial pain. In the current study, we enrolled patients with unilateral orofacial pain and also with unilateral posterior scissors-bite. The patients with unilateral TMJ sounds and unilateral posterior scissors-bite were included as symptom controls. The purpose of our study was to detect whether the SEMG activity of the bilateral MM and TA during centric maximal voluntary clenching (MVC) was consistently higher or lower on the symptom side and/or on the scissors-bite side. The null hypothesis was no side difference of the jaw-closing muscles’ SEMG activity during centric clenching in view of either scissorsbite or TMD symptom(s).
2. Materials and methods 2.1. Subjects The study population consisted of a consecutive sample of patients with either orofacial pain or TMJ sound who visited the department of TMD and Orofacial Pain, Stomatology Hospital, the Fourth Military Medical University, Xi’an, China during the period from January 2013 to January 2015. The inclusion criteria were as follows: (1) unilateral posterior scissors-bite in at least one pair of posterior teeth; (2) chief complaint of either orofacial pain (myalgia) that had lasted for at least 1 month or TMJ sound(s); (3) complete permanent dentition except for missing third molars; and (4) Skeletal Class I and a mesofacial growth pattern (according to lateral cephalograms). The exclusion criteria were as follows: (1) an orofacial trauma history, (2) skeletal asymmetries, (3) previous or current orthodontic treatment, (4) prosthetic restorations, (5) obvious periodontal disease, and (6) the presence of neurological disturbances. Thirty-two females, with a mean age of 23.4 ± 3.04 years (range 18–28 years), satisfied all of the criteria. Fifteen of the 32 patients complained of orofacial pain, and the other 17 patients complained of TMJ sounds. In patients with orofacial pain, 6 of the patients had pain on the right side, and the other 9 patients had pain on the left side. In the patients with TMJ sounds, 6 of the patients had sounds on the right side, and the other 11 patients had sounds on the left side (Table 1). Nine of the 32 patients had scissors-bite on the left side, and the other 23 patients had scissors-bite on the right side. Two of 15 patients with orofacial pain were limited in opening their mouth; their mouth opening lengths were 28 mm and 29 mm, respectively. The orofacial pain and TMJ sounds were confirmed by patients’ complaints and by palpations performed by one of the authors (Xu). In the group of patients with myalgia, 3 of 15 patients complained of pain in the temple, and 12 patients had pain in front of the ear. The palpation of the temporalis and master muscle was performed by one of the authors (Xu) in the manner described in the RDC/TMD criteria (Dworkin and Leresche, 1992). The TMJ sounds included a clicking and/or a popping sound (without crepitus) examined by palpation by the same author (Xu). Using a visual analog scale (VAS), all patients were asked to mark one point that represented the intensity of
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self-reported pain on a non-graded straight line of 10 cm, from no pain to the worst pain imaginable (Carlsson, 1983). The mean value of the VAS for the patients in pain was 3.33 ± 0.82 cm. Each of the 32 patients signed an informed consent form, and the study was approved by the local ethical committee of the Fourth Military Medical University. 2.2. Testing task Each subject was comfortably seated with back support and feet placed flat on the floor, with their eyes directed at a mark 2 m away at eye level and their head postured with the Frankfort horizontal plane parallel to the floor. The subjects were encouraged to close their jaw as fast as possible from rest to their intercuspal position (ICP) and clench with maximal effort. The task was demonstrated and explained to each subject using dental casts. The subjects were instructed to repeat the task at least five times in front of a mirror prior to the recordings. The task was performed twice, and each recording lasted for 10 s. A two-minute rest period was allowed between each recording to avoid muscle fatigue. The total recording time was approximately 10 min. 2.3. Recordings of occlusion and SEMG The occluding features and SEMG activity of the bilateral MM and TA were recorded simultaneously using the T-Scan III occlusal analysis system (Tekscan, Inc., Boston, MA, USA) and the BioEMG III electromyographic recording system (BioPAK system, version 6.0, Bioresearch