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Effect of unilateral posterior crossbite on the electromyographic activity of human masticatory muscles
ORIGINAL ARTICLE Effect of unilateral posterior crossbite on the electromyographic activity of human masticatory muscles José Antonio Alarcón, DDS, PhD,a Conchita Martín, DDS, PhD,b and Juan Carlos Palma, MD, PhDc Madrid, Spain Studies dealing with the electromyographic activity of masticatory muscles in patients with unilateral posterior crossbite are infrequent. The purpose of this study was to assess the electromyographic pattern of masticatory muscles at rest position, during swallowing, and during mastication, in 30 subjects with right posterior crossbite and to compare them to 30 normocclusive subjects. The 2 groups were matched according to age, gender, skeletal Class I, and mesofacial growth pattern. Electromyographic activity of right and left anterior temporalis, posterior temporalis, masseter, and anterior digastric muscles was recorded at rest position, while swallowing water, and while chewing. Disposable bipolar surface electrodes were used in both groups. Data were compared between groups and between right and left sides within each group. The results revealed that the posterior temporalis of the non–crossbite side was more active than that of the same side in subjects with crossbite at rest position and during swallowing. The activity of both anterior digastrics was higher in the crossbite subjects during swallowing. During chewing the right masseter muscle was less active in the crossbite patients than in normocclusive subjects. The results obtained during chewing indicate a bilateral masticatory pattern in both groups. (Am J Orthod Dentofacial Orthop 2000;118:328-34)
he neuromuscular characteristics associated with unilateral posterior crossbite (UPCB) have not been extensively studied. From a therapeutic point of view, this malocclusion does not correct spontaneously and generally persists through adulthood.1,2 Several deleterious effects have been linked to UPCB. It may cause occlusal interferences as a result of the inadequate relationship between both dental arches.3,4 Skeletally, crossbites with lateral shift influence the normal growth of the mandible.5-9 Another consequence of an untreated UPCB is the likely asymmetry in the condylar position and trajectories, with a displacement of the ipsilateral condyle toward the crossbite side10-12 and an increased growth of the contralateral condyle.13 The intimate mechanism that links the lateral shift of the mandible with the condylar growth remains unclear, but it seems that the main cause could be abnormal muscular activity.3,10,14,15 There is a certain degree of asymmetric muscle activity. Troelstrup and Möller16,17 found that the posterior temporalis of the same side of the crossbite showed higher electromyographic (EMG) activity than the contralateral muscle at rest and during maximum
T
From the Faculty of Odontology, University Complutense, Madrid, Spain. aAssociate Professor of Orthodontic. bAssociate Professor of Orthodontic, University Complutense, Madrid, Spain. cProfessor of Orthodontics. Reprint requests to: Conchita Martín. C/Bola del Mundo, 38 28023 Madrid, Spain; e-mail, [email protected]. Submitted April 1999; Revised and accepted September 1999. Copyright © 2000 by the American Association of Orthodontists. 0889-5406/2000/$12.00 + 0 8/1/103252 doi:10.1067/mod.2000.103252
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clenching, whereas the ipsilateral anterior temporalis was less active than the contralateral muscle at rest. Ingervall and Thilander18 found a certain degree of asymmetry in the activity of masticatory muscles in 19 children with laterally forced bite (16 of them had unilateral crossbite). The posterior temporalis on the forced bite side was more active at rest, during chewing, and at maximal bite than that of the nonforced bite side, whereas the anterior temporalis on the forced bite side was more active during chewing than that of the nonforced bite side. The purpose of this study was to assess the EMG pattern of masticatory muscles at rest position, during swallowing, and during mastication, in children with unilateral posterior crossbite and to compare this pattern with the one obtained in normocclusive children. The knowledge of the behavior of masticatory muscles in this malocclusion could help its diagnosis and management. SUBJECTS AND METHODS Patient Population
The study population consisted of a consecutive sample of 60 white subjects from the Children’s Department of the Faculty of Odontology of University Complutense, Madrid (Spain), divided into 2 groups: a control group of 30 normocclusive subjects (16 girls and 14 boys; mean age, 12 years 5 months) and an experimental group of 30 subjects (17 girls and 13 boys; mean age, 12 years 2 months) with right posterior crossbite of at least the first molar. The following criteria were used in the selection of
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the 2 groups: age between 10 and 14 years; skeletal Class I malocclusion according to ANB angle, convexity, and Wits appraisal; and mesofacial growth pattern according to Frankfort horizontal-to-mandibular plane angle. Subjects were excluded if they had clinical signs or symptoms of temporomandibular joint dysfunction, skeletal asymmetry, previous or current orthodontic treatment, extensive restorations, cast restorations or cuspal coverage, pathologic periodontal condition, or missing teeth. All subjects received full explanations of the aims and design of the study before its start and agreed to participate by signing an informed consent. Recording of Muscular Activity
