Evaluation of masticatory muscle activity in patients with unilateral posterior crossbite before and after rapid maxillary expansion

Evaluation of masticatory muscle activity in patients with unilateral posterior crossbite before... Summary Objectives The relationship between unilateral posterior crossbite (UPCB) and the possible asymmetric activation of the jaw muscles in children is still under debate. This study aimed at evaluating the jaw muscle activity of children with UPCB before and after rapid maxillary expansion (RME) by means of surface electromyography and a standardized sampling protocol. Subjects and methods Twenty-nine children with UPCB (UPCB-group, mean age 9.6 ± 1.6 years) and 40 UPCB-free controls (Control-group, 10.5 ± 1.1) were recruited. The activity of the left and right anterior temporalis (AT) and superficial masseter muscles (MM) was recorded during maximum voluntary clenching and a chewing task (T0). In the UPCB-group, data were collected, also, after the correction of the UPCB with RME (T1) and 6 months later (T2), without any further treatment. Electromyographic indices comparing the activity of paired muscle were computed via software to estimate the extent of asymmetric AT and MM activity. Paired and unpaired t-test or Wilcoxon-signed rank and Mann–Whitney U test, ANOVA or Friedman test and chi-squared test were used in the statistical analysis. Results Both groups presented with asymmetric activity of the muscles, which did not differ between groups (T0, all P > 0.05). The treatment determined a decrease in muscular activity (T1, P = 0.040), and a more asymmetric pattern of muscle activation during chewing (T1, P = 0.040), which returned similar to baseline values at T2 (all P > 0.05). Conclusions UPCB does not contribute to an asymmetric activation of AT and MM during functional tasks. The treatment of UPCB by RME did not determine a more symmetric activity of the assessed muscles. Introduction Posterior crossbite (PCB) is a common malocclusion, which affects 8–22 per cent of orthodontic patients in the primary and early mixed dentition (1) and 5–15 per cent of the general population (2). Unilateral posterior crossbite (UPCB) with a functional shift of the mandible occurs in 71–84 per cent of individuals with PCB (3). UPCB has been suggested to determine an asymmetrical activation of the masticatory muscles and therefore might contribute to the onset of skeletal asymmetries and temporomandibular joint disorders (TMD) (4–6). Based on these assumptions, early treatment of UPCB by maxillary expansion (7–9) is commonly recommended to reduce the risk of developing craniofacial anomalies and TMD in adulthood (4, 5). The activity of muscles is commonly investigated in research settings by using surface electromyography (sEMG). Nonetheless, electromyographic (EMG) data can be affected by several artefacts, which could account for a problematic data analysis and interpretation (10). The introduction of standardized EMG protocols and indices to assess the activity of paired masticatory muscles has allowed for more reliable analyses (11–13). Ferrario et al. (12) developed a method for standardizing myoelectric potentials, which computes indices depicting the activation of elevator muscles and the extent of symmetric activation between paired muscles during specific functional tasks. This method reduces the intra-sample variability and can be used for the assessment of jaw muscle activity during both static and dynamic tasks (12, 13). The effects of the correction of UPCB on the activity of anterior temporalis (AT) and superficial masseter (MM) muscles have been evaluated using sEMG, with controversial findings (14–20). One study (18) concluded that the degree of asymmetry of masticatory muscles during function is not affected by the presence of crossbite. Others reported that the treatment of crossbite contributes to a more symmetric pattern of activation of the chewing muscles during function only to a slight extent (15, 20). Finally, findings included in other reports may be questionable since they lack of untreated subjected acting as controls (17, 19). A recent review has reported that the treatment of crossbite contributes to increasing the activity of masticatory muscles, approaching levels similar to subjects with normal occlusion (21). Differently from other studies, this research has investigated the relationship between crossbite and asymmetry in the activity of the chewing muscles by using a standardized EMG protocol and indices. This method allows for a more precise and objective assessment of the muscle function and overcomes the limits of classical approaches using surface EMG (e.g. EMG cross-talk, artefacts, changes into the signal due to the location of the electrodes). The protocol of this study used standardized EMG potentials, which allow for more accurate intragroup and between group comparisons. In addition, the use of indices of asymmetry instead of values of electric potentials (microvolt) provides clinicians with more relevant and intelligible clinical information. The relationship between crossbite and asymmetric jaw muscle activity has been subject of debate in several studies. An early treatment of crossbite is commonly recommended to reduce the risk of developing skeletal asymmetries as a consequence of abnormalities in masticatory function between the right and left sides. A better understanding of both the possible relationship between UPCB and asymmetric muscular function and the effect of RPE on the extent of muscular asymmetry during function might contribute to clarifying whether an early treatment of UPCB with RPE should be recommended. This study aimed at evaluating the AT and MM muscle activity of children with UPCB before and after RME by means of sEMG and a standardized EMG sampling protocol. The null hypotheses to be tested were: the UPCB patients do not present more asymmetric AT and MM muscle activity compared to UPCB-free controls during standardized tasks; and maxillary expansion does not determine a more symmetric activation of AT and MM muscles during functional tasks. Materials and methods Study sample Twenty-nine children with UPCB (UPCB-group: 13 males, 16 females, mean age ± SD = 9.6 ± 1.6 years) and 40 UPCB-free controls (Control-group: 17 males, 23 females; mean age 10.5 ± 1.1 years) seeking an orthodontic consultation were recruited consecutively. For both groups, exclusion criteria were genetic or congenital abnormalities, craniofacial anomalies, systemic diseases affecting growth and development, clinical signs or symptoms of TMD (22), reporting of oral parafunctions (22), and previous or current orthodontic treatment. Inclusion criteria were an Angle Class I relationship, presence of the four first permanent molars, mixed dentition stage, and the absence of tooth mobility or decayed teeth. The experimental group included subjects with UPCB and lateral shift towards the UPCB side as assessed by Dawson’s manoeuvre (23). The control group included subjects without UPCB. Parents or guardians received information about the research protocol and signed an informed consent. The research protocol was designed in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans and was reviewed and approved by the Research Ethics Board (protocol 22616). EMG assessment The electrical activity of the right and left AT and MM muscles was recorded simultaneously during standardized tasks via sEMG. Silver-silver chloride bipolar surface pre-gelled electrodes (Kendall, Mansfield, MA, USA) with a diameter of 24 mm were placed on the skin along the main direction of the muscular fibres according to the protocol described by Ferrario et al. (12). To minimize electrode impedance, the skin was thoroughly cleaned with an abrasive preparation gel (Everi, Spes Medica, Genova, Italy) before electrode placement. Recordings were performed at least 5–6 minutes after the application of the electrode to allow the conductive gel to adequately moisten the skin surface. All participants sat in a dental chair. The position of the seatback was fixed, while the vertical excursion of the dental chair could be adjusted by the operator. The study was performed using a wireless EMG device (TMJOINT, BTS SpA, Garbagnate Milanese, Italy). The EMG signals were acquired at 1KHZ, amplified (gain 150) and filtered via hardware (low-pass filter 500Hz; high-pass 10Hz). A software program (Dental Contact Analyser, BTS SpA) processed the raw electrical signals and generated root mean square (RMS) values. Thereafter, RMS values were processed by an algorithm to generate indices of muscle activity and asymmetry. The EMG protocol included two static and two dynamic tests. All participants received standardized instructions about the research protocol. The EMG protocol and the algorithm used for the standardization of the EMG signals and the computation of the indices have been used and described in several research studies (11–13, 24). The static tests included the following: 1. Maximum voluntary contraction (MVC) in intercuspal position (CLENCH)—participants clenched their teeth as hard as possible for 5 seconds; 2. MVC in intercuspal position on cotton rolls (COT)—participants clenched as hard as possible for 5 seconds on 10 mm thick cotton rolls (Intermedical, Terlano, Bolzano, Italy) positioned from the mandibular first molar to the canine on both sides. For the 5-second static tests, two hundred 25 msec RMS samples were collected. The 120 samples, corresponding to 3 second, with the highest RMS values were used to compute the indices. The EMG waves of each muscle (120 samples) with and without cotton rolls were superimposed sample by sample, and the ratio between the superimposed areas and the total areas was computed automatically via software. Hence, for each subject, the EMG potentials recorded during the MVC were expressed as percentage of the mean RMS potential recorded during the MVC on the cotton rolls (EMG standardized potentials). The dynamic tests included the following: 1. Chewing gum (Air Action Vigorsol, Lainate, Italy) on the right side for 15 seconds. 