Changes in electric activity of masseter and anterior temporalis muscles before and after orthognathic surgery in skeletal class III patients

Changes in electric activity of masseter and anterior temporalis muscles before and after orthognathic surgery in skeletal class III patients

Vol. 116 No. 4 October 2013 Changes in electric activity of masseter and anterior temporalis muscles before and after orthognathic surgery in skeleta...

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Vol. 116 No. 4 October 2013

Changes in electric activity of masseter and anterior temporalis muscles before and after orthognathic surgery in skeletal class III patients Gianluigi Frongia, DDS, DOS, PhD,a Guglielmo Ramieri, MD, DDS,b Corrado De Biase, DDS, DOS,a Pietro Bracco, MD, DDS, DOS,a and Maria Grazia Piancino, MD, DDS, PhDa University of Turin, Italy

Objective. The purpose of this study was to evaluate, through clinical and electromyographic (EMG) assessments, the electric activity of masseter muscle and anterior temporalis muscles during clenching, before and after orthodontic treatment and mandibular setback, with or without LeFort I osteotomy, for correction of mandibular excess. Study design. Seventeen adult patients (10 males, 7 females, mean age: 22.5  2.4 years) were recruited for this study. All patients received orthodontic treatment and surgical corrections. EMG recordings were obtained from 4 channels of the 8-channel electromyograph FREELY (DeGoetzen spa, Olgiate Olona, VA, Italy). Results. A significant difference was found in the value of activity index at T0-T1 (33% T0, 1% T1) (P < .05), of asymmetry index at T0-T1 (21% T0, 4% T1) (P < .05), and of torque index at T0-T1 (24% T0, 5% T1) (P < .05). Conclusions. The evaluation of EMG activity after surgery may be considered a sign of good adaptation of the neuromuscular system to the new occlusal condition and a good method for detecting nonresponding patients who might require further treatment. (Oral Surg Oral Med Oral Pathol Oral Radiol 2013;116:398-401)

Orthognathic surgery is commonly used to correct severe dentofacial deformities, including congenital and acquired jaw discrepancies, with predictable outcomes.1 In some cases, this discrepancy can be corrected by early treatment to change the growth pattern, but in other cases, when it is not possible to modify the growth pattern, late treatment using orthognathic surgery is the best approach to correct severe skeletal and dental malocclusion.2 Skeletal, occlusal, and esthetic outcomes are predictable, but the short- and long-term functional effects of the surgicaleorthodontic treatment on the masticatory muscles are, however, still unclear. The relative position of the upper and lower molar and premolar determines occlusal stability, which is related to muscular performance. In fact modifications of the craniofacial morphology using orthognathic surgery reflect not only on esthetics, but also on the masticatory muscles, specifically the masseter muscle (MM) and anterior temporalis (TA) muscles.3 Previous studies have investigated changes in the masticatory muscles after orthognathic surgery using electromyography.4-6 Surface electromyography is a noninvasive technique, which provides information about the muscle properties through electrodes located over the skin.7 It is well established8 that the electromyographic (EMG) activity of MM and TA muscles, in a

Department of Orthodontics and Gnathology-Masticatory Function, University of Turin. b Department of Maxillofacial Surgery, University of Turin. Received for publication Mar 25, 2013; accepted for publication Jun 9, 2013. Ó 2013 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter http://dx.doi.org/10.1016/j.oooo.2013.06.008

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normal young people during rest position, contact in centric occlusion and clench. Preorthognathic surgery patients with a variety of dentofacial deformities showed lower masticatory performances,9,10 reduced maximum EMG activity,10 and also reduced EMG activity during mastication.10,11 Surgery did not increase EMG activity during maximum clenching in retrognathic patients,12,13 3 years after surgery in muscle activity per unit in bite force,14 and 5 years after orthognathic surgery.15 Raustia and Oikarinen noted an increase in EMG activity during maximal bite in intercuspal position and chewing 12 months after surgery in the MM and TA muscles.3 Other studies reported an improvement in muscular activity after 6-8 months because of better occlusal stability,16 and an improvement in index of the symmetric distribution of the muscular activity (percentage overlapping coefficient [POC]) and torque index (TI) after surgery.16 In a recent study Trawitzki et al.17 have demonstrated an improvement in the EMG activity during chewing and

Statement of Clinical Relevance The evaluation of electromyographic activity after surgery may be considered a sign of good adaptation of the neuromuscular system to the new occlusal condition and a good method for detecting nonresponding patients who might require further treatment.