Simultaneous bilateral (left, and right) surface electromyographs of anterior temporalis (AT), posterior temporalis (PT), masseter (MM), and anterior digastric (AD) muscles were recorded at rest (mandibular postural position), during swallowing, and during chewing. EMG measurements were recorded with an 8-channel electromyograph (EM2) interfaced with an IBM PC computer (Myo-Tronics, Seattle, Wash). This system allows 8 muscles to be monitored without interfering with the functional activity of the subjects. Disposable silver chloride bipolar surface electrodes (Duo-Trode, Myo-Tronics Inc) were prepositioned on the muscular bellies parallel with the muscular fibers according to the following protocol (Ferrario et al19 and Jankelson20): MM The operator stood behind the patient and palpated the muscle while asking the patient to clench in habitual occlusion. Electrodes were placed over an oblique line connecting the patient´s eye and his or her mandibular angle, about 3 cm above and in front of the gonial angle. AT The muscle was palpated asking the patient to clench in habitual occlusion. Electrodes were placed vertically over the anterior border of the muscle, on the area corresponding to the frontoparietal suture. PT The operator asked the patient to place the tongue against the palate and to press. The electrode was placed almost horizontally parallel to the posterosuperior border of the ear. AD With the patient pressing the tongue against the palate, the electrode was placed under the chin parallel to the mandibular body over the suprahyoid triangle. The ground electrode was a disk-type electrode (Duo-trode, Myo-Tronics Inc) placed on the side surface of the neck. In order to minimize electrode impedance, the recording sites were thoroughly cleansed with a piece of cotton soaked in 70% alcohol. Recordings were performed at least 5 minutes after application of
the electrode to allow the conductive paste to adequately moisten the skin surface. EMG activity was recorded at rest position, during swallowing, and during chewing, using the following protocol: Rest (mandibular rest position without occlusal contact). To obtain this resting position patients were asked to moisten the lips, to swallow saliva, to breath deeply and to relax their jaws with closed eyes. Average EMG activity (µV) was obtained with a calibration of 30 µV. Swallowing. Muscular activity was registered during the intake of water. Subjects were instructed to take a mouthful of water and to hold their jaws at rest position. They were then instructed to swallow the water and, after swallowing, to hold their jaws at rest position again. The peak (maximum amplitude, µV) was obtained with a calibration of 30 µV, allowing a resting period of 1 minute between each swallowing. Chewing. Muscular activity was registered during mastication of chips. The operator just asked the subject to eat chips without further instructions. The EMG activity was then recorded for the last 10 seconds of the chewing. Average EMG activity (µV) was obtained with a calibration of 30 µV. There was a quiet, dark, and comfortable atmosphere during the experiment. Verbal instructions were given to the patients before starting in order to avoid any stressful situation, and several trial tests were made to instruct the patient. Irregular or spurious tracings were omitted, and the measurements repeated. For continuity, one calibrated examiner performed all EMG measurements in a “blind to status” manner. The examiner was blind to the presence of posterior crossbite. Collected data remained blind to status throughout analysis by assigning each subject a code number. Therefore, the true status of the subjects was not revealed until the data had been compiled in order to decrease the possibility of bias at any stage in the study. Reproducibility of the EMG Data
In order to evaluate the reproducibility of the EMG records, the results of different consecutive measurements were compared. The rest position test was reproduced starting with electrode placement. Four trials were performed in 5 subjects over 4 days according to experimental protocol. The data from the first day were compared with those of the other 3 days for statistical significance with the Student t variable test. Statistical Analysis
Means and standard deviations were calculated for the EMG values in the 3 tests. Data were compared between groups and between right and left sides within
330 Alarcón, Martín, and Palma
Table I. Comparison
American Journal of Orthodontics and Dentofacial Orthopedics September 2000
of EMG data (µV) taken 4 successive days for rest position test First day
Second day
Third day
Fourth day
Muscle
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric
2.07 2.82 4.90 3.87 3.15 2.59 2.21 2.33
0.75 0.64 1.11 1.07 0.73 0.62 0.26 0.30
2.61 3.31 4.25 4.05 2.78 2.48 2.36 2.55
0.58 0.53 1.24 1.17 0.60 0.41 0.51 0.41
2.63 2.87 4.54 3.42 2.84 2.87 2.48 2.34
0.51 0.62 1.18 1.21 0.54 0.43 0.47 0.38
2.38 2.68 4.87 4.25 2.80 2.10 2.65 2.57
0.61 0.57 1.01 1.02 0.34 0.23 0.33 0.36
Table II. Means
and standard deviations of the EMG data (µV) at rest position and during swallowing and chewing and comparison between normooclusive group and right posterior crossbite group Normoclusive group Muscle Rest position* Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric Swallowing** Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric Chewing* Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric
Right posterior crossbite group
Student t
Mean
SD
Mean
SD
P
3.23 1.97 3.87 4.03 2.67 3.20 2.37 2.13
1.68 0.99 2.36 3.29 2.26 4.11 1.19 1.41
3.74 2.47 3.30 5.05 2.61 1.78 2.33 2.39
3.46 1.65 2.75 5.07 3.40 1.40 1.23 1.09
.34 .24 .24 .71 .25 .21 .92 .13
NS NS NS NS NS NS NS NS
58.14 43.29 43.21 55.89 54.37 65.53 92.31 103.52
56.10 46.27 23.26 49.11 28.25 51.82 35.74 64.65
77.35 110.85 57.30 80.65 71.50 71.50 131.90 137.45
63.83 126.65 46.29 68.09 52.43 68.08 58.79 54.18
.10 <.05 .57 .41 .19 .84 <.01 <.05
NS S NS NS NS NS S S
40.90 38.87 22.90 22.70 47.03 43.93 26.40 27.93
18.33 18.48 7.90 11.26 20.82 18.17 10.78 11.82
41.15 43.55 20.45 22.50 37.20 38.75 36.00 33.70
18.62 16.28 10.85 12.23 22.91 19.91 18.22 12.95
.91 .26 .33 .83 <.05 .54 <.05 .22
NS NS NS NS S NS S NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
each group using parametric statistics (Student t test). Significance was set at the 5% level (P ≤ .05). These tests were carried out with statistical analysis software (BMDP6D Statistical Software, Inc, Los Angeles, Calif). RESULTS
As can be seen in Table I, differences between repeated recordings were not statistically significant.
Muscular Activity at Rest Position
Table II shows the mean values and standard deviations of electric potentials recorded from the 8 examined muscles at rest position. When comparing both study groups, normocclusive and right posterior crossbite subjects, no significant differences were found in any of the tested muscles.