2. Chewing on the left side for 15 seconds. Between the static and the dynamic tests, participants were asked to rest for 3 minutes. The following standardized EMG indices were calculated via software: Computed indices (static tests) 1. POC (percentage of overlapping coefficient). The standardized EMG waves of the left and right AT and MM were compared by computing a percentage overlapping coefficient (POC, unit: %, range: 0–100 per cent, norm values 85 per cent ≤ POC ≤ 100 per cent) (11, 13, 24). If the muscles contract with perfect symmetry, a POC of 100 per cent (perfect symmetry) is expected. Conversely, a value corresponding to 0 per cent indicates the absence of concurrent activation of paired muscles (no symmetry). Three indices were computed for each subject (POC AT, POC MM and POC medium). 2. TC (torque coefficient). This index is obtained by measuring the overlapping activity (standardized EMG waves) between the left MM and right AT and the right MM and left AT. The higher muscular activity of one couple (i.e. left MM and right AT) over the other (i.e. right MM and left AT) results in a torquing effect on the lower jaw. TC ranges between 0 per cent (no symmetric activation of the couples, greatest torquing effect) and 100 per cent (perfect symmetric activation of the couples, no torquing effect). Normal values are 90 per cent ≤ TC ≤ 100 per cent (12, 13, 24). 3. IMPACT (total standardized muscle activity). This index is computed as the integrated area of the EMG standardized potentials of both MM and AT over time (5 seconds MVC). Norm values are 85 per cent ≤ IC ≤ 115 per cent (12). Lower values indicate that the EMG standardized potentials were reduced during the clenching tasks, and that the maximal EMG activity could not be expressed. 4. ASIM (asymmetry index). This index is calculated by comparing the activity of the right couple (right AT and right MM) to the left couple (left AT and left MM). ASIM ranges from −100 per cent and +100 per cent; a value of 0 per cent depicts a perfect symmetric activation of the two couples. A negative value indicates greater activity of the left couple; conversely, a positive value indicates a greater activity of the right couple. Norm values are −10 per cent ≤ ASIM ≤ +10 per cent (25). Computed indices (dynamic tests) 1. SMI (symmetrical mastication index) was computed to assess whether the left- and the right-side chewing tests were performed with symmetrical muscular patterns. It indicates the distance between the centre of the chart and the centre of the ellipse in a graph that describes the prevalence of one side over the other during mastication (Figure 1). SMI ranges between 0 per cent (no symmetry) and 100 per cent (symmetrical muscular pattern). Normal values are 70 per cent ≤ SMI ≤ 100 per cent (11). 2. SPM (side of prevalent mastication) in case of SMI values lower than 70 per cent, the dominant side of mastication was identified as side of prevalent mastication (Figure 1). Three categories could be identified, that is right, left and symmetric. 3. FREQ (frequency index) measures the frequency of masticatory cycles during the chewing experimental tasks and was reported in hertz (Hz: bites per second). Figure 1 View largeDownload slide Determination of the symmetrical mastication index (SMI). x-axis: differential masseter (left (-) versus right); y-axis: differential temporal (left (-) versus right) (µV). Red dots and the corresponding ellipse depict data recorded during the task ‘chewing on the left side’. Blue dots and the corresponding ellipse depict data recorded during the task ‘chewing on the right side’. In an ideal condition (complete symmetric activity between right and left sides during chewing), the centre of the ellipse describing the task ‘chewing on the right side’ will be located in the first quadrant (top left) and the centre of the ellipse describing the task ‘chewing on the left side’ in the third quadrant (bottom right). The symmetrical mastication index (SMI, %) is calculated using the distance between the centres of the two confidence ellipses and the origin of the axes. If the right and left chewing tasks are symmetric, the right and left ellipses will have the same distance from the origin of the axes, and a 180 degree difference between phase angles (angle between the x-axis and the segment connecting the centre of the ellipse and the axis origin). Symmetric patient (A). Similar distances between the system origin and the centre of the ellipse, and similar phase angle between the two tasks. Asymmetric patient (B). The blue ellipse has a bigger distance respect to the centre and the difference between the angles is lower than 180 degree. Figure 1 View largeDownload slide Determination of the symmetrical mastication index (SMI). x-axis: differential masseter (left (-) versus right); y-axis: differential temporal (left (-) versus right) (µV). Red dots and the corresponding ellipse depict data recorded during the task ‘chewing on the left side’. Blue dots and the corresponding ellipse depict data recorded during the task ‘chewing on the right side’. In an ideal condition (complete symmetric activity between right and left sides during chewing), the centre of the ellipse describing the task ‘chewing on the right side’ will be located in the first quadrant (top left) and the centre of the ellipse describing the task ‘chewing on the left side’ in the third quadrant (bottom right). The symmetrical mastication index (SMI, %) is calculated using the distance between the centres of the two confidence ellipses and the origin of the axes. If the right and left chewing tasks are symmetric, the right and left ellipses will have the same distance from the origin of the axes, and a 180 degree difference between phase angles (angle between the x-axis and the segment connecting the centre of the ellipse and the axis origin). Symmetric patient (A). Similar distances between the system origin and the centre of the ellipse, and similar phase angle between the two tasks. Asymmetric patient (B). The blue ellipse has a bigger distance respect to the centre and the difference between the angles is lower than 180 degree. Rapid maxillary expansion All subjects of the UPCB group were treated with a two-band palatal expander and rapid maxillary expansion (RME, Figure 2) (26). The appliance was banded to the maxillary first permanent molars and placed using glass ionometer cement (Multi-Cure Glass ionomer Cement; Unitek, Monrovia, CA, USA). The screw was initially turned eight times (2.0 mm) at chair side 2 hours after curing. Thereafter, the patients’ parents were trained to turn the screw three times per day (0.75 mm). During the expansion phase, subjects were monitored once a week. The screw was activated until a 2-mm molar transverse overcorrection was achieved. After the active expansion phase, the screw was locked with light-cure flow composite resin (Premise Flowable; Kerr Corporation, Orange, CA, USA). The active treatment (expansion) ranged between 10 and 16 days. The patients wore the appliance as fixed retainer for 6 months. Figure 2 View largeDownload slide Two-band palatal expander at the end of the expansion phase. Figure 2 View largeDownload slide Two-band palatal expander at the end of the expansion phase. Data collection The EMG activity of the AT and MM of both sides (left end right) was recorded at baseline after recruitment (T0) for both the UPCB and Control-group. For the UPCB group, EMG activity was recorded also when the UPCB was corrected (T1), and 