Associates, Inc., Milwaukee, WI, USA) with the aid of the T-Scan/BioPAK linking software (Tekscan, Inc./Bioresearch Associates, Inc. technology partnership), as described in a recent publication (Li et al., 2016). The analog EMG signal was amplified differentially with a fixed gain of 5000, within a peak-to-peak input range ±2000 lV, and digitized with 16-bit resolution at a 1000 Hz A/D sampling frequency. The theoretical resolution is 0.03 lV using a differential amplifier with a high common mode rejection ratio (CMRR > 130 dB at 50/60 Hz [either line frequency], input impedance 1012 X, and maximum signal to noise ratio 106 to 1) and filtered bandwidth in the frequency range of 20–500 Hz (low pass = 6 dB/octave, high pass = 12 dB/octave); an additional 20 dB band-stop for common 50/60 Hz interference was available with an intelligent software digital filter. Surface electrodes (BioFLEX; Bioresearch Associates, Inc., Milwaukee, WI, USA, 2 conductive polyester adhesive rectangular contacts of 144 square millimeters with 20 mm center-to-center spacing) were placed after cleaning the skin with 95% alcohol, according to generally accepted standards (Hellmann et al., 2012). A common electrode (38 mm by 32 mm; Bioresearch Associates, Inc., Milwaukee, WI, USA) was placed on the back of the neck as a reference. The electromyographic contractile activity was recorded simultaneously with the T-Scan III relative force data during acquisition. The T-Scan III occlusion analysis system with software version 6.0 was used to record occlusal contact locations, timings and relative biting forces. The sheet sensor (HD recording sensor, Tekscan Inc. Boston, MA, USA) was 60-lm-thick when compressed (Kerstein, 2004; Kerstein and Radke, 2006). The recordings were made in Turbo Mode, when the sensor was scanned in 0.003-s increments to maximize the timing resolution of the recorded occlusal contact data. Sensor sensitivity adjustment was performed following the operators manual before formal recording to fit the individual’s bite force level within the sensor’s responsiveness. Briefly, this was done by adjusting the number of red color-coded sensels, which represented the highest magnitude of the contact force, to be less than five (Kerstein and Radke, 2006).
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Table 1 Clinical information of the patients. Patients number
Age
Teeth with scissors-bite relation
Side with orofacial pain
Side with TMJ sound(s)
Duration of the disease (Month)
VAS value of pain
Mouth opening length (mm)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
19 21 22 26 23 20 26 28 24 22 23 28 27 20 27 18 21 22 19 26 24 28 19 22 21 25 26 23 21 27 27 24
A5/C5 A7/C7 A7/C7 A5/C5 A4/C4 A7/C7 A7/C7 A7/C7 A4/C4 A7/C7 B5/D5 B7/D7 B7/D7 B4/D4 B7/D7 A5/C5 A7/C7 A5/C5 A7/C7 A7/C7 A7/C7 A4/C4 A7/C7 A7/C7 A7/C7 A7/C7 A5/C5 A7/C7 B7/D7 B7/D7 B4/D4 B7/D7
Left Right Left Left Left Left Right Right Left Left Right Right Left Right Left / / / / / / / / / / / / / / / / /
/ / / / / / / / / / / / / / / Left Left Right Left Left Left Left Right Left Left Left Right Right Right Left Right Left
2 1 1 2 2 2 1 4 1 2 4 2 3 3 2 3 6 4 5 6 2 4 4 6 8 6 4 5 6 6 3 3
3 3 5 3 4 4 3 2 4 3 3 4 3 2 4 / / / / / / / / / / / / / / / / /
38 40 28 36 35 36 38 43 29 34 42 38 37 44 34 41 44 42 44 43 46 40 38 37 41 44 43 45 41 42 40 38
2.4. Parameters For each recording, the following parameters were provided automatically by the software of the T-Scan III system (Tekscan, Inc.) and the BioPAK Electrognathography software (Maruyama et al., 1986; Radke et al., 2014). (i) The Numbers of occlusal contacts: including red, yellow, green and blue colored sensels. The sum of all four color-coded sensels was represented as one contact number. If more than one color displayed in the same site, the contact number of this site was taken as one. (ii) The biting force spatial distribution: a percentage of the biting force in different dental sections, such as the right side or left side of the dental arch. (iii) The root-mean-square (in lV) SEMG activity. The time points selected for statistical analysis were when the relative force reached 25% and 50% of the maximal force and also the earliest time point at which maximal force was achieved; these time points were recorded as 25%-ICP, 50%-ICP and MVC-ICP, respectively. In the case that no point could be located on the graphs that matched the exact values of 25% and 50% relative force, the point closest to the corresponding value was selected. Finally, the selected minimum points were 21.6% and 46.2%, respectively, for the 25%-ICP and the 50%-ICP values; the selected maximums were 27.2% and 53.8%, accordingly, for the 25%-ICP and 50%-ICP values. 2.5. Statistical analysis Data from patients with pains and sounds were analyzed separately using the SPSS 13.0 package. Three-way analysis of the variance (ANOVA) was used to compare the influence of the following three factors on the occlusal contact number, biting force distribution and SEMG values. These three factors included (1) the biting force level, (2) the side of the scissors-bite and (3) the side with