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Table III. Comparison
of EMG activity (µV) between right and left side muscles in the normocclusive group Right
Muscle Rest position* Anterior temporalis Posterior temporalis Right masseter Right anterior digastric Swallowing** Anterior temporalis Posterior temporalis Masseter Anterior digastric Chewing* Anterior temporalis Posterior temporalis Masseter Anterior digastric
Left
Student t
Mean
SD
Mean
SD
P
3.26 3.87 2.67 2.37
1.60 2.36 2.26 1.19
1.97 4.03 3.20 2.13
0.99 3.29 4.11 1.41
<.05 .74 .90 .26
S NS NS NS
58.14 43.21 54.37 92.31
56.10 23.26 28.25 35.74
43.29 55.89 65.53 103.52
46.27 49.11 51.82 64.65
.12 .31 .58 .25
NS NS NS NS
40.90 22.90 47.03 26.40
18.33 7.90 20.82 10.78
38.87 22.70 43.93 27.93
18.48 11.26 18.17 11.82
.52 .92 .46 .57
NS NS NS NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
Table IV. Comparison
of EMG activity (µV) between right and left side muscles in the right crossbite group Right
Muscle Rest position* Anterior temporalis Posterior temporalis Right masseter Right anterior digastric Swallowing** Anterior temporalis Posterior temporalis Masseter Anterior digastric Chewing* Anterior temporalis Posterior temporalis Masseter Anterior digastric
Mean
Left SD
Mean
Student t SD
P
3.74 3.30 2.61 2.33
3.46 2.75 3.40 1.23
2.47 5.05 1.78 2.39
1.65 5.07 1.40 1.09
.08 <.05 .12 .76
NS S NS NS
77.35 57.30 71.50 131.90
63.83 46.29 52.43 58.79
110.85 80.65 71.50 137.45
126.65 68.09 68.08 54.18
.50 <.05 1.00 .64
NS S NS NS
41.15 20.45 37.20 36.00
18.62 10.85 22.91 18.22
43.55 22.50 38.75 33.70
16.28 12.23 19.91 12.95
.50 .49 .69 .65
NS NS NS NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
Right and left muscles were compared in each group. In the normocclusive children, the right AT was significantly more active (3.23 µV) than the one of the left side (1.97 µV) (Table III). In the right posterior crossbite group, the left PT was more active (5.05 µV) than the right one (3.30 µV, Table IV). Therefore, the PT opposite to the crossbite side was more active than the ipsilateral one at rest position.
Muscular Activity during Swallowing
The maximum amplitude during swallowing for the 2 study populations is shown in Table II. In the right posterior crossbite subjects, the EMG activity of left AT (P < .05), left AD (P < .05), and right AD (P < .01) was higher than in the normocclusive subjects during swallowing. Although the anterior digastrics are the dominant muscles during swallowing, these muscles showed
332 Alarcón, Martín, and Palma
an unusual increase in activity in the right posterior crossbite subjects. In the normocclusive subjects, no significant differences were found between the muscles of the right side and the muscles of the left side during swallowing (Table III). In the right posterior crossbite group, the left PT showed a higher peak of EMG activity (80.65 µV) than the right PT (57.30 µV); this difference is statistically significant (P < .05) (Table IV). Muscular Activity during Chewing
Significant differences were found between both groups during chewing (Table II); the crossbite right MM showed a lower activity (37.20 µV) than the normocclusive right MM (47.03 µV) and the crossbite right AD was more active (36 µV) than that of the normocclusive children (26.40 µV). In both groups (normocclusive and crossbite, Table III and IV) the muscular activity during chewing was fairly symmetric. No significant differences were found between the muscles of the right side and of the left side. DISCUSSION
We have chosen two matched samples of subjects with a balanced skeletal pattern in order to test differences caused only by the presence or absence of unilateral posterior crossbite. Transversal malocclusions are normally associated with other types of sagittal or vertical anomalies,21 and it is difficult to determine the influence of these anomalies on the neuromuscular system. However, several studies have examined variations in EMG activity among subjects with skeletal Class I, Class II, or Class III malocclusions22-28 and between dolicofacial and brachyfacial subjects.26,29-32 Therefore, one of our inclusion criteria was skeletal Class I malocclusion and mesofacial growth pattern. We performed a pilot study in order to test the reproducibility of the EMG data. It showed that surface EMG measurements allow good reproducibility in different functional conditions such as rest position, swallowing, and chewing. This reproducibility has also been reported by other investigators.19,20,33 We found very large standard deviations relative to the mean values of EMG activity in both normocclusive and crossbite groups. This finding is also present in other studies34-36 and is probably due to the great biological variability found among individuals. At rest no statistical differences between the normocclusive subjects and the crossbite subjects were found in the EMG activity of the studied muscles. However, when we compared right and left muscles within each group, we found statistically significant differences. In the normocclusive group, the right AT
American Journal of Orthodontics and Dentofacial Orthopedics September 2000
demonstrated a higher EMG activity than the left AT (3.26 µV versus 1.97 µV). Similarly, Ferrario et al36 showed that the “normal” population shows a certain degree of muscular asymmetry that can be considered as physiologic and compatible with a normal function. In the right posterior crossbite subjects, the left PT (contralateral to the crossbite side) showed a higher EMG activity (5.05 µV) than the right PT (3.30 µV, P < .05). We believe that this asymmetry in the PT muscle is due to the functional mandibular shift that exists in the patients with unilateral posterior crossbites. This shift acts as a mechanism to reach a certain degree of occlusal stability. We therefore suggest that the role of the PT muscle is positioning and stabilizing the mandible.32,37-41 These results are not in agreement with the ones found in the few studies that have assessed the EMG activity of MMs in a unilateral posterior crossbite population.16-18 They found that at rest the PT ipsilateral to the crossbite was more active than the contralateral one. These differences can be due to the reduced number of subjects and to the different selection criteria and techniques used by these authors. A question that arises from these results is why the EMG asymmetry of the PT shows at rest, when there are no occlusal interferences producing a functional shift of the mandible. A possible answer is that the functional shift found in maximal intercuspation persists also at rest. We found large standard deviations for both groups during swallowing. This greater variability is also found in other EMG studies16,18,27,34,36 and could be explained by the use