6 months after when the appliance was removed (T2). EMG indices for both static and dynamic tests were computed at each time point. Sample size calculation and statistical analysis A sample size calculation was performed before recruitment. The primary outcome measure of this study was the POC medium index. Based on a previous investigation (12), it was assumed that a difference in POC medium values of 5 per cent (SD = 4.55 per cent) between the UPCB and the Control-group could be considered of clinical relevance. A sample including 21 subjects per group was sufficient to detect between-group differences in POC medium (α = 0.05 and 1 − β = 0.9). The Shapiro–Wilk test was used to check whether data were normally distributed. Mean and standard deviation (SD) for data distributed normally, and median with first and third interquartile range for data not normally distributed were calculated. Between-group differences in standardized EMG indices, except ASIM and SPM, were tested by means of an unpaired t-test or Mann–Whitney U test for between-group comparisons. Repeated measures ANOVA or the Friedman test was used to test the effect of orthodontic treatment on EMG indices (POC AT, POC MM, Tc, IMPACT, SMI) and to detect differences between the time points in the UPCB group. The post hoc Tukey’s test with Bonferroni’s correction or the Wilcoxon signed-rank test was used. For FREQ, the differences between the crossbite side minus the non-crossbite side, in the UPCB group, and between the right side minus the left side in the Control-group, were calculated. This variable, normally distributed, was analyzed for each group and for each time point by means of a paired t-test for within-group comparisons and by means of an unpaired t-test for between-group comparisons. ASIM and SPM were reported as frequencies. ASIM and SPM values were used to categorize participants in two groups (symmetric and asymmetric) based on normative values (symmetric: −10 per cent ≤ ASIM ≤ +10 per cent; asymmetric: ASIM ≥ +10 per cent or ASIM ≤ −10 per cent; symmetric: SPM > 70 per cent; asymmetric: SPM < 70 per cent). A chi-squared test was performed to examine whether the distribution of ASIM and SPM categories was similar between the study groups. Moreover, for patients that showed symmetrical jaw muscle activity, the prevalent side was recorded, and a chi-squared test was done to assess whether there was an association between the side of prevalent muscular activity and the side of the UPCB (UPCB group) at both T0 and T2. Standard statistical software package (SPSS version 22.0, SPSS IBM, Armonk, NY, USA) was used for statistical analysis. Results EMG indices at baseline: within-group and between-group comparisons All the indices of the static tests (POC, TC, IMPACT) did not differ between groups at T0 (Table 1). Based on the assessment of ASIM values, 20 out of 29 patients from the UPCB group and 29 out of 40 individuals presented symmetric EMG activity. The ASIM index was not associated with the presence of UPCB (P = 0.749). Table 1 Standardized EMG indices of control and UPCB group at T0. Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Values are expressed in %, mean and standard deviation (SD), for data distributed normally and median with first and third interquartile for data not distributed normally. View Large Table 1 Standardized EMG indices of control and UPCB group at T0. Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Values are expressed in %, mean and standard deviation (SD), for data distributed normally and median with first and third interquartile for data not distributed normally. View Large During the chewing tasks, SMI did not differ between the two groups (Table 1); moreover, 19 out of 29 patients in the UPCB group and 25 out of 40 individuals had a side of prevalent mastication (SPM). The chi-square test showed that SPM was independent from the presence of the UPCB (P = 0.736). Finally, FREQ (T0) was not different both between sides (UPCB: UPCB side 1.6 ± 0.2 Hz; no UPCB side 1.6 ± 0.3 Hz—P=0.052; Control-group: Right 1.4 ± 0.3 Hz; Left 1.5 ± 0.3 Hz—P = 0.072) and between groups (P = 0.614). EMG indices in the UPCB group before and after orthodontic treatment (T0–T2) POC and TC values did not change significantly throughout the three time points of the study (All P > 0.05; Table 2). IMPACT changed significantly with time (P = 0.040); it decreased at T1 (P = 0.007), and returned to baseline values at T2 (P = 0.424). The ASIM categories varied considerably over the three time points (Figure 3). Table 2 Standardized EMG indices of UPCB group at T0, T1 and T2. Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Values are expressed in %, mean and standard deviation (SD) (for data distributed normally) and median with first and third interquartile (for data not distributed normally) are reported. Bold text indicates statistically significant differences between time points. Post hoc tests with Bonferroni’s correction was used. View Large Table 2 Standardized EMG indices of UPCB group at T0, T1 and T2. Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Values are expressed in %, mean and standard deviation (SD) (for data distributed normally) and median with first and third interquartile (for data not distributed normally) are reported. Bold text indicates statistically significant differences between time points. Post hoc tests with Bonferroni’s correction was used. View Large Figure 3 View largeDownload slide Changes in the asymmetry index (ASIM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates an asymmetric muscular activity coincident with the side of the PCB. A dashed line indicates symmetric muscular activity. A dot-dash line indicates an asymmetric muscular activity not coincident with the side of the PCB. Figure 3 View largeDownload slide Changes in the asymmetry index (ASIM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates an asymmetric muscular activity coincident with the side of the PCB. A dashed line indicates symmetric muscular activity. A dot-dash line indicates an asymmetric muscular activity not coincident with the side of the PCB. SMI varied significantly across the time points (P = 0.040). It decreased immediately after the PCB correction (T1), indicating a greater asymmetry of the chewing pattern, and returned to values similar to the baseline at T2. SPM varied considerably across the time points in children with UPCB (Figure 4). Figure 4 View largeDownload slide Changes in the side of prevalence mastication index (SPM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates a prevalent side of mastication coincident with the side of the PCB. A dashed line indicates a symmetric mastication. A dot-dash line indicates a prevalent side of mastication not coincident with the side of the PCB. Figure 4 View largeDownload slide Changes in the side of prevalence mastication index (SPM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates a prevalent side of mastication coincident with the side of the PCB. A dashed line indicates a symmetric mastication. A dot-dash line indicates a prevalent side of mastication not coincident with the side of the PCB. FREQ did not differ significantly between the UPCB side and the no UPCB side (T0: UPCB side 1.6 ± 0.2 Hz; no UPCB side 1.6 ± 0.3 Hz—P=0.052; T1: UPCB side 1.5 ± 0.3 Hz; no UPCB side 1.5 ± 0.4 Hz—P = 0.773); T2: UPCB side 1.5 ± 0.3 Hz; no UPCB side 1.5 ± 0.2 Hz—P = 0.276) and between the time points (P = 0.255). Discussion The present study investigated whether individuals with UPCB have more asymmetric activity of the jaw muscles, and assessed whether the correction of UPCB contributes to more symmetric jaw muscle activity during standardized functional tasks. The findings of this study confirm the null hypotheses, that is patients with UPCB do not present more asymmetric AT and MM muscle activity as compared to UPCB-free controls, and that maxillary expansion does not determine a more symmetric activation of both AT and MM. In this study, an innovative EMG approach was used. This method, through the standardization of the EMG signals and normalizing the data as a percentage of the MVC effort on cotton rolls, reduces the biological noise, allows comparisons between subjects (10) and is widely used and validated in normal subjects and in patients with TMD (8, 10, 11, 24, 25). The data reveal that EMG indices (POC, TC, IMPACT and SMI) were similar between groups at baseline (T0). Also, the asymmetry of muscle contraction was not associated with the presence of UPCB (ASIM index and SPM index) both in static and dynamic tasks. This suggests that a crossbite does not contribute to more asymmetric activity of the masticatory muscles during functional tasks. Hence, all the indices used to assess the symmetry in the activity of masticatory muscles