orofacial pain or TMJ sounds. The Student–Newman–Keuls posttest was performed if significant differences between the groups were found. The level of significance was set at P < 0.05 for all statistical tests. For all of the comparisons, a = 0.05. 3. Results The time required for the biting force to increase from 25%-ICP to ICP-MVC was 2.17 ± 0.94 s. The three-way ANOVA data indicated that in both the group with pain and the group with TMJ sounds there were not any interactional effects of the three factors i.e., the biting-force level, the side of the scissors-bite and the side with TMD symptoms on the occlusal contact number, biting force distribution and the SEMG activity levels of the MM and TA. The factors of the biting force level and scissors-bite side showed an association with the occlusal contact number, the biting force distribution and the values of the SEMG activity of the MM (P < 0.05), while the factor of the symptom side, either the orofacial pain or the TMJ sounds, did not show such an association. The biting force level also showed an association with the value of the TA SEMG activity (P < 0.05), but neither the factor of scissors-bite side nor the factor of the symptom side, including orofacial pain and TMJ sound, showed any significant association (Tables 2 and 3). The occlusal contact number gradually increased in both sides as the biting force increased (P < 0.05; Fig. 1 and Tables 2–4). The contact number on the scissors-bite side was smaller than that on the non-scissors-bite side at all three biting force levels (P < 0.05; Fig. 1a and b). The non-scissors-bite side sustained a larger percentage of bite force (Fig. 2a and b). At the level of 100%-ICP, the scissors-bite side was 54.35% and non-scissors-bite side was 45.65% of the total bite force. When the biting force level increased from 25% to 50%, the activity of both the TA and MM significantly
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Table 2 P values disclosed by three-way ANOVA analysis for the association of the factors of biting-force level, scissors-bite side and/or orofacial pain side with the Tooth Contact Number and Biting Force Distribution disclosed by T-Scan System, and on the values of surface electromyographic (SEMG) of masseter (MM) and anterior temporalis (TA) during centric maximal voluntary clenching (MVC). Pain patients
Tooth contact number Biting force distribution SEMG value of TA SEMG value of MM
Force level
Scissorsbite
Orofacial pain
Interaction Force level & scissors-bite
Force level & orofacial pain
Scissors-bite & orofacial pain
Force level & scissors-bite & orofacial pain
0.000
0.001
0.415
0.957
0.905
0.810
0.905
1.000
0.000
0.056
0.995
0.244
0.910
0.985
0.038 0.038
0.264 0.017
0.985 0.998
0.819 0.984
0.877 0.930
0.815 0.442
0.787 0.708
Table 3 P values disclosed by three-way ANOVA analysis for the association of the factors of biting-force level, scissors-bite side and/or TMJ sound(s) side on with the Tooth Contact Number and Biting Force Distribution disclosed by T-Scan System, and on the values of surface electromyographic (SEMG) of masseter (MM) and anterior temporalis (TA) during centric maximal voluntary clenching (MVC). TMJ sound(s) patients
Force level
Scissors bite
TMJ sound (s)
Interaction Force level & scissors bite
Force level & TMJ sound(s)
Scissors bite & TMJ sound(s)
Tooth contact number Biting force distribution SEMG value of TA SEMG value of MM
0.000
0.000
.364
.827
.726
.496
.981
1.000
0.000
.837
.893
.402
.999
1.000
0.009 0.039
.153 0.004
.154 .527
.983 .820
.656 .927
.151 .082
.843 .599
Force level & scissors bite & TMJ sound(s)
Fig. 1. Comparison of the mean (±SD) of the Number of contacts between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
increased (P < 0.05; Figs. 3 and 4). When the force increased from 50% to 100% of the maximum, however, the SEMG activity of both the TA and MM did not show further changes (Figs. 3 and 4).