of the peak of activity instead of the mean activity during swallowing, which increases the differences among subjects. These standard deviations are even larger in the crossbite patients, probably due to the higher prevalence of atypical deglutition patterns found in this group. Left AT (contralateral to the crossbite) was significantly more active (P < .05) in the crossbite subjects than in the normocclusive subjects. Both anterior digastrics (right and left) were also more active in the crossbite subjects than in the control ones (P < .05). Our results are not in agreement with the study by Ingervall and Thilander18 that examined the swallowing activity in children with posterior crossbite. They found a statistically significant reduction of the activity of the PT muscle contralateral to the crossbite and of the ipsilateral masseter muscle in children with posterior crossbite compared with normocclusive children. In our study, we did not find significant differences in the activity of the PT and MM between the normocclusive and the crossbite children. Those authors18 used a different sample selection and experimental
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design and did not include the anterior digastrics despite their important role during the deglutition, so their results are not totally comparable with ours. The increased EMG activity of the AD muscles in the crossbite subjects compared with the normocclusive subjects could possibly be the result of the higher frequency of atypical deglutition found in the crossbite group. It is known that atypical deglutition increases the activity of the digastric and perioral muscles.42,43 When we compared the EMG activity of the muscles of the right side with the muscles of the left side within the normocclusive group, we did not find significant differences (symmetric function). In the crossbite group, the left PT was more active (80.65 µV) than the right one (57.30 µV, P < .05). This asymmetric behavior of the PT muscles during swallowing in the crossbite subjects is identical to the one found in these subjects at rest. Our opinion is that it is due to the same reason, and therefore the lateral shift persists during swallowing. In this sense, Williamson et al42 stated that swallowing without tooth contact was highly associated with a lateral shift of the mandible. In agreement with Hamerling,44 we consider that the lateral shift of the mandible is due more to a learned neuromuscular pattern than to conditioning occlusal factors because this lateral shift is present both at rest and during swallowing without tooth contact. During chewing, the EMG activity demonstrates that subjects with posterior crossbite show a masticatory pattern that is unique and different from the pattern of the normocclusive subjects. The AT muscles are the most active instead of the MM. In an EMG study during chewing, Mushimoto and Mitani45 found that the MMs generate the power, the AT muscles collaborate, and the PT muscles stabilize the mandible and participate in the lateral and retrusive movements of the mandible. This pattern is found in the normocclusive subjects but not in the crossbite subjects. In the crossbite subjects, it is possible that the sequence of priorities of the neuromuscular system is different; the most important role is to position the mandible correctly in order to reach a higher occlusal stability and, once there, to generate the necessary power to chew. This could be the reason why the AT is the most active. The right MM (ipsilateral to the crossbite) was less active in the crossbite group (37.2 µV) than in the normocclusive group (47.03 µV, P < .05). This could be due to an inhibitory–protective reflex to avoid injury of the structures of the stomatognathic system. A tooth contact in an unstable position could cause discomfort or even pain. For this reason, the capacity of the MMs to generate power could be diminished. In the study by Ingervall and Thilander,18 patients with lateral shift
showed a lower activity of the AT and PT muscles than the normocclusive subjects. Relating the activity of the MMs, no differences were found. Our results are not in agreement with the results of these authors, although the data are not totally comparable because they recorded the maximum peak of EMG activity during chewing, and we recorded the mean activity during chewing. When we compared the EMG activity of the muscles of the right side with the muscles of the left side, we did not find significant differences in any of the groups. This could mean that during chewing there is a symmetric function of the MMs, and therefore chewing is bilateral. These results are in agreement with those reported by Ingervall and Thilander18 and Kurol and Berglund.3 CONCLUSIONS
EMG recordings of MMs from 30 subjects with right posterior crossbite and 30 normocclusive subjects at rest position, during swallowing and chewing revealed differences between both groups. The PT of the non–crossbite side was more active than that of the same side in the crossbite subjects (asymmetric activity) at rest position and during swallowing. In addition, the activity of both anterior digastrics was higher in the crossbite subjects during swallowing. During chewing, the MM of the crossbite side showed a lower activity than that of the same side in the normocclusive subjects. Masseter activity was symmetric in both groups. REFERENCES 1. Kurol J, Berglund L. Longitudinal study and cost-benefit analysis of the effect of early treatment of posterior crossbite in the primary dentition. Eur J Orthod 1992;14:173-9. 2. Kisling E. Occlusal interferences in the primary dentition. J Dent Child 1981;48:181-91. 3. Darque J, Darque F, Pujol A, Saulue P. Terapéutica ortodóncica y musculatura. Ortod Esp 1992;33(suppl):177-86. 4. Egermark-Eriksson I, Ingervall B. Anomalies of occlusion predisposing to occlusal interference in children. Angle Orthod 1982;52:293-9. 5. Mew J. Comment on mandibular and facial asymmetries. Am J Orthod Dentofacial Orthop 1995;108:17A 6. Schmid W, Mongini F, Felisio A. A computer bases assessment of structural and displacement asymmetries of the mandible. Am J Orthod Dentofacial Orthop 1991;100:19-34. 7. Pirttiniemi P, Kantomaa T, Lahtela P. Relationship between craniofacial and condyle path asymmetry in unilateral crossbite patients. Eur J Orthod 1990;12:408-13. 8. Fushima K, Akimoto S, Takamoto K, Sato S, Suzuki Y. Morphological feature and incidence of TMJ disorders in mandibular lateral displacement cases. Nippon Kyosei Shika Gakkai Zasshi 1989;3:322-3. 9. Thilander B. Temporomandibular joint problems in children. In: Cärlsson DS, McNamara JA, editors. Developmental aspects of temporomandibular joint disorders. Monograph 16. Craniofacial