showed consistent results, reinforcing the concept that the presence of a UPCB in children is not associated with asymmetric muscular activity during both clenching and chewing. The mean indices (POC, TC and SMI) measured in the current study for both groups were lower than the mean values reported in literature for healthy adults (i.e. POC = 86.6, Tc = 91 and SMI = 79.2) (11–13, 24), suggesting that adolescents (our sample included individuals younger than 13 years old) may have slightly more asymmetric activity of the masticatory muscles than adults. Developmental changes in musculotendinous structures and jaw muscle compartments may account for this slight discrepancy. Indeed, the adaptation of jaw muscles to functional and non-functional demands may be dependent on dental development and diet, which differ substantially between children and adults (27). However, further studies are needed to address this point. Our data reveal that the EMG indices (POC, TC, IMPACT and SMI) were similar between groups at baseline (T0). Also, the asymmetric activity of muscles during both static and dynamic tasks was not associated with the presence of UPCB. This suggest that a UPCB does not contribute to more asymmetric activity of the masticatory muscles during functional tasks, and that a certain degree of asymmetric activation of jaw muscles during function has to be considered a physiological characteristic of the stomatognathic system (11–13). Our indices cannot be compared with other studies, since they were never used before in children. Nonetheless, many studies evaluating the contraction pattern of masticatory muscles of children with and without PCB by using conventional EMG assessments reported inconsistent data with questionable clinical relevance (15, 18, 20, 28, 29). Some studies concluded that children with UPCB have greater asymmetry in muscle activity than normocclusive children, finding differences of just 2 µV between groups (15); or found one statistical significant difference among several statistical tests (18); on the other hand some studies did not find any differences between the two groups (28, 29). Maxillary expansion did not significantly affect POC and TC indices. ASIM and SPM indices were highly variable across the time points. These results are in contrast with other studies analysing the effects of PCB correction on masticatory muscle activity (14–21). A systematic review summarizing the functional changes occurring after an early treatment of UPCB has recently suggested that orthodontic treatment of UPCB could improve both occlusal contact quality and occlusal stability (21). However, whether the correction of UPCB contributes to a more symmetric activation of jaw muscles during function is still questionable. Indeed, the increased symmetry of the muscle activity reported in some studies, which ranges between 20 and 50 µV (14–20), although statistically significant, must be considered of limited clinical relevance because of discrepancies in research designs, inclusion criteria (i.e. bilateral PCB or no functional shift) (16, 17, 19), treatment duration (15, 17–20), treatment protocol (15, 17, 18, 20) and EMG assessment (14–20). In spite of this, in our study the EMG records were performed only after the expansion phase, without the interference of any other appliances (braces, retention plate), and the follow up of the patients for just 6 months avoided any interference by the growth in the muscular function due to the brief period assessed (30). Finally, Di Palma et al. (31) used the same standardized indices in a group of 21 children with UPCB to evaluate the modifications of the RME on the AT and MM activity. They included only children that did not have an asymmetrical muscular activation and they found that 3 months after the correction achieved with the RME, patients did not show any significant change in the EMG activity. This study used a four bands hyrax that is more bulky than the two-band palatal expander used in our study, however, in the middle term there were not differences in the EMG activity due to the appliance design between the two studies. Immediately after UPCB correction (T1), IMPACT and SMI decreased significantly. The transient decrease in muscular recruitment (IMPACT) and the increased asymmetry during the chewing tasks (SMI) might be due to many factors, such as tooth soreness caused by the stimulation of the periodontium of the posterior teeth during expansion, the lack of adaptation of the neuromuscular system to the new occlusal condition, and the discomfort created by sudden changes in the maxilla-mandibular relationship (32). In fact, occlusal instability, modifications in dentition, and the repositioning of bones or skeletal configuration may cause transient effects on jaw muscles (33). The neuromuscular adaptation of the stomatognathic system to the new mandibular position does not occur immediately after treatment but only when a satisfactory occlusal engagement is achieved (18, 34, 35). Our data suggest that an asymmetric activation of the jaw muscles during functional tasks is an ordinary aspect in children. It must be stressed that all body segments present with a certain degree of asymmetry, which should be regarded as a physiological characteristic of each individual. Healthy subjects should not be expected to have a perfect symmetric activation of masticatory muscles, which is a man-made construct, during normal function (32). This was shown in several studies analysing healthy subjects without signs of dysfunction, in which the standardized indices POC and TC were never close to 100 per cent (11–13, 24). The aim of this study was testing the effect of cross bite with mandibular side shift on masticatory muscle asymmetry. This occlusal condition is characterized by a discrepancy between centric occlusion (CO) and centric relation (CR), which determines an asymmetrical position of the condyles in the glenoid fossa (36). Hence, in the current study, the clinical manoeuvre described by Dawson (23) was used to select study participants. This clinical manoeuvre is commonly used to distinguish between functional and morphologic crossbite, and to detect the CR position and the discrepancy between CO and CR. In this study, all participants had a posterior unilateral crossbite in CO but not CR, with a shift CR–CO. This study has a few limitations. First, most of the EMG indices were computed using the MVC. MVC is dependent on the participant’s compliance. Although all the participants were verbally encouraged during the experimental tasks, MVC values recorded may be slightly different across the time points. However, the RMS algorithm, used for the computation of the indices, analysed the 3 seconds of the test with the highest EMG amplitude, providing a normalized estimate of the MVC. Therefore, it may be assumed that variations of MVC across the conditions did not significantly affect the outcome measures. Second, in this study, the dental contacts were not recorded, although interferences between the upper and dental arches were reported to influence the EMG indices (37). Third, ASIM and SMI analysis were performed using adult normative values. This may raise questions concerning the validity of the analysis and the interpretation of the data. However, on the other hand there is no evidence suggesting that the threshold of muscular asymmetry is or should be different between adults and children. Conclusions In conclusion, the present study has shown that children with and without UPCB present slight asymmetric activity of AT and MM during functional tasks and these muscles of children with UPCB are not more asymmetric than healthy children without crossbite. Furthermore, the treatment of UPCB with RME does not reduce the asymmetry of MM and AT activity; hence, the symmetrization of the muscular activity cannot be an indication of maxillary expansion. Early treatment of UPCB by maxillary expansion should not be advocated to promote a more symmetric activation of the MM and AT in the short-medium term. Longitudinal studies with a long-term follow-up are still required to evaluate the long-term effects of the treatment. Conflict of Interest None to declare. References 1. 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For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The European Journal of Orthodontics Oxford University Press

Evaluation of masticatory muscle activity in patients with unilateral posterior crossbite before and after rapid maxillary expansion

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© The Author(s) 2018. Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: journals.permissions@oup.com
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Abstract