At the 100%-ICP force level, the scissors-bite side for the MM showed lower SEMG activity than that of the non-scissors-bite side (P < 0.05; Fig. 4a and b). This side difference was not found at the
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Table 4 Comparison of occlusion contact numbers at different force levels between sides. Force level
Side
Red (highest level)
Yellow (high level)
Green (middle level)
Blue (low level)
Total
25% (pain patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
0.20 0.40 0.20 0.40
0.07 0.20 0.20 0.20
3.33 3.87 3.73 3.53
0.53 0.60 0.40 0.53
4.13 5.07 4.53 4.67
25% (sound patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
0.24 0.35 0.29 0.29
0.12 0.29 0.12 0.29
3.59 4 3.88 3.71
0.53 0.94 0.71 0.76
4.59 5.59 5 5.06
50%(Pain Patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
0.40 0.53 0.47 0.47
0.53 0.93 0.93 1.07
4.00 4.73 4.53 5.00
1.73 1.53 1.20 1.00
6.66 7.72 7.13 7.54
50%(Sound Patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
0.35 0.47 0.41 0.41
0.59 0.77 0.65 0.71
4.12 4.76 4.47 4.41
0.77 0.88 0.76 0.88
5.82 6.88 6.29 6.41
100%(Pain Patients)
Scissors-bite Non scissors-bite Orofacial pain Orofacial pain free
1.00 1.60 1.20 0.60
1.00 1.20 1.33 1.67
4.47 4.27 4.67 4.33
2.00 2.27 1.67 2.33
8.47 9.34 8.87 8.93
100%(Sound Patients)
Scissors-bite Non scissors-bite TMJ sound(s) Non TMJ sound(s)
1.12 1.06 1.06 1.12
1.18 1.29 1.35 1.12
4.65 5.06 4.76 4.94
2.12 2.71 2.35 2.47
9.06 10.12 9.53 9.65
Note: Biting force level is ordered as red > yellow > green > blue.
Fig. 2. Comparison of the mean (±SD) of the biting force distribution between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
K. Qi et al. / Journal of Electromyography and Kinesiology 28 (2016) 114–122
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Fig. 3. Comparison of the mean (±SD) of the SEMG of TA between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels.
other two biting force levels. There were also no symptom side differences of MM activity at any biting force levels in patients with orofacial pain or patients with TMJ sounds (Fig. 4c and d).