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masseter and orbicularis oris muscle activity and craniofacial morphology in children. Am J Orthod 1984;86:319-30. Southard TE, Behrents RG, Tolley EA. La composante antérieure de la force occlusale. Am J Orthod Dentofacial Orthop 1990;2:14-22(ed franc) Fields HW, Proffit WR, Case JC, Vig WL.Variables affecting measurement of vertical occlusal force. J Dent Res 1986;65:1358. Lowe AA. Correlations between orofacial muscle activity and craniofacial morphology in a sample of control and anterior open-bite subjects. Am J Orthod 1980;78:89-98. Darque J, Bertrand-Brangier N. Divergence des bases squelettiques et deonnées électromyographiques. Orthod Fr 1978;49:769-72. Ahlgren J, Ingervall B, Thilander B. Muscle activity in normal and postnormal occlusion. Am J Orthod 1973;64:445-55. Burdette BH, Gale EN. Reliability of surface electromyography of the masseteric and anterior temporal areas. Arch Oral Biol 1991;35:747-51. Ahlgren J, Sonesson B, Blitz M. An electromyographic analysis of the temporalis function of normal occlusion. Am J Orthod 1985;87:220-39. Ahlgren J. EMG pattern of temporalis in normal occlusion. Eur J Orthod 1986;8:185-91. Ferrario VF, Sforza C, Miani A, D’Addona A, Barbini E. Electromyographic activity of human masticatory muscles in normal young people: statistical evaluation of reference values for clinical applications. J Oral Rehabil 1993;20:271-80. McCarrol RS, Naeije M, Kim YK, Hansson TL. The inmediate effect of splint-induced changes in jaw positioning on the asymmetry of submaximal masticatory muscle activity. J Oral Rehabil 1989;16:163-70. Jimenez ID. Dental stability and maximal masticatory muscle activity. J Oral Rehabil 1987;14: 591-8. Dubrul EL. Sicher’s oral anatomy. St Louis: CV Mosby; 1980. Latif A. An electromyographic study of the temporalis muscle in normal persons during selected positions and movements of the mandible. Am J Orthod 1957;43:577. Carlsöö S. Nervous coordination and mechanical function of the mandibular elevators. Acta Odontol Scand 1952;10(Suppl11). Williamson EH, Hall TH, Zwemer JD. Swallowing patterns in human subjects with and without temporomandibular dysfunction. Am J Orthod Dentofacial Orthop 1990;98:507-11. Tulley WJ. Methods of recording patterns of behavior of the orofacial muscles using the electromyograph. J Dent Res 1953;73:741. Hamerling K, Naeije C, Myrberg N. Mandibular function in children with a lateral forced bite. Eur J Orthod 1991;13:35-42. Mushimoto E, Mitani M. Bilateral coordination pattern of masticatory muscle activities during chewing in normal subjects. J Prosthet Dent 1982;48:191-7.
he neuromuscular characteristics associated with unilateral posterior crossbite (UPCB) have not been extensively studied. From a therapeutic point of view, this malocclusion does not correct spontaneously and generally persists through adulthood.1,2 Several deleterious effects have been linked to UPCB. It may cause occlusal interferences as a result of the inadequate relationship between both dental arches.3,4 Skeletally, crossbites with lateral shift influence the normal growth of the mandible.5-9 Another consequence of an untreated UPCB is the likely asymmetry in the condylar position and trajectories, with a displacement of the ipsilateral condyle toward the crossbite side10-12 and an increased growth of the contralateral condyle.13 The intimate mechanism that links the lateral shift of the mandible with the condylar growth remains unclear, but it seems that the main cause could be abnormal muscular activity.3,10,14,15 There is a certain degree of asymmetric muscle activity. Troelstrup and Möller16,17 found that the posterior temporalis of the same side of the crossbite showed higher electromyographic (EMG) activity than the contralateral muscle at rest and during maximum
T
From the Faculty of Odontology, University Complutense, Madrid, Spain. aAssociate Professor of Orthodontic. bAssociate Professor of Orthodontic, University Complutense, Madrid, Spain. cProfessor of Orthodontics. Reprint requests to: Conchita Martín. C/Bola del Mundo, 38 28023 Madrid, Spain; e-mail, [email protected]. Submitted April 1999; Revised and accepted September 1999. Copyright © 2000 by the American Association of Orthodontists. 0889-5406/2000/$12.00 + 0 8/1/103252 doi:10.1067/mod.2000.103252
328
clenching, whereas the ipsilateral anterior temporalis was less active than the contralateral muscle at rest. Ingervall and Thilander18 found a certain degree of asymmetry in the activity of masticatory muscles in 19 children with laterally forced bite (16 of them had unilateral crossbite). The posterior temporalis on the forced bite side was more active at rest, during chewing, and at maximal bite than that of the nonforced bite side, whereas the anterior temporalis on the forced bite side was more active during chewing than that of the nonforced bite side. The purpose of this study was to assess the EMG pattern of masticatory muscles at rest position, during swallowing, and during mastication, in children with unilateral posterior crossbite and to compare this pattern with the one obtained in normocclusive children. The knowledge of the behavior of masticatory muscles in this malocclusion could help its diagnosis and management. SUBJECTS AND METHODS Patient Population
The study population consisted of a consecutive sample of 60 white subjects from the Children’s Department of the Faculty of Odontology of University Complutense, Madrid (Spain), divided into 2 groups: a control group of 30 normocclusive subjects (16 girls and 14 boys; mean age, 12 years 5 months) and an experimental group of 30 subjects (17 girls and 13 boys; mean age, 12 years 2 months) with right posterior crossbite of at least the first molar. The following criteria were used in the selection of
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the 2 groups: age between 10 and 14 years; skeletal Class I malocclusion according to ANB angle, convexity, and Wits appraisal; and mesofacial growth pattern according to Frankfort horizontal-to-mandibular plane angle. Subjects were excluded if they had clinical signs or symptoms of temporomandibular joint dysfunction, skeletal asymmetry, previous or current orthodontic treatment, extensive restorations, cast restorations or cuspal coverage, pathologic periodontal condition, or missing teeth. All subjects received full explanations of the aims and design of the study before its start and agreed to participate by signing an informed consent. Recording of Muscular Activity