Summary Objectives The relationship between unilateral posterior crossbite (UPCB) and the possible asymmetric activation of the jaw muscles in children is still under debate. This study aimed at evaluating the jaw muscle activity of children with UPCB before and after rapid maxillary expansion (RME) by means of surface electromyography and a standardized sampling protocol. Subjects and methods Twenty-nine children with UPCB (UPCB-group, mean age 9.6 ± 1.6 years) and 40 UPCB-free controls (Control-group, 10.5 ± 1.1) were recruited. The activity of the left and right anterior temporalis (AT) and superficial masseter muscles (MM) was recorded during maximum voluntary clenching and a chewing task (T0). In the UPCB-group, data were collected, also, after the correction of the UPCB with RME (T1) and 6 months later (T2), without any further treatment. Electromyographic indices comparing the activity of paired muscle were computed via software to estimate the extent of asymmetric AT and MM activity. Paired and unpaired t-test or Wilcoxon-signed rank and Mann–Whitney U test, ANOVA or Friedman test and chi-squared test were used in the statistical analysis. Results Both groups presented with asymmetric activity of the muscles, which did not differ between groups (T0, all P > 0.05). The treatment determined a decrease in muscular activity (T1, P = 0.040), and a more asymmetric pattern of muscle activation during chewing (T1, P = 0.040), which returned similar to baseline values at T2 (all P > 0.05). Conclusions UPCB does not contribute to an asymmetric activation of AT and MM during functional tasks. The treatment of UPCB by RME did not determine a more symmetric activity of the assessed muscles. Introduction Posterior crossbite (PCB) is a common malocclusion, which affects 8–22 per cent of orthodontic patients in the primary and early mixed dentition (1) and 5–15 per cent of the general population (2). Unilateral posterior crossbite (UPCB) with a functional shift of the mandible occurs in 71–84 per cent of individuals with PCB (3). UPCB has been suggested to determine an asymmetrical activation of the masticatory muscles and therefore might contribute to the onset of skeletal asymmetries and temporomandibular joint disorders (TMD) (4–6). Based on these assumptions, early treatment of UPCB by maxillary expansion (7–9) is commonly recommended to reduce the risk of developing craniofacial anomalies and TMD in adulthood (4, 5). The activity of muscles is commonly investigated in research settings by using surface electromyography (sEMG). Nonetheless, electromyographic (EMG) data can be affected by several artefacts, which could account for a problematic data analysis and interpretation (10). The introduction of standardized EMG protocols and indices to assess the activity of paired masticatory muscles has allowed for more reliable analyses (11–13). Ferrario et al. (12) developed a method for standardizing myoelectric potentials, which computes indices depicting the activation of elevator muscles and the extent of symmetric activation between paired muscles during specific functional tasks. This method reduces the intra-sample variability and can be used for the assessment of jaw muscle activity during both static and dynamic tasks (12, 13). The effects of the correction of UPCB on the activity of anterior temporalis (AT) and superficial masseter (MM) muscles have been evaluated using sEMG, with controversial findings (14–20). One study (18) concluded that the degree of asymmetry of masticatory muscles during function is not affected by the presence of crossbite. Others reported that the treatment of crossbite contributes to a more symmetric pattern of activation of the chewing muscles during function only to a slight extent (15, 20). Finally, findings included in other reports may be questionable since they lack of untreated subjected acting as controls (17, 19). A recent review has reported that the treatment of crossbite contributes to increasing the activity of masticatory muscles, approaching levels similar to subjects with normal occlusion (21). Differently from other studies, this research has investigated the relationship between crossbite and asymmetry in the activity of the chewing muscles by using a standardized EMG protocol and indices. This method allows for a more precise and objective assessment of the muscle function and overcomes the limits of classical approaches using surface EMG (e.g. EMG cross-talk, artefacts, changes into the signal due to the location of the electrodes). The protocol of this study used standardized EMG potentials, which allow for more accurate intragroup and between group comparisons. In addition, the use of indices of asymmetry instead of values of electric potentials (microvolt) provides clinicians with more relevant and intelligible clinical information. The relationship between crossbite and asymmetric jaw muscle activity has been subject of debate in several studies. An early treatment of crossbite is commonly recommended to reduce the risk of developing skeletal asymmetries as a consequence of abnormalities in masticatory function between the right and left sides. A better understanding of both the possible relationship between UPCB and asymmetric muscular function and the effect of RPE on the extent of muscular asymmetry during function might contribute to clarifying whether an early treatment of UPCB with RPE should be recommended. This study aimed at evaluating the AT and MM muscle activity of children with UPCB before and after RME by means of sEMG and a standardized EMG sampling protocol. The null hypotheses to be tested were: the UPCB patients do not present more asymmetric AT and MM muscle activity compared to UPCB-free controls during standardized tasks; and maxillary expansion does not determine a more symmetric activation of AT and MM muscles during functional tasks. Materials and methods Study sample Twenty-nine children with UPCB (UPCB-group: 13 males, 16 females, mean age ± SD = 9.6 ± 1.6 years) and 40 UPCB-free controls (Control-group: 17 males, 23 females; mean age 10.5 ± 1.1 years) seeking an orthodontic consultation were recruited consecutively. For both groups, exclusion criteria were genetic or congenital abnormalities, craniofacial anomalies, systemic diseases affecting growth and development, clinical signs or symptoms of TMD (22), reporting of oral parafunctions (22), and previous or current orthodontic treatment. Inclusion criteria were an Angle Class I relationship, presence of the four first permanent molars, mixed dentition stage, and the absence of tooth mobility or decayed teeth. The experimental group included subjects with UPCB and lateral shift towards the UPCB side as assessed by Dawson’s manoeuvre (23). The control group included subjects without UPCB. Parents or guardians received information about the research protocol and signed an informed consent. The research protocol was designed in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans and was reviewed and approved by the Research Ethics Board (protocol 22616). EMG assessment The electrical activity of the right and left AT and MM muscles was recorded simultaneously during standardized tasks via sEMG. Silver-silver chloride bipolar surface pre-gelled electrodes (Kendall, Mansfield, MA, USA) with a diameter of 24 mm were placed on the skin along the main direction of the muscular fibres according to the protocol described by Ferrario et al. (12). To minimize electrode impedance, the skin was thoroughly cleaned with an abrasive preparation gel (Everi, Spes Medica, Genova, Italy) before electrode placement. Recordings were performed at least 5–6 minutes after the application of the electrode to allow the conductive gel to adequately moisten the skin surface. All participants sat in a dental chair. The position of the seatback was fixed, while the vertical excursion of the dental chair could be adjusted by the operator. The study was performed using a wireless EMG device (TMJOINT, BTS SpA, Garbagnate Milanese, Italy). The EMG signals were acquired at 1KHZ, amplified (gain 150) and filtered via hardware (low-pass filter 500Hz; high-pass 10Hz). A software program (Dental Contact Analyser, BTS SpA) processed the raw electrical signals and generated root mean square (RMS) values. Thereafter, RMS values were processed by an algorithm to generate indices of muscle activity and asymmetry. The EMG protocol included two static and two dynamic tests. All participants received standardized instructions about the research protocol. The EMG protocol and the algorithm used for the standardization of the EMG signals and the computation of the indices have been used and described in several research studies (11–13, 24). The static tests included the following: 1. Maximum voluntary contraction (MVC) in intercuspal position (CLENCH)—participants clenched their teeth as hard as possible for 5 seconds; 2. MVC in intercuspal position on cotton rolls (COT)—participants clenched as hard as possible for 5 seconds on 10 mm thick cotton rolls (Intermedical, Terlano, Bolzano, Italy) positioned from the mandibular first molar to the canine on both sides. For the 5-second static tests, two hundred 25 msec RMS samples were collected. The 120 samples, corresponding to 3 second, with the highest RMS values were used to compute the indices. The EMG waves of each muscle (120 samples) with and without cotton rolls were superimposed sample by sample, and the ratio between the superimposed areas and the total areas was computed automatically via software. Hence, for each subject, the EMG potentials recorded during the MVC were expressed as percentage of the mean RMS potential recorded during the MVC on the cotton rolls (EMG standardized potentials). The dynamic tests included the following: 1. Chewing gum (Air Action Vigorsol, Lainate, Italy) on the right side for 15 seconds. 