4. Discussion The present results showed that in this group of unilateral scissors-bite patients with unilateral orofacial pain or TMJ sounds, it was the scissors-bite relation rather than the TMD symptoms that was associated with MM SEMG activity during centric MVC. Compared to the non-scissors-side, the scissors-bite side showed a lower level of MM SEMG activity together with a smaller occlusal contact number and less biting force distribution. No such an occlusion association was noticed with TA SEMG activity. Biting force during MVC is influenced by occlusion (Bakke, 2006; English et al., 2002). Using a polynomial regression model, Bakke et al. (1990) indicated that 10–20% of the variation of maximum bite force in adults was determined by occlusal contact. Scissors-bite results in a reduced occlusal contact area because of reduced intercuspation of the maxillary and mandibular teeth (Maeda et al., 2008). Thus, patients with scissors-bite have a lower level of bite force (Sonnesen et al., 2001). Biting force is ascribed to the contraction of the jaw-closing muscles. The present lower level of MM SEMG activity at the scissors-bite side during centric MVC agrees with the detected data of lower biting force and smaller contact number at the scissors-bite side. This decrease of SEMG activity was not observed in the TA which differs from what was reported by Tomonari et al. (2014) who found both TA and MM on the scissors-bite side had lower SEMG activity than on the non-scissors-bite side, but agrees with the fact that there is a functional difference between MM and TA. For example, when clenched
with unilateral occlusal support, which causes a less symmetric load of the jaw and TMJ tissues (Van der Bilt et al., 2008), the MM contributes to keep the mandible in balance by lowering its activity at the working side, while the TA more likely provides clenching power at the working side (Wang et al., 2010). In agreement with this muscle’s functional difference, a less balanced occlusion, such as the scissors-bite in the current study and posterior cross-bite in other reports (Alarcón et al., 2000; Piancino et al., 2009), has demonstrated an association with a lower level of MM SEMG activity. As for the TA, its SEMG activity was increased when the biting force increases, having least association with the contact number. In addition to biting force (Baba et al., 1996; Christensen and Rassouli, 1995; Naeije et al., 1989) and the number of occlusal contacts (Kerstein, 2004; Ferrario et al., 2002), the SEMG activity of jaw-closing muscles during clenching is also influenced by many other factors, such as jaw position (Baba et al., 2000) and the contact locations (Bakke, 1993). Thus, the SEMG activity is an outcome of the summation of many factors. Some subsets of SEMG activity are responsible for stabilizing the mandibular bone during clenching (Wang et al., 2013). Our previous report indicated that in healthy subjects, when the number of the occlusal contacts increased to the MVC level, the requirement for moving the mandible to a stable condition is reduced, leading to a decrease in the MM SEMG activity at the MVC level compared to that at 50% of the MVC level (Wang et al., 2013). However, in the present scissors-bite orofacial pain patients, this decrease in MM SEMG activity was not observed, implying a functional increase of this muscle in these patients. Moreover, the MM SEMG activity from 25%-ICP to 50%-ICP in healthy individuals showed no difference (Wang et al., 2013), while this activity value was increased in patients. Specifically, the patients with an unstable scissors-bite
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Fig. 4. Comparison of the mean (±SD) of the SEMG of MM between the scissors-bite side and non-scissors-bite side in orofacial pain patients (a) and TMJ sound(s) patients (b), orofacial pain side and non orofacial pain side in orofacial pain patients (c), TMJ sound(s) side and non TMJ sound(s) side in TMJ sound(s) patients (d) during centric maximal voluntary clenching (MVC) from rest to 25%, 50% and 100% maximal force level (represented in panels as 25%, 50% and 100%, respectively). ⁄: P < 0.05 between force levels. #: P < 0.05 between sides.