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bite force in MM only, after 3 years of the orthognathic surgery to correct skeletal class III. A greater instability has been observed in the temporalis muscle. The purpose of this study was to evaluate, through clinical and EMG assessment, the electric activity of MM and TA muscles during clenching, before and after orthodontic treatment, and mandibular setback, with or without LeFort I osteotomy, for correction of mandibular excess.

MATERIALS AND METHODS Seventeen patients (10 males, 7 females, mean age: 22.5  2.4 years) requiring correction for mandibular excess were recruited, from June 2001 through December 2003, to participate in this longitudinal study, and informed consent was obtained from all subjects. Inclusion criteria of the patient group (PG) were as follows: (1) skeletal and dental class III;18 (2) anterior and posterior bilateral cross bite; (3) absence of fixed or removable dental prosthesis; (4) absence of periodontal disease; and (5) presence of all teeth (with the exception of the third molars, which were routinely extracted at the beginning of treatment, if present). Subjects with craniofacial syndromes or clefts were excluded from this study. Each patient received preoperative and postoperative orthodontic treatment (mean duration 36  12 months) with fixed appliances. All the patients underwent surgery by the same 2 surgeons, who had over 10 years of experience in orthognathic surgery. Nine patients received bilateral sagittal split osteotomy (BSSO) to reduce mandibular excess and 8 patients received combined BSSO and LeFort I osteotomy for maxillary advancement. In all cases, fixation of the mandibular segments was performed with 1 titanium individually bent miniplate and 4 monocortical screws per side, whereas the maxilla was fixed with 4 miniplates. Intra-operative manual seating of the condyle in the passive dorsocranial position in the glenoid fossa was performed in all cases, whereas the distal fragment was held in planned occlusion with temporary intermaxillary fixation. No postoperative intermaxillary fixation was used, light guidance elastics were placed to maintain the ideal occlusion for 2 weeks and a soft diet was suggested for 4 weeks. EMG recordings were obtained from 4 channels of the 8-channel electromyograph FREELY (DeGoetzen spa, Olgiate Olona, VA, Italy). The analogic EMG signal was amplified, digitized, and digitally filtered. The instrument was interfaced with a computer for data storage and subsequent analysis (EMA software, DeGoetzen spa). The signal was assessed as the

Fig. 1. Comparison of activity index, asymmetry index, and torque index before (T0) and after (T1) orthodontic treatmentesurgical correction of severe skeletal class III patients.

root mean square of the amplitude. Four electrodes (Duotrode silver/silver chloride EMG electrodes; Myotronics Inc., Tukwila, WA, USA) were located on the MM and TA muscles of both sides with an interelectrode distance of 20 mm. Before electrode placement, the skin was cleaned with ethanol. The location of the electrodes was based on anatomical landmarks.19 The EMG data of the right and left MM and TA muscles were evaluated during clenching in the PG at baseline (T0), and 6-8 months (T1) after completing the surgicaleorthodontic treatment. Following were the EMG parameters considered8: - Activity index (range between 100% and þ100%): positive values indicate an MM dominance and negative values indicate TA muscle dominance. The normal value during clenching of the activity index is 15%  9%. - Asymmetry index (range between 100% and þ100%): positive values indicate a stronger right side muscular activity and negative values indicate a stronger left side muscular activity. The normal value during clenching of the activity index is 9.37%  7.43%. - Torque index (range between 100% and þ100%): positive values indicate a stronger right side resultant force and negative values indicate a stronger left side resultant force. The normal value during clenching of the activity index is 9.47%  7.19%. Reference values used were suggested by Ferrario et al.8 The statistical analysis was performed with the Student t test to compare data before (T0) and after (T1) therapy.

RESULTS The results showed (Figure 1): - a significant difference in the value of activity index at T0-T1 (33% T0, 1% T1) (P < .05);

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Fig. 2. Intra-oral photographs before (A) and after (B) orthodontic treatmentesurgical correction of severe skeletal class III patients. Example of percentage of EMG activity before (C) and after (D) therapy.

- a significant difference in the value of asymmetry index at T0-T1 (21% T0, 4% T1) (P < .05); and - a significant difference in the value of torque index at T0-T1 (24% T0, 5% T1) (P < .05).