2. Chewing on the left side for 15 seconds. Between the static and the dynamic tests, participants were asked to rest for 3 minutes. The following standardized EMG indices were calculated via software: Computed indices (static tests) 1. POC (percentage of overlapping coefficient). The standardized EMG waves of the left and right AT and MM were compared by computing a percentage overlapping coefficient (POC, unit: %, range: 0–100 per cent, norm values 85 per cent ≤ POC ≤ 100 per cent) (11, 13, 24). If the muscles contract with perfect symmetry, a POC of 100 per cent (perfect symmetry) is expected. Conversely, a value corresponding to 0 per cent indicates the absence of concurrent activation of paired muscles (no symmetry). Three indices were computed for each subject (POC AT, POC MM and POC medium). 2. TC (torque coefficient). This index is obtained by measuring the overlapping activity (standardized EMG waves) between the left MM and right AT and the right MM and left AT. The higher muscular activity of one couple (i.e. left MM and right AT) over the other (i.e. right MM and left AT) results in a torquing effect on the lower jaw. TC ranges between 0 per cent (no symmetric activation of the couples, greatest torquing effect) and 100 per cent (perfect symmetric activation of the couples, no torquing effect). Normal values are 90 per cent ≤ TC ≤ 100 per cent (12, 13, 24). 3. IMPACT (total standardized muscle activity). This index is computed as the integrated area of the EMG standardized potentials of both MM and AT over time (5 seconds MVC). Norm values are 85 per cent ≤ IC ≤ 115 per cent (12). Lower values indicate that the EMG standardized potentials were reduced during the clenching tasks, and that the maximal EMG activity could not be expressed. 4. ASIM (asymmetry index). This index is calculated by comparing the activity of the right couple (right AT and right MM) to the left couple (left AT and left MM). ASIM ranges from −100 per cent and +100 per cent; a value of 0 per cent depicts a perfect symmetric activation of the two couples. A negative value indicates greater activity of the left couple; conversely, a positive value indicates a greater activity of the right couple. Norm values are −10 per cent ≤ ASIM ≤ +10 per cent (25). Computed indices (dynamic tests) 1. SMI (symmetrical mastication index) was computed to assess whether the left- and the right-side chewing tests were performed with symmetrical muscular patterns. It indicates the distance between the centre of the chart and the centre of the ellipse in a graph that describes the prevalence of one side over the other during mastication (Figure 1). SMI ranges between 0 per cent (no symmetry) and 100 per cent (symmetrical muscular pattern). Normal values are 70 per cent ≤ SMI ≤ 100 per cent (11). 2. SPM (side of prevalent mastication) in case of SMI values lower than 70 per cent, the dominant side of mastication was identified as side of prevalent mastication (Figure 1). Three categories could be identified, that is right, left and symmetric. 3. FREQ (frequency index) measures the frequency of masticatory cycles during the chewing experimental tasks and was reported in hertz (Hz: bites per second). Figure 1 View largeDownload slide Determination of the symmetrical mastication index (SMI). x-axis: differential masseter (left (-) versus right); y-axis: differential temporal (left (-) versus right) (µV). Red dots and the corresponding ellipse depict data recorded during the task ‘chewing on the left side’. Blue dots and the corresponding ellipse depict data recorded during the task ‘chewing on the right side’. In an ideal condition (complete symmetric activity between right and left sides during chewing), the centre of the ellipse describing the task ‘chewing on the right side’ will be located in the first quadrant (top left) and the centre of the ellipse describing the task ‘chewing on the left side’ in the third quadrant (bottom right). The symmetrical mastication index (SMI, %) is calculated using the distance between the centres of the two confidence ellipses and the origin of the axes. If the right and left chewing tasks are symmetric, the right and left ellipses will have the same distance from the origin of the axes, and a 180 degree difference between phase angles (angle between the x-axis and the segment connecting the centre of the ellipse and the axis origin). Symmetric patient (A). Similar distances between the system origin and the centre of the ellipse, and similar phase angle between the two tasks. Asymmetric patient (B). The blue ellipse has a bigger distance respect to the centre and the difference between the angles is lower than 180 degree. Figure 1 View largeDownload slide Determination of the symmetrical mastication index (SMI). x-axis: differential masseter (left (-) versus right); y-axis: differential temporal (left (-) versus right) (µV). Red dots and the corresponding ellipse depict data recorded during the task ‘chewing on the left side’. Blue dots and the corresponding ellipse depict data recorded during the task ‘chewing on the right side’. In an ideal condition (complete symmetric activity between right and left sides during chewing), the centre of the ellipse describing the task ‘chewing on the right side’ will be located in the first quadrant (top left) and the centre of the ellipse describing the task ‘chewing on the left side’ in the third quadrant (bottom right). The symmetrical mastication index (SMI, %) is calculated using the distance between the centres of the two confidence ellipses and the origin of the axes. If the right and left chewing tasks are symmetric, the right and left ellipses will have the same distance from the origin of the axes, and a 180 degree difference between phase angles (angle between the x-axis and the segment connecting the centre of the ellipse and the axis origin). Symmetric patient (A). Similar distances between the system origin and the centre of the ellipse, and similar phase angle between the two tasks. Asymmetric patient (B). The blue ellipse has a bigger distance respect to the centre and the difference between the angles is lower than 180 degree. Rapid maxillary expansion All subjects of the UPCB group were treated with a two-band palatal expander and rapid maxillary expansion (RME, Figure 2) (26). The appliance was banded to the maxillary first permanent molars and placed using glass ionometer cement (Multi-Cure Glass ionomer Cement; Unitek, Monrovia, CA, USA). The screw was initially turned eight times (2.0 mm) at chair side 2 hours after curing. Thereafter, the patients’ parents were trained to turn the screw three times per day (0.75 mm). During the expansion phase, subjects were monitored once a week. The screw was activated until a 2-mm molar transverse overcorrection was achieved. After the active expansion phase, the screw was locked with light-cure flow composite resin (Premise Flowable; Kerr Corporation, Orange, CA, USA). The active treatment (expansion) ranged between 10 and 16 days. The patients wore the appliance as fixed retainer for 6 months. Figure 2 View largeDownload slide Two-band palatal expander at the end of the expansion phase. Figure 2 View largeDownload slide Two-band palatal expander at the end of the expansion phase. Data collection The EMG activity of the AT and MM of both sides (left end right) was recorded at baseline after recruitment (T0) for both the UPCB and Control-group. For the UPCB group, EMG activity was recorded also when the UPCB was corrected (T1), and 6 months after when the appliance was removed (T2). EMG indices for both static and dynamic tests were computed at each time point. Sample size calculation and statistical analysis A sample size calculation was performed before recruitment. The primary outcome measure of this study was the POC medium