relation tended to perform a modified MVC, possibly to prevent potential harm; It took 2.17 ± 0.94 s from 25% to MVC when the patients were required to perform a fast close, while healthy individuals took 1.55 ± 0.84 s to complete this movement (Wang et al., 2013). Orofacial pain and TMJ sounds are two of the most common signs of TMD. Nowdays, there remains no consensus on the association of TMD and the jaw muscles’ EMG activity. Nielsen et al. (1990) reported that there were no significant differences of MM SEMG values during clenching between TMD patients and healthy controls. However, pain and sounds may have different effects on the masticatory muscles. Santana-Mora et al. (2009) reported that the MM SEMG activity of patients with unilateral TMD pain symptoms for over 6 months (VAS: 4.76 ± 1.70) was lower on the pain side than on the pain-free side. In addition, Liu et al. (1989) stated that TMJ sounds were related to the function of the lateral pterygoid muscles, but less related to the SEMG activity of the MM and TA in centric clenching. However, no occlusion details were provided in these reports, and the differences in patient homogenization and study methodology make precise comparison between reports impossible. The inclusion criteria for the present study were carefully implemented by choosing patients with not only unilateral symptoms, pains or sounds but also with unilateral scissor-bite relations. In this way, we were able to compare the side differences and to disclose the association of SEMG activity of the jaw-closing muscles with occlusion and/or symptoms. Our results indicate that not only did the sound side show no association with the jaw-closing muscles’ SEMG activity, as was reported (Liu et al., 1989), but also that the pain side showed no such association, which is in agreement with our recent report (Li et al.,
2016). In considering the present results, the number of subjects was too small to be a reflection of a specific population. Furthermore, there could have been an effect from the T-Scan sensor that was inserted between the dentitions, although it was only 60–100 lm in thickness (Kerstein, 2004; Kerstein and Radke, 2006). Indeed, a previous study on interocclusal thickness discrimination showed that aluminum foil as thin as 20 lm could impact the bite-disturbing proprioceptive information for a subject (Kampe et al., 1987). Thus, the data from this type of instrument only provide a general idea of the occlusal contacts. Overall, the present data from a small number of subjects indicate, in patients with unilateral TMD symptom(s) and scissors-bite, that the jaw-closing muscles’ SEMG activity during centric MVC was more associated with the scissors-bite rather than the symptoms of orofacial pain or TMJ sounds. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgments The study was supported by the National Nature Science Foundation of China (NSFC) No. 81470762. Thanks to John Radke, Chairman of BioResearch Associates, Inc., for his advice regarding the using of the software and analyzing program, and also a proof reading. The statistics assistance of Lin Sun was gratefully acknowledged. The participation of patients was greatly appreciated.
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References Alarcón, J.A., Martín, C., Palma, J.C., 2000. Effect of unilateral posterior crossbite on the electromyographic activity of human masticatory muscles. Am. J. Orthod. Dentofac. Orthop. 118 (3), 328–334. Baba, K., Ai, M., Mizutani, H., Enosawa, S., 1996. Influence of experimental occlusal discrepancy on masticatory muscle activity during clenching. J. Oral Rehabil. 23 (1), 55–60. Baba, K., Yugami, K., Akishige, S., Ai, M., 2000. Immediate effect of occlusal contact pattern in lateral jaw position on the EMG activity in jaw-elevator muscles in humans. Int. J. Prosthodont. 13 (6), 500–505. Bakke, M., 1993. Mandibular elevator muscles: physiology, action, and effect of dental occlusion. Scand. J. Dent. Res. 101 (5), 314–331. Bakke, M., 2006. Bite force and occlusion. Semin. Orthod. 12 (2), 120–126. Bakke, M., Holm, B., Jensen, B.L., Lars, M., Eigild, M., 1990. Unilateral, isometric bite force in 8–68-year-old women and men related to occlusal factors. Scand. J. Dent. Res. 98 (2), 149–158. Carlsson, A.M., 1983. Assessment of chronic pain. I. Aspects of the reliability and validity of the visual analogue scale. Pain 16 (1), 87–101. Christensen, L.V., Rassouli, N.M., 1995. Experimental occlusal interferences. Part II. Masseteric EMG responses to an intercuspal interference. J. Oral Rehabil. 