DISCUSSION This preliminary study evaluated the EMG activity of MM and TA muscles before and after mandibular setback via BSSO, with or without LeFort I osteotomy, in skeletal class III patients. This analysis provides following indications: (1) how skeletal and dental malocclusion influences the EMG activity before and after surgery, and (2) the muscular adaptation of the masticatory system after orthognathic surgery. Previous studies report some specific types of malocclusion, included dental and skeletal class III to be significantly associated with signs and symptoms of temporomandibular disorders (TMD),20-22 including muscular functionality23,24; moreover, in literature the influence of surgicaleorthodontic treatment on the muscular activity3,10,13,16,17,25,26 has been studied. In our study we evaluated the activity index, the asymmetry index, and the torque index before and after orthognathic surgery. As reported in the literature, activity index and asymmetry index give us useful information about patients with craniomandibular disorders27 or after modifications of the occlusal surfaces.28,29 Subjects with craniomandibular disorders showed a higher level of the asymmetry,30 (higher in MM than TA muscles); whereas subjects with no signs and symptoms of TMD had a higher level of asymmetry with a low muscle activity (rest position and centric occlusion conditions) and a lower level of

asymmetry during maximum clench,8 higher in MM than TA muscles. Ferrario et al.8 also described that the MM and TA muscle asymmetries have opposite signs and this phenomenon produces a couple of force with a laterodeviating effect on the mandible called torque. In normal subjects the torque index had a minimum value during clenching (<10%). In our study the results are in agreement with the literature8,30; in fact before therapy the activity index, the asymmetry index, and the torque index were abnormal (33%, 21%, and 24%, respectively), after therapy the EMG values are normal and similar to Ferrario reference values.8 These findings are similar to the results of some authors16,17,26 that evaluated surgical class III patients, and different from other authors,10-13 but these authors evaluated surgical class II patients. This muscular improvement suggests that the masticatory muscles and generally the whole masticatory system maintains adaptive capability in adults,31 and that the surgical correction of skeletal class III patients improves occlusion and masticatory muscles balance (Figure 2). A balanced EMG activity during clenching is considered a sign of good adaptation of the neuromuscular system to the new occlusal condition32; evaluation of EMG activity after surgery may be considered a good method for detecting nonresponding patients who might require further treatment. Further controls and long-term evaluation of these patients are necessary to confirm the reported changes. REFERENCES 1. Proffit WR, White RP Jr, Sarver MD. Contemporary Treatment of Dentofacial Deformity. Elsevier Health Sciences; 2002:2.

OOOO Volume 116, Number 4 2. Tulloch JF, Phillips C, Koch G, Proffit WR. The effect of early intervention on skeletal pattern in class II malocclusion: a randomized clinical trial. Am J Orthod Dentofacial Orthop. 1997;111:391-400. 3. Raustia AM, Oikarinen KS. Changes in electric activity of masseter and temporal muscles after mandibular sagittal split osteotomy. Int J Oral Maxillofac Surg. 1994;23:180-184. 4. Ingervall B, Ridell A, Thilander B. Changes in activity of the temporal, masseter and lip muscles after surgical correction of mandibular prognathism. Int J Oral Surg. 1979;8:290-300. 5. Magnusson T, Ahlborg G, Svartz K. Function of the masticatory system in 20 patients with mandibular hypo- or hyperplasia after correction by a sagittal split osteotomy. Int J Oral Maxillofac Surg. 1990;19:289-293. 6. Youssef RE, Throckmorton GS, Ellis E 3rd, Sinn DP. Comparison of habitual masticatory cycles and muscles activity before and after orthognathic surgery. J Oral Maxillofac Surg. 1997;55:699-707. 7. Castroflorio T, Bracco P, Farina D. Surface electromyography in the assessment of jaw elevator muscles. J Oral Rehabil. 2008;35: 638-645. 8. Ferrario VF, Sforza C, Milani A Jr, D’Addona A, Barbini E. Electromyography activity of human masticatory muscles in normal young people. Statistical evaluation of reference values for clinical applications. J Oral Rehabil. 1993;20:271-280. 9. Tate GS, Throckmorton GS, Ellis E 3rd, Sinn DP. Masticatory performance, muscle activity, and occlusal force in pre-orthognathic surgery patients. J Oral Maxillofac Surg. 1994;52:476-481. 10. Kobayashi T, Honma K, Shingaki S, Nakajima T. Changes in masticatory function after orthognathic treatment in patients with mandibular prognathism. Br J Oral Maxillofac Surg. 2001;39: 260-265. 11. Tate GS, Throckmorton GS, Ellis E 3rd, Sinn DP, Blackwood DJ. Estimated masticatory forces in patients before orthognathic surgery. J Oral Maxillofac Surg. 1994;52:130-136. 12. Harper RP, de Bruin H, Burcea I. Muscle activity during mandibular retrognathic subjects. J Oral Maxillofac Surg. 1997;55:225-233. 13. van der Braber W, van der Glas HW, van der Bilt A, Bosman F. Masticatory function in retrognathic patients, before and after mandibular advancement surgery. J Oral Maxillofac Surg. 2004;62:549-554. 14. Zarrinkelk HM, Throckmorton GS, Ellis E 3rd, Sinn DP. Functional and morphologic alterations secondary to superior repositioning of the maxilla. J Oral Maxillofac Surg. 1995;53:1258-1267. 15. van der Braber W, van der Bilt A, van der Glas HW, Rosenberg T, Koole R. The influence of mandibular advancement surgery on oral function in retrognathic patients: 5 years follow-up study. J Oral Maxillofac Surg. 2006;64:1237-1240. 16. Di Palma E, Gasparini G, Pelo S, Tartaglia GM, Chimenti C. Activities of masticatory muscles in patients after orthognathic surgery. J Craniomaxillofac Surg. 2009;37:417-420. 17. Trawitzki LVV, Dantas RO, Mello-Filho FV, Marques W Jr. Masticatory muscle function three years after surgical correction of class III dentofacial deformity. Int J Oral Maxillofac Surg. 2010;39:853-856. 18. Bracco P, Vercellino V. Classificazione basale di 150 soggetti disgnatici secondo ricketts, Steiner e Cervera. Minerva Stomatol. 1980;1:1-38.