Simultaneous bilateral (left, and right) surface electromyographs of anterior temporalis (AT), posterior temporalis (PT), masseter (MM), and anterior digastric (AD) muscles were recorded at rest (mandibular postural position), during swallowing, and during chewing. EMG measurements were recorded with an 8-channel electromyograph (EM2) interfaced with an IBM PC computer (Myo-Tronics, Seattle, Wash). This system allows 8 muscles to be monitored without interfering with the functional activity of the subjects. Disposable silver chloride bipolar surface electrodes (Duo-Trode, Myo-Tronics Inc) were prepositioned on the muscular bellies parallel with the muscular fibers according to the following protocol (Ferrario et al19 and Jankelson20): MM The operator stood behind the patient and palpated the muscle while asking the patient to clench in habitual occlusion. Electrodes were placed over an oblique line connecting the patient´s eye and his or her mandibular angle, about 3 cm above and in front of the gonial angle. AT The muscle was palpated asking the patient to clench in habitual occlusion. Electrodes were placed vertically over the anterior border of the muscle, on the area corresponding to the frontoparietal suture. PT The operator asked the patient to place the tongue against the palate and to press. The electrode was placed almost horizontally parallel to the posterosuperior border of the ear. AD With the patient pressing the tongue against the palate, the electrode was placed under the chin parallel to the mandibular body over the suprahyoid triangle. The ground electrode was a disk-type electrode (Duo-trode, Myo-Tronics Inc) placed on the side surface of the neck. In order to minimize electrode impedance, the recording sites were thoroughly cleansed with a piece of cotton soaked in 70% alcohol. Recordings were performed at least 5 minutes after application of
the electrode to allow the conductive paste to adequately moisten the skin surface. EMG activity was recorded at rest position, during swallowing, and during chewing, using the following protocol: Rest (mandibular rest position without occlusal contact). To obtain this resting position patients were asked to moisten the lips, to swallow saliva, to breath deeply and to relax their jaws with closed eyes. Average EMG activity (µV) was obtained with a calibration of 30 µV. Swallowing. Muscular activity was registered during the intake of water. Subjects were instructed to take a mouthful of water and to hold their jaws at rest position. They were then instructed to swallow the water and, after swallowing, to hold their jaws at rest position again. The peak (maximum amplitude, µV) was obtained with a calibration of 30 µV, allowing a resting period of 1 minute between each swallowing. Chewing. Muscular activity was registered during mastication of chips. The operator just asked the subject to eat chips without further instructions. The EMG activity was then recorded for the last 10 seconds of the chewing. Average EMG activity (µV) was obtained with a calibration of 30 µV. There was a quiet, dark, and comfortable atmosphere during the experiment. Verbal instructions were given to the patients before starting in order to avoid any stressful situation, and several trial tests were made to instruct the patient. Irregular or spurious tracings were omitted, and the measurements repeated. For continuity, one calibrated examiner performed all EMG measurements in a “blind to status” manner. The examiner was blind to the presence of posterior crossbite. Collected data remained blind to status throughout analysis by assigning each subject a code number. Therefore, the true status of the subjects was not revealed until the data had been compiled in order to decrease the possibility of bias at any stage in the study. Reproducibility of the EMG Data
In order to evaluate the reproducibility of the EMG records, the results of different consecutive measurements were compared. The rest position test was reproduced starting with electrode placement. Four trials were performed in 5 subjects over 4 days according to experimental protocol. The data from the first day were compared with those of the other 3 days for statistical significance with the Student t variable test. Statistical Analysis
Means and standard deviations were calculated for the EMG values in the 3 tests. Data were compared between groups and between right and left sides within
330 Alarcón, Martín, and Palma
Table I. Comparison
American Journal of Orthodontics and Dentofacial Orthopedics September 2000
of EMG data (µV) taken 4 successive days for rest position test First day
Second day
Third day
Fourth day
Muscle
Mean
SD
Mean
SD
Mean
SD
Mean
SD
Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric
2.07 2.82 4.90 3.87 3.15 2.59 2.21 2.33
0.75 0.64 1.11 1.07 0.73 0.62 0.26 0.30
2.61 3.31 4.25 4.05 2.78 2.48 2.36 2.55
0.58 0.53 1.24 1.17 0.60 0.41 0.51 0.41
2.63 2.87 4.54 3.42 2.84 2.87 2.48 2.34
0.51 0.62 1.18 1.21 0.54 0.43 0.47 0.38
2.38 2.68 4.87 4.25 2.80 2.10 2.65 2.57
0.61 0.57 1.01 1.02 0.34 0.23 0.33 0.36
Table II. Means
and standard deviations of the EMG data (µV) at rest position and during swallowing and chewing and comparison between normooclusive group and right posterior crossbite group Normoclusive group Muscle Rest position* Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric Swallowing** Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric Chewing* Right anterior temporalis Left anterior temporalis Right posterior temporalis Left posterior temporalis Right masseter Left masseter Right anterior digastric Left anterior digastric
Right posterior crossbite group
Student t
Mean
SD
Mean
SD
P
3.23 1.97 3.87 4.03 2.67 3.20 2.37 2.13
1.68 0.99 2.36 3.29 2.26 4.11 1.19 1.41
3.74 2.47 3.30 5.05 2.61 1.78 2.33 2.39
3.46 1.65 2.75 5.07 3.40 1.40 1.23 1.09
.34 .24 .24 .71 .25 .21 .92 .13
NS NS NS NS NS NS NS NS
58.14 43.29 43.21 55.89 54.37 65.53 92.31 103.52
56.10 46.27 23.26 49.11 28.25 51.82 35.74 64.65
77.35 110.85 57.30 80.65 71.50 71.50 131.90 137.45
63.83 126.65 46.29 68.09 52.43 68.08 58.79 54.18
.10 <.05 .57 .41 .19 .84 <.01 <.05
NS S NS NS NS NS S S
40.90 38.87 22.90 22.70 47.03 43.93 26.40 27.93
18.33 18.48 7.90 11.26 20.82 18.17 10.78 11.82
41.15 43.55 20.45 22.50 37.20 38.75 36.00 33.70
18.62 16.28 10.85 12.23 22.91 19.91 18.22 12.95
.91 .26 .33 .83 <.05 .54 <.05 .22
NS NS NS NS S NS S NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
each group using parametric statistics (Student t test). Significance was set at the 5% level (P ≤ .05). These tests were carried out with statistical analysis software (BMDP6D Statistical Software, Inc, Los Angeles, Calif). RESULTS
As can be seen in Table I, differences between repeated recordings were not statistically significant.
Muscular Activity at Rest Position
Table II shows the mean values and standard deviations of electric potentials recorded from the 8 examined muscles at rest position. When comparing both study groups, normocclusive and right posterior crossbite subjects, no significant differences were found in any of the tested muscles.