22 (7), 521–531. Dworkin, S.F., Leresche, L., 1992. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J. Craniomandib. Disord. 6 (4), 301–355. English, J.D., Buschang, P.H., Throckmorton, G.S., 2002. Does malocclusion affect masticatory performance? Angle Orthod. 72 (1), 21–27. Felício, C.M.D., Ferreira, C.L.P., Medeiros, A.P.M., Tartaglia, G.M., Sforza, C., 2012. Electromyographic indices, orofacial myofunctional status and temporomandibular disorders severity: a correlation study. J. Electromyogr. Kinesiol. 22 (2), 266–272. Ferrario, V.F., Serrao, G., Dellavia, C., Caruso, E., Sforza, C., 2002. Relationship between the number of occlusal contacts and masticatory muscle activity in healthy young adults. Cranio 20 (20), 91–98. Fogle, L.L., Glaros, A.G., 1995. Contributions of facial morphology, age, and gender to EMG activity under biting and resting conditions: a canonical correlation analysis. J. Dent. Res. 74 (8), 1496–1500. Hellmann, D., Giannakopoulos, N.N., Schmitter, M., Lenz, J., Schindler, H.J., 2012. Anterior and posterior neck muscle activation during a variety of biting tasks. Eur. J. Oral Sci. 120 (4), 326–334. Jonsson, T., Arnlaugsson, S., Karlsson, K.O., 2007. Orthodontic treatment experience and prevalence of malocclusion traits in an Icelandic adult population. Am. J. Orthod. Dentofac. Orthop. 131 (1), 8.e11–8.e18. Kampe, T., Haraldson, T., Hannerz, H., Carlsson, G.E., 1987. Occlusal perception and bite force in young subjects with and without dental fillings. Acta Odontol. Scand. 45 (2), 101–107. Kerstein, R.B., 2004. Combining technologies: a computerized occlusal analysis system synchronized with a computerized electromyography system. Cranio 22 (2), 96–109. Kerstein, R.B., Radke, J., 2006. The effect of disclusion time reduction on maximal clench muscle activity levels. Cranio 24 (3), 156–165. Lambourne, C., Lampasso, J., William, C., Buchanan, J., Dunford, R., Mccall, W., 2007. Malocclusion as a risk factor in the etiology of headaches in children and adolescents. Am. J. Orthod. Dentofac. Orthop. 132 (6), 754–761. Li, B.Y., Zhou, L.J., Guo, S.X., Zhang, Y., Lu, L., Wang, M.Q., 2016. An investigation on the simultaneously recorded occlusion contact and surface electromyographic activity for patients with unilateral temporomandibular disorders pain. J. Electromyogr. Kinesiol. 28, 199–207. Liu, Z.J., Wang, H.Y., Pu, W.Y., 1989. A comparative electromyographic study of the lateral pterygoid muscle and arthrography in patients with temporomandibular joint disturbance syndrome sounds. J. Prosthet. Dent. 62 (2), 229–233. Lobbezzo, F., van Selms, M.K.A., Naeije, M., 2006. Masticatory muscle pain and disordered jaw motor behaviour: literature review over the past decade. Arch. Oral Biol. 51 (9), 713–720. Maeda, A., Soejima, K., Ogura, M., Ohmure, H., Sugihara, K., Miyawaki, S., 2008. Orthodontic treatment combined with mandibular distraction osteogenesis and changes in stomatognathic function. Angle Orthod. 78 (6), 1125–1132. Maruyama, T., Kuwabara, T., Mizumori, T., Miyauchi, S., Kuroda, T., 1986. The effect of TMJ abnormalities on chewing movements. J. Osaka Univ. Dent. Sch. 25, 63–77. Naeije, M., McCarroll, R.S., Weijs, W.A., 1989. Electromyographic activity of the human masticatory muscles during submaximal clenching in the intercuspal position. J. Oral Rehabil. 16 (1), 63–70. Nielsen, I.L., McNeill, C., Danzig, W., Goldman, S., Levy, J., Miller, A.J., 1990. Adaptation of craniofacial muscles in subjects with craniomandibular disorders. Am. J. Orthod. Dentofac. Orthop. 97 (1), 20–34. Piancino, M.G., Farina, D., Talpone, F., Merlo, A., Bracco, P., 2009. Muscular activation during reverse and non-reverse chewing cycles in unilateral posterior crossbite. Eur. J. Oral Sci. 117 (2), 122–128. Radke, J.C., Kull, R.S., Sethi, M.S., 2014. Chewing movements altered in the presence of temporomandibular joint internal derangements. Cranio 32 (3), 187–192. Santana-Mora, U., Cudeiro, J., Mora-Bermúdez, M.J., 2009. Changes in EMG activity during clenching in chronic pain patients with unilateral temporomandibular disorders. J. Electromyogr. Kinesiol. 19 (6), e543–e549. Sonnesen, L., Bakke, M., Solow, B., 2001. Bite force in pre-orthodontic children with unilateral crossbite. Eur. J. Orthod. 23 (6), 741–749.