ORIGINAL ARTICLE Frongia et al. 401 19. Castroflorio T, Icardi K, Becchino B, et al. Reproducibility of surface EMG variables in isometric sub-maximal contractions of jaw elevator muscles. J Electromyogr Kinesiol. 2006;16: 498-505. 20. McNamara JA Jr, Seligman DA, Okeson JP. Occlusion, orthodontic treatment, and temporomandibular disorders: a review. J Orofac Pain. 1995;9:73-90. 21. Pullinger AG, Seligman DA. Quantification and validation of predictive values of occlusal variables in temporomandibular disorders using a multifactorial analysis. J Prosthet Dent. 2000;84:114-115. 22. Thilander B, Rubio G, Pena L, Mayorga C. Prevalence of temporomandibular disorders and its association with malocclusion in children and adolescents: an epidemiologic study related to specific stages of dental development. Angle Orthod. 2002;72: 146-154. 23. Kim YG, Oh SH. Effect of mandibular setback surgery on occlusal force. J Oral Maxillofac Surg. 1997;55:121-126. 24. Throckmorton GS, Buschang PH, Ellis E 3rd. Improvement of maximum occlusal forces after orthognathic surgery. J Oral Maxillofac Surg. 1996;54:1080-1086. 25. Eckardt L, Harzer W, Schneevoigt R. Comparative study of excitation patterns in the masseter muscle before and after orthognathic surgery. J Craniomaxillofac Surg. 1997;25:344-352. 26. Sforza C, Peretta R, Grandi G, Ferronato G, Ferrario VF. Soft tissue facial planes and masticatory muscle function in skeletal class III patients before and after orthognathic surgery treatment. J Oral Maxillofac Surg. 2008;66:691-698. 27. Humsi ANK, Naeije M, Hippe JA, Hansson TL. The immediate effects of a stabilization splint on the muscular symmetry in the masseter and anterior temporalis muscles of patients with a craniomandibular disorders. J Prosthet Dent. 1989;62:339-343. 28. McCarroll RS, Naeije M, Hippe JA, Hansson TL. The immediate effect of splint-induced changes in jaw positioning on the asymmetry of submaximal masticatory muscle activity. J Oral Rehab. 1989;16:163-170. 29. McCarroll RS, Naeije M, Hippe JA, Hansson TL. Short-term effect of a stabilization in splint on the asymmetry of submaximal masticatory muscle activity. J Oral Rehab. 1989;16:171-176. 30. Naeije M, McCarroll RS, Weijs WA. Electromyographic activity of the human masticatory muscles during submaximal clenching in the intercuspal position. J Oral Rehab. 1989;16:63-70. 31. Piancino MG, Frongia G, Dalessandri D, Bracco P, Ramieri G. Reverse cycle chewing before and after orthodonticesurgical correction in class III patients. Oral Surg Oral Med Oral Pathol Oral Radiol; 2012. 32. Ferrario VF, Sforza C, Colombo A, Ciusa V. An electromyographic investigation of masticatory muscles symmetry in normoocclusion subjects. J Oral Rehabil. 2000;27:33-40. Reprint requests: Gianluigi Frongia, DDS, DOS, PhD Department of Orthodontics and Gnathology Dental School, University of Turin, Via Nizza 230 10126 Torino, Italy [email protected]