index. Based on a previous investigation (12), it was assumed that a difference in POC medium values of 5 per cent (SD = 4.55 per cent) between the UPCB and the Control-group could be considered of clinical relevance. A sample including 21 subjects per group was sufficient to detect between-group differences in POC medium (α = 0.05 and 1 − β = 0.9). The Shapiro–Wilk test was used to check whether data were normally distributed. Mean and standard deviation (SD) for data distributed normally, and median with first and third interquartile range for data not normally distributed were calculated. Between-group differences in standardized EMG indices, except ASIM and SPM, were tested by means of an unpaired t-test or Mann–Whitney U test for between-group comparisons. Repeated measures ANOVA or the Friedman test was used to test the effect of orthodontic treatment on EMG indices (POC AT, POC MM, Tc, IMPACT, SMI) and to detect differences between the time points in the UPCB group. The post hoc Tukey’s test with Bonferroni’s correction or the Wilcoxon signed-rank test was used. For FREQ, the differences between the crossbite side minus the non-crossbite side, in the UPCB group, and between the right side minus the left side in the Control-group, were calculated. This variable, normally distributed, was analyzed for each group and for each time point by means of a paired t-test for within-group comparisons and by means of an unpaired t-test for between-group comparisons. ASIM and SPM were reported as frequencies. ASIM and SPM values were used to categorize participants in two groups (symmetric and asymmetric) based on normative values (symmetric: −10 per cent ≤ ASIM ≤ +10 per cent; asymmetric: ASIM ≥ +10 per cent or ASIM ≤ −10 per cent; symmetric: SPM > 70 per cent; asymmetric: SPM < 70 per cent). A chi-squared test was performed to examine whether the distribution of ASIM and SPM categories was similar between the study groups. Moreover, for patients that showed symmetrical jaw muscle activity, the prevalent side was recorded, and a chi-squared test was done to assess whether there was an association between the side of prevalent muscular activity and the side of the UPCB (UPCB group) at both T0 and T2. Standard statistical software package (SPSS version 22.0, SPSS IBM, Armonk, NY, USA) was used for statistical analysis. Results EMG indices at baseline: within-group and between-group comparisons All the indices of the static tests (POC, TC, IMPACT) did not differ between groups at T0 (Table 1). Based on the assessment of ASIM values, 20 out of 29 patients from the UPCB group and 29 out of 40 individuals presented symmetric EMG activity. The ASIM index was not associated with the presence of UPCB (P = 0.749). Table 1 Standardized EMG indices of control and UPCB group at T0. Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Values are expressed in %, mean and standard deviation (SD), for data distributed normally and median with first and third interquartile for data not distributed normally. View Large Table 1 Standardized EMG indices of control and UPCB group at T0. Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Index Control group UPCB group P value POC AT 82.0 (9.3) 84.7 (5.9) 0.395 POC MM 84.5 (7.8) 83.0 (7.4) 0.092 POC medium 83.3 (7.7) 83.9 (4.9) 0.551 TC 88.3 (6.2) 88.3 (6.2) 0.738 IMPACT 117.5 (89.5;152.5) 118.0 (102.0;146.0) 0.851 SMI 67.8 (22.8) 71.7 (17.4) 0.734 Values are expressed in %, mean and standard deviation (SD), for data distributed normally and median with first and third interquartile for data not distributed normally. View Large During the chewing tasks, SMI did not differ between the two groups (Table 1); moreover, 19 out of 29 patients in the UPCB group and 25 out of 40 individuals had a side of prevalent mastication (SPM). The chi-square test showed that SPM was independent from the presence of the UPCB (P = 0.736). Finally, FREQ (T0) was not different both between sides (UPCB: UPCB side 1.6 ± 0.2 Hz; no UPCB side 1.6 ± 0.3 Hz—P=0.052; Control-group: Right 1.4 ± 0.3 Hz; Left 1.5 ± 0.3 Hz—P = 0.072) and between groups (P = 0.614). EMG indices in the UPCB group before and after orthodontic treatment (T0–T2) POC and TC values did not change significantly throughout the three time points of the study (All P > 0.05; Table 2). IMPACT changed significantly with time (P = 0.040); it decreased at T1 (P = 0.007), and returned to baseline values at T2 (P = 0.424). The ASIM categories varied considerably over the three time points (Figure 3). Table 2 Standardized EMG indices of UPCB group at T0, T1 and T2. Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Values are expressed in %, mean and standard deviation (SD) (for data distributed normally) and median with first and third interquartile (for data not distributed normally) are reported. Bold text indicates statistically significant differences between time points. Post hoc tests with Bonferroni’s correction was used. View Large Table 2 Standardized EMG indices of UPCB group at T0, T1 and T2. Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Index T0 T1 T2 P value T0 versus T1 T1 versus T2 T0 versus T2 POC AT 84.7 (5.9) 83.2 (5.5) 83.6 (10) 0.666 POC MM 83.0 (7.4) 82.4 (10.2) 84.9 (5.6) 0.311 POC medium 83.9 (4.9) 82.6 (6.6) 84.4 (5.3) 0.323 TC 88.3 (6.2) 88 (5.0) 87.3 (6.8) 0.726 IMPACT 118.0 (102.0; 146.0) 97.0 (71.0; 121.0) 122.3 (97.0; 124.0) 0.040 0.007 0.036 0.424 SMI 71.7 (17.4) 59.4 (20.2) 67.1 (20.8) 0.040 0.027 1 0.432 Values are expressed in %, mean and standard deviation (SD) (for data distributed normally) and median with first and third interquartile (for data not distributed normally) are reported. Bold text indicates statistically significant differences between time points. Post hoc tests with Bonferroni’s correction was used. View Large Figure 3 View largeDownload slide Changes in the asymmetry index (ASIM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates an asymmetric muscular activity coincident with the side of the PCB. A dashed line indicates symmetric muscular activity. A dot-dash line indicates an asymmetric muscular activity not coincident with the side of the PCB. Figure 3 View largeDownload slide Changes in the asymmetry index (ASIM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates an asymmetric muscular activity coincident with the side of the PCB. A dashed line indicates symmetric muscular activity. A dot-dash line indicates an asymmetric muscular activity not coincident with the side of the PCB. SMI varied significantly across the time points (P = 0.040). It decreased immediately after the PCB correction (T1), indicating a greater asymmetry of the chewing pattern, and returned to values similar to the baseline at T2. SPM varied considerably across the time points in children with UPCB (Figure 4). Figure 4 View largeDownload slide Changes in the side of prevalence mastication index (SPM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates a prevalent side of mastication coincident with the side of the PCB. A dashed line indicates a symmetric mastication. A dot-dash line indicates a prevalent side of mastication not coincident with the side of the PCB. Figure 4 View largeDownload slide Changes in the side of prevalence mastication index (SPM) 6 months after UPCB correction (T2). The numbers of subjects are reported. A solid line indicates a prevalent side of mastication coincident with the side of the PCB. A dashed line indicates a symmetric mastication. A dot-dash line indicates a prevalent side of mastication not coincident with the side of the PCB. FREQ did not differ significantly between the UPCB side and the no UPCB side (T0: UPCB side 1.6 ± 0.2 Hz; no UPCB side 1.6 ± 0.3 Hz—P=0.052; T1: UPCB side 1.5 ± 0.3 Hz; no UPCB side 1.5 ± 0.4 Hz—P = 0.773); T2: UPCB side 1.5 ± 0.3 Hz; no UPCB side 1.5 ± 0.2 Hz—P = 0.276) and between the time points (P = 0.255). Discussion The present study investigated whether individuals with UPCB have more asymmetric activity of the jaw muscles, and assessed whether the correction of UPCB contributes to more symmetric jaw muscle activity during standardized functional tasks. The findings of this study confirm the null hypotheses, that is patients with UPCB do not present more asymmetric AT and MM muscle activity as compared to UPCB-free controls, and that maxillary expansion does not determine a more symmetric activation of both AT and MM. In this study, an innovative EMG approach was used. This method, through the standardization of the EMG signals and normalizing the data as a percentage of the MVC effort on cotton rolls, reduces the biological noise, allows comparisons between subjects (10) and is widely used and validated in normal subjects and in patients with TMD (8, 10, 11, 24, 25). The data reveal that EMG indices (POC, TC, IMPACT and SMI) were similar