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Table III. Comparison
of EMG activity (µV) between right and left side muscles in the normocclusive group Right
Muscle Rest position* Anterior temporalis Posterior temporalis Right masseter Right anterior digastric Swallowing** Anterior temporalis Posterior temporalis Masseter Anterior digastric Chewing* Anterior temporalis Posterior temporalis Masseter Anterior digastric
Left
Student t
Mean
SD
Mean
SD
P
3.26 3.87 2.67 2.37
1.60 2.36 2.26 1.19
1.97 4.03 3.20 2.13
0.99 3.29 4.11 1.41
<.05 .74 .90 .26
S NS NS NS
58.14 43.21 54.37 92.31
56.10 23.26 28.25 35.74
43.29 55.89 65.53 103.52
46.27 49.11 51.82 64.65
.12 .31 .58 .25
NS NS NS NS
40.90 22.90 47.03 26.40
18.33 7.90 20.82 10.78
38.87 22.70 43.93 27.93
18.48 11.26 18.17 11.82
.52 .92 .46 .57
NS NS NS NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
Table IV. Comparison
of EMG activity (µV) between right and left side muscles in the right crossbite group Right
Muscle Rest position* Anterior temporalis Posterior temporalis Right masseter Right anterior digastric Swallowing** Anterior temporalis Posterior temporalis Masseter Anterior digastric Chewing* Anterior temporalis Posterior temporalis Masseter Anterior digastric
Mean
Left SD
Mean
Student t SD
P
3.74 3.30 2.61 2.33
3.46 2.75 3.40 1.23
2.47 5.05 1.78 2.39
1.65 5.07 1.40 1.09
.08 <.05 .12 .76
NS S NS NS
77.35 57.30 71.50 131.90
63.83 46.29 52.43 58.79
110.85 80.65 71.50 137.45
126.65 68.09 68.08 54.18
.50 <.05 1.00 .64
NS S NS NS
41.15 20.45 37.20 36.00
18.62 10.85 22.91 18.22
43.55 22.50 38.75 33.70
16.28 12.23 19.91 12.95
.50 .49 .69 .65
NS NS NS NS
*Average electromyographic activity (µV). **Peak (maximum amplitude, µV).
Right and left muscles were compared in each group. In the normocclusive children, the right AT was significantly more active (3.23 µV) than the one of the left side (1.97 µV) (Table III). In the right posterior crossbite group, the left PT was more active (5.05 µV) than the right one (3.30 µV, Table IV). Therefore, the PT opposite to the crossbite side was more active than the ipsilateral one at rest position.
Muscular Activity during Swallowing
The maximum amplitude during swallowing for the 2 study populations is shown in Table II. In the right posterior crossbite subjects, the EMG activity of left AT (P < .05), left AD (P < .05), and right AD (P < .01) was higher than in the normocclusive subjects during swallowing. Although the anterior digastrics are the dominant muscles during swallowing, these muscles showed
332 Alarcón, Martín, and Palma
an unusual increase in activity in the right posterior crossbite subjects. In the normocclusive subjects, no significant differences were found between the muscles of the right side and the muscles of the left side during swallowing (Table III). In the right posterior crossbite group, the left PT showed a higher peak of EMG activity (80.65 µV) than the right PT (57.30 µV); this difference is statistically significant (P < .05) (Table IV). Muscular Activity during Chewing
Significant differences were found between both groups during chewing (Table II); the crossbite right MM showed a lower activity (37.20 µV) than the normocclusive right MM (47.03 µV) and the crossbite right AD was more active (36 µV) than that of the normocclusive children (26.40 µV). In both groups (normocclusive and crossbite, Table III and IV) the muscular activity during chewing was fairly symmetric. No significant differences were found between the muscles of the right side and of the left side. DISCUSSION
We have chosen two matched samples of subjects with a balanced skeletal pattern in order to test differences caused only by the presence or absence of unilateral posterior crossbite. Transversal malocclusions are normally associated with other types of sagittal or vertical anomalies,21 and it is difficult to determine the influence of these anomalies on the neuromuscular system. However, several studies have examined variations in EMG activity among subjects with skeletal Class I, Class II, or Class III malocclusions22-28 and between dolicofacial and brachyfacial subjects.26,29-32 Therefore, one of our inclusion criteria was skeletal Class I malocclusion and mesofacial growth pattern. We performed a pilot study in order to test the reproducibility of the EMG data. It showed that surface EMG measurements allow good reproducibility in different functional conditions such as rest position, swallowing, and chewing. This reproducibility has also been reported by other investigators.19,20,33 We found very large standard deviations relative to the mean values of EMG activity in both normocclusive and crossbite groups. This finding is also present in other studies34-36 and is probably due to the great biological variability found among individuals. At rest no statistical differences between the normocclusive subjects and the crossbite subjects were found in the EMG activity of the studied muscles. However, when we compared right and left muscles within each group, we found statistically significant differences. In the normocclusive group, the right AT
American Journal of Orthodontics and Dentofacial Orthopedics September 2000
demonstrated a higher EMG activity than the left AT (3.26 µV versus 1.97 µV). Similarly, Ferrario et al36 showed that the “normal” population shows a certain degree of muscular asymmetry that can be considered as physiologic and compatible with a normal function. In the right posterior crossbite subjects, the left PT (contralateral to the crossbite side) showed a higher EMG activity (5.05 µV) than the right PT (3.30 µV, P < .05). We believe that this asymmetry in the PT muscle is due to the functional mandibular shift that exists in the patients with unilateral posterior crossbites. This shift acts as a mechanism to reach a certain degree of occlusal stability. We therefore suggest that the role of the PT muscle is positioning and stabilizing the mandible.32,37-41 These results are not in agreement with the ones found in the few studies that have assessed the EMG activity of MMs in a unilateral posterior crossbite population.16-18 They found that at rest the PT ipsilateral to the crossbite was more active than the contralateral one. These differences can be due to the reduced number of subjects and to the different selection criteria and techniques used by these authors. A question that arises from these results is why the EMG asymmetry of the PT shows at rest, when there are no occlusal interferences producing a functional shift of the mandible. A possible answer is that the functional shift found in maximal intercuspation persists also at rest. We found large standard deviations for both groups during swallowing. This greater variability is also found in other EMG studies16,18,27,34,36 and could be explained by