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Tomonari, H., Kubota, T., Yagi, T., Kuninori, T., Kitashima, F., Uehara, S., Miyamaki, S., 2014. Posterior scissors-bite: masticatory jaw movement and muscle activity. J. Oral Rehabil. 41 (4), 257–265. Türp, J.C., Schindler, H., 2012. The dental occlusion as a suspected cause for TMDs: epidemiological and etiological considerations. J. Oral Rehabil. 39 (7), 502–512. Van der Bilt, A., Tekamp, A., Van der Glas, H., Abbink, J., 2008. Bite force and electromyography during maximum unilateral and bilateral clenching. Eur. J. Oral Sci. 116 (3), 217–222. Wang, M.Q., He, J.J., Zhang, J.H., Wang, K., Svensson, P., Widmalm, S.E., 2010. SEMG activity of jaw-closing muscles during biting with different unilateral occlusal supports. J. Oral Rehabil. 37 (9), 719–725. Wang, X.R., Zhang, Y., Xu, Y.F., Wang, M.Q., 2013. Stable tooth contacts in intercuspal occlusion makes for utilities of the jaw elevators during maximal voluntary clenching. J. Oral Rehabil. 40 (5), 319–328.
Kun Qi received the B.S. (2005) and the M.S. degree (2008) in Medical Science from the Xi’an Jiaotong University. He is currently attending to his Ph.D. in Oral Anatomy and Physiology at the Fourth Military Medical University. His clinical and research interests are correlations between occlusion and temporomandibular disorders.
Shaoxiong Guo received the B.S. (2012) in Medical Science from Xi’an Medical University and the M.S. degree (2015) in the Fourth Military Medical University. He is currently attending to his Ph.D. in Oral Anatomy and Physiology at the Fourth Military Medical University. He has focused significant part of his research activity on the correlations between the masticatory system and cervical system and evidence-based dentistry.
YiFei Xu received the B.S. (2007) and the M.S. degree (2010) in Medical Science from the Xi’an Jiaotong University. She is currently Attending Dentist in Oral Anatomy and Physiology at the Fourth Military Medical University. Her clinical and research interests are correlations between othodontics and temporomandibular disorders.
Qi Deng received the B.S. (2012) and she is a clinical research member and physical therapist in the Fourth Military Medical University. She has cured about 300 oral-facial pain patients. Her clinical and research interests are health care of Temporomandibular Disorders and SEMG of masticatory muscle.
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K. Qi et al. / Journal of Electromyography and Kinesiology 28 (2016) 114–122 Lu Liu received the B.S. (2013) and she is a clinical research member and physical therapist in the Fourth Military Medical University. She has cured about 400 oral-facial pain patients. Her clinical and research interests are health care of Temporomandibular Disorders and laser therapy of masticatory muscle disorder.
Baoyong Li received the B.S. (2003) and the M.S. degree (2007) in Medical Science from the Fourth Military Medical University. He is currently attending to his Ph. D. in Oral Anatomy and Physiology at the Fourth Military Medical University. His clinical and research interests are correlations between occlusion and temporomandibular disorders.
Dr. Meiqing Wang is the Chief Professor in Dept. Oral Anatomy and Physiology and TMJ, College of Stomatology, Fourth Military Medical University. She is an occlusionist and specialist in Temporomandibular Disorders (TMD). She treats over 30 TMD patients per week from 1997. She have published more than 200 papers, including over 40 English papers to expression her scientific view point that occlusion takes a role in TMD. She has also edited and published 4 books in Chinese on Oral Anatomy and Physiology and Occlusion. She has supervised more than 50 postgraduate students. She has won the awards of Education Progress in Military (1997), the Science and Technology Progress in Military (Second Class, 2003) and in Shanxi Province (First Class, 2005). She was honoured as the Excellent Teacher of Chinese Military Schools (1998, 2006 and 2010). She is now the vice president of the Society of TMD and Occlusion and the president of Occlusion Branch, Chinese Stomatological Association (CSA). She is now the editorial board member of J Bone Mineral Res, J Oral Rehabil and CRANIO.