between groups at baseline (T0). Also, the asymmetry of muscle contraction was not associated with the presence of UPCB (ASIM index and SPM index) both in static and dynamic tasks. This suggests that a crossbite does not contribute to more asymmetric activity of the masticatory muscles during functional tasks. Hence, all the indices used to assess the symmetry in the activity of masticatory muscles showed consistent results, reinforcing the concept that the presence of a UPCB in children is not associated with asymmetric muscular activity during both clenching and chewing. The mean indices (POC, TC and SMI) measured in the current study for both groups were lower than the mean values reported in literature for healthy adults (i.e. POC = 86.6, Tc = 91 and SMI = 79.2) (11–13, 24), suggesting that adolescents (our sample included individuals younger than 13 years old) may have slightly more asymmetric activity of the masticatory muscles than adults. Developmental changes in musculotendinous structures and jaw muscle compartments may account for this slight discrepancy. Indeed, the adaptation of jaw muscles to functional and non-functional demands may be dependent on dental development and diet, which differ substantially between children and adults (27). However, further studies are needed to address this point. Our data reveal that the EMG indices (POC, TC, IMPACT and SMI) were similar between groups at baseline (T0). Also, the asymmetric activity of muscles during both static and dynamic tasks was not associated with the presence of UPCB. This suggest that a UPCB does not contribute to more asymmetric activity of the masticatory muscles during functional tasks, and that a certain degree of asymmetric activation of jaw muscles during function has to be considered a physiological characteristic of the stomatognathic system (11–13). Our indices cannot be compared with other studies, since they were never used before in children. Nonetheless, many studies evaluating the contraction pattern of masticatory muscles of children with and without PCB by using conventional EMG assessments reported inconsistent data with questionable clinical relevance (15, 18, 20, 28, 29). Some studies concluded that children with UPCB have greater asymmetry in muscle activity than normocclusive children, finding differences of just 2 µV between groups (15); or found one statistical significant difference among several statistical tests (18); on the other hand some studies did not find any differences between the two groups (28, 29). Maxillary expansion did not significantly affect POC and TC indices. ASIM and SPM indices were highly variable across the time points. These results are in contrast with other studies analysing the effects of PCB correction on masticatory muscle activity (14–21). A systematic review summarizing the functional changes occurring after an early treatment of UPCB has recently suggested that orthodontic treatment of UPCB could improve both occlusal contact quality and occlusal stability (21). However, whether the correction of UPCB contributes to a more symmetric activation of jaw muscles during function is still questionable. Indeed, the increased symmetry of the muscle activity reported in some studies, which ranges between 20 and 50 µV (14–20), although statistically significant, must be considered of limited clinical relevance because of discrepancies in research designs, inclusion criteria (i.e. bilateral PCB or no functional shift) (16, 17, 19), treatment duration (15, 17–20), treatment protocol (15, 17, 18, 20) and EMG assessment (14–20). In spite of this, in our study the EMG records were performed only after the expansion phase, without the interference of any other appliances (braces, retention plate), and the follow up of the patients for just 6 months avoided any interference by the growth in the muscular function due to the brief period assessed (30). Finally, Di Palma et al. (31) used the same standardized indices in a group of 21 children with UPCB to evaluate the modifications of the RME on the AT and MM activity. They included only children that did not have an asymmetrical muscular activation and they found that 3 months after the correction achieved with the RME, patients did not show any significant change in the EMG activity. This study used a four bands hyrax that is more bulky than the two-band palatal expander used in our study, however, in the middle term there were not differences in the EMG activity due to the appliance design between the two studies. Immediately after UPCB correction (T1), IMPACT and SMI decreased significantly. The transient decrease in muscular recruitment (IMPACT) and the increased asymmetry during the chewing tasks (SMI) might be due to many factors, such as tooth soreness caused by the stimulation of the periodontium of the posterior teeth during expansion, the lack of adaptation of the neuromuscular system to the new occlusal condition, and the discomfort created by sudden changes in the maxilla-mandibular relationship (32). In fact, occlusal instability, modifications in dentition, and the repositioning of bones or skeletal configuration may cause transient effects on jaw muscles (33). The neuromuscular adaptation of the stomatognathic system to the new mandibular position does not occur immediately after treatment but only when a satisfactory occlusal engagement is achieved (18, 34, 35). Our data suggest that an asymmetric activation of the jaw muscles during functional tasks is an ordinary aspect in children. It must be stressed that all body segments present with a certain degree of asymmetry, which should be regarded as a physiological characteristic of each individual. Healthy subjects should not be expected to have a perfect symmetric activation of masticatory muscles, which is a man-made construct, during normal function (32). This was shown in several studies analysing healthy subjects without signs of dysfunction, in which the standardized indices POC and TC were never close to 100 per cent (11–13, 24). The aim of this study was testing the effect of cross bite with mandibular side shift on masticatory muscle asymmetry. This occlusal condition is characterized by a discrepancy between centric occlusion (CO) and centric relation (CR), which determines an asymmetrical position of the condyles in the glenoid fossa (36). Hence, in the current study, the clinical manoeuvre described by Dawson (23) was used to select study participants. This clinical manoeuvre is commonly used to distinguish between functional and morphologic crossbite, and to detect the CR position and the discrepancy between CO and CR. In this study, all participants had a posterior unilateral crossbite in CO but not CR, with a shift CR–CO. This study has a few limitations. First, most of the EMG indices were computed using the MVC. MVC is dependent on the participant’s compliance. Although all the participants were verbally encouraged during the experimental tasks, MVC values recorded may be slightly different across the time points. However, the RMS algorithm, used for the computation of the indices, analysed the 3 seconds of the test with the highest EMG amplitude, providing a normalized estimate of the MVC. Therefore, it may be assumed that variations of MVC across the conditions did not significantly affect the outcome measures. Second, in this study, the dental contacts were not recorded, although interferences between the upper and dental arches were reported to influence the EMG indices (37). Third, ASIM and SMI analysis were performed using adult normative values. This may raise questions concerning the validity of the analysis and the interpretation of the data. However, on the other hand there is no evidence suggesting that the threshold of muscular asymmetry is or should be different between adults and children. Conclusions In conclusion, the present study has shown that children with and without UPCB present slight asymmetric activity of AT and MM during functional tasks and these muscles of children with UPCB are not more asymmetric than healthy children without crossbite. Furthermore, the treatment of UPCB with RME does not reduce the asymmetry of MM and AT activity; hence, the symmetrization of the muscular activity cannot be an indication of maxillary expansion. Early treatment of UPCB by maxillary expansion should not be advocated to promote a more symmetric activation of the MM and AT in the short-medium term. Longitudinal studies with a long-term follow-up are still required to evaluate the long-term effects of the treatment. Conflict of Interest None to declare. References 1. 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The European Journal of OrthodonticsOxford University Press

Published: Apr 23, 2018

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