the use of the peak of activity instead of the mean activity during swallowing, which increases the differences among subjects. These standard deviations are even larger in the crossbite patients, probably due to the higher prevalence of atypical deglutition patterns found in this group. Left AT (contralateral to the crossbite) was significantly more active (P < .05) in the crossbite subjects than in the normocclusive subjects. Both anterior digastrics (right and left) were also more active in the crossbite subjects than in the control ones (P < .05). Our results are not in agreement with the study by Ingervall and Thilander18 that examined the swallowing activity in children with posterior crossbite. They found a statistically significant reduction of the activity of the PT muscle contralateral to the crossbite and of the ipsilateral masseter muscle in children with posterior crossbite compared with normocclusive children. In our study, we did not find significant differences in the activity of the PT and MM between the normocclusive and the crossbite children. Those authors18 used a different sample selection and experimental
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design and did not include the anterior digastrics despite their important role during the deglutition, so their results are not totally comparable with ours. The increased EMG activity of the AD muscles in the crossbite subjects compared with the normocclusive subjects could possibly be the result of the higher frequency of atypical deglutition found in the crossbite group. It is known that atypical deglutition increases the activity of the digastric and perioral muscles.42,43 When we compared the EMG activity of the muscles of the right side with the muscles of the left side within the normocclusive group, we did not find significant differences (symmetric function). In the crossbite group, the left PT was more active (80.65 µV) than the right one (57.30 µV, P < .05). This asymmetric behavior of the PT muscles during swallowing in the crossbite subjects is identical to the one found in these subjects at rest. Our opinion is that it is due to the same reason, and therefore the lateral shift persists during swallowing. In this sense, Williamson et al42 stated that swallowing without tooth contact was highly associated with a lateral shift of the mandible. In agreement with Hamerling,44 we consider that the lateral shift of the mandible is due more to a learned neuromuscular pattern than to conditioning occlusal factors because this lateral shift is present both at rest and during swallowing without tooth contact. During chewing, the EMG activity demonstrates that subjects with posterior crossbite show a masticatory pattern that is unique and different from the pattern of the normocclusive subjects. The AT muscles are the most active instead of the MM. In an EMG study during chewing, Mushimoto and Mitani45 found that the MMs generate the power, the AT muscles collaborate, and the PT muscles stabilize the mandible and participate in the lateral and retrusive movements of the mandible. This pattern is found in the normocclusive subjects but not in the crossbite subjects. In the crossbite subjects, it is possible that the sequence of priorities of the neuromuscular system is different; the most important role is to position the mandible correctly in order to reach a higher occlusal stability and, once there, to generate the necessary power to chew. This could be the reason why the AT is the most active. The right MM (ipsilateral to the crossbite) was less active in the crossbite group (37.2 µV) than in the normocclusive group (47.03 µV, P < .05). This could be due to an inhibitory–protective reflex to avoid injury of the structures of the stomatognathic system. A tooth contact in an unstable position could cause discomfort or even pain. For this reason, the capacity of the MMs to generate power could be diminished. In the study by Ingervall and Thilander,18 patients with lateral shift
showed a lower activity of the AT and PT muscles than the normocclusive subjects. Relating the activity of the MMs, no differences were found. Our results are not in agreement with the results of these authors, although the data are not totally comparable because they recorded the maximum peak of EMG activity during chewing, and we recorded the mean activity during chewing. When we compared the EMG activity of the muscles of the right side with the muscles of the left side, we did not find significant differences in any of the groups. This could mean that during chewing there is a symmetric function of the MMs, and therefore chewing is bilateral. These results are in agreement with those reported by Ingervall and Thilander18 and Kurol and Berglund.3 CONCLUSIONS
EMG recordings of MMs from 30 subjects with right posterior crossbite and 30 normocclusive subjects at rest position, during swallowing and chewing revealed differences between both groups. The PT of the non–crossbite side was more active than that of the same side in the crossbite subjects (asymmetric activity) at rest position and during swallowing. In addition, the activity of both anterior digastrics was higher in the crossbite subjects during swallowing. During chewing, the MM of the crossbite side showed a lower activity than that of the same side in the normocclusive subjects. Masseter activity was symmetric in both groups. REFERENCES 1. Kurol J, Berglund L. Longitudinal study and cost-benefit analysis of the effect of early treatment of posterior crossbite in the primary dentition. Eur J Orthod 1992;14:173-9. 2. Kisling E. Occlusal interferences in the primary dentition. J Dent Child 1981;48:181-91. 3. Darque J, Darque F, Pujol A, Saulue P. Terapéutica ortodóncica y musculatura. Ortod Esp 1992;33(suppl):177-86. 4. Egermark-Eriksson I, Ingervall B. Anomalies of occlusion predisposing to occlusal interference in children. Angle Orthod 1982;52:293-9. 5. Mew J. Comment on mandibular and facial asymmetries. Am J Orthod Dentofacial Orthop 1995;108:17A 6. Schmid W, Mongini F, Felisio A. A computer bases assessment of structural and displacement asymmetries of the mandible. Am J Orthod Dentofacial Orthop 1991;100:19-34. 7. Pirttiniemi P, Kantomaa T, Lahtela P. Relationship between craniofacial and condyle path asymmetry in unilateral crossbite patients. Eur J Orthod 1990;12:408-13. 8. Fushima K, Akimoto S, Takamoto K, Sato S, Suzuki Y. Morphological feature and incidence of TMJ disorders in mandibular lateral displacement cases. Nippon Kyosei Shika Gakkai Zasshi 1989;3:322-3. 9. Thilander B. Temporomandibular joint problems in children. In: Cärlsson DS, McNamara JA, editors. Developmental aspects of temporomandibular joint disorders. Monograph 16. Craniofacial
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