External location of the buccinator muscle to facilitate electromyographic analysis

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1B3r0az Dent J (2008) 19(2): 130-133 R.H.B. Tavares da Silva et al. ISSN 0103-6440 External Location of the Buccinator Muscle to Facilitate Electromyographic Analysis Regina Helena Barbosa TAVARES DA SILVA1 Hélio Ferraz PORCIÚNCULA2 Renata Savastano Ribeiro JARDINI3 Ana Paula Gonçalves PITA1 Ana Paula Dias RIBEIRO1 1Department of Dental Materials and Prosthodontics, Dental School of Araraquara, São Paulo State University, Araraquara, SP, Brazil 2Department of Morphology, Dental School of Araraquara, São Paulo State University, Araraquara, SP, Brazil 3Speech Therapist, Medical School of São Paulo, Federal University of São Paulo, São Paulo, SP, Brazil Electromyography is frequently used to measure the activity of masticatory muscles. It requires the precise setting of the electrodes, which demands the accurate location of the muscle to be evaluated. The purpose of this study was to investigate the accuracy of an external method to locate the buccinator muscle. Fifteen human cadavers were evaluated and planes were determined on the face using anatomic landmarks. An angle (α) was obtained at the intersection of these planes on the central point of buccinator muscle and measured with a protractor. The value of the angle allows locating the central point of buccinator muscle based on anatomic landmarks on the face. Statistical analysis of the collected data indicated an angle of 90º with 95% reliability, thus proving the efficacy of the proposed method. Key Words: facial muscles, buccinator muscle, electromyography. INTRODUCTION The buccinator muscle is a plain, square-shaped bilateral mimic muscle, which composes the mobile and adaptable portion of the cheek. It is frequently referred to as an accessory muscle of mastication because of its role on chewing food and swallowing and compressing the cheeks against the molars, as well as its use for whistling, sucking and blowing. The buccinator muscle gradually contracts during mouth closing and relaxes during mouth opening, maintaining the required tension of the cheeks, in order to avoid biting on the jugal mucosa (1,2). This muscle has different origins: the pterygomandibular raphe and the buccal alveolar bone of maxillary and mandibular molars. First, it originates from a fibrous bundle (the pterygomandibular raphe), which runs from the pterygoid hamulus on the inferior portion of the medial surface of the mandible close to the posterior portion of the mylohyoid line. The pterygomandibular raphe connects the anterior portion of the superior constrictor muscle of the pharynx with the posterior portion of the buccinator (1,2). From the two bone origins (buccal alveolar bone of maxillary and mandibular molars) and from the pterygomandibular raphe, the fibers of the buccinator muscle run anteriorly, forming the musculature of the cheek. They blend with the fibers of the orbicularis oris at the corners of the mouth (Fig. 1). While its central fibers run ahead, its upper fibers and the lower fibers join the fibers of the orbicular muscle of mouth in the lower lip and upper lip, respectively. Buccinator innervation comes from both portions of the facial (7th pair of cranial nerves), temporofacial and cervicofacial nerves (1-3). In some individuals, the facial muscles, including the chewing muscles, present parafunctional activities Correspondence: Profa. Dra. Regina Helena Barbosa Tavares da Silva, Departamento de Materiais Odontológicos e Prótese, Faculdade de Odontologia de Araraquara, UNESP, Rua Humaitá, 1680, 14801-903 Araraquara, SP, Brasil. Tel: +55-16-3301-6406. Fax: +55-163301-6406. e-mail: Braz Dent J 19(2) 2008 External location of the buccinator muscle 131 in addition to the normal functional action. Unlike the functional activities, the parafunctional ones are not controlled and cause damage to the adjacent structures (4). Bruxism is a well known parafunctional habit defined as the non-functional dental contact characterized by grinding and/or clenching of teeth (5) during sleep or while awake (4). The actual causes of these disturbances have not yet been clarified, but parafunction is believed to have occlusal, psychological and/or central nervous system origins (4,6,7). Individuals with bruxism presents increased electrical activity of the chewing musculature (buccinator, temporomandibular, masseter and pterygoid muscles) (8), and thus a possible indirect involvement of the buccinator muscle in parafunctional habits has been suggested (7). Numerous studies relating to facial expression, pronunciation, swallowing, sucking, blowing, mandibular movements and mastication have been conducted with the buccinator muscle (9). However, there are no studies proving the electrical activity alterations of the buccinator muscle during the occurrence of these habits. Electromyography (EMG) is the study of mus- cular function by recording electrical signs propagated in the muscles (10). These records are done by accurately placing electrodes at the exact point corresponding to the external location of the muscle whose electrical activity should be measured. EMG analysis is currently a practical and efficient method to detect the occurrence of alterations in the electrical activity of muscles involved in parafunctional habits. The aim of this study was to investigate the accuracy of an external method to locate the buccinator muscle using landmarks. MATERIAL AND METHODS Fifteen formalin-fixed adult human cadaver heads belonging to the Department of Morphology, Dental School of Araraquara, São Paulo State University, Brazil, were used in this study. Three landmarks were first determined in a hemiface (Fig. 1): Point A: eye external angle; Point B: labial angle; Point C: external point corresponding to the central point of buccinator muscle. Points A and B (Fig. 2) were easily demarcated by positioning pins on the Figure 1. Buccinator muscle. Figure 2. Schematic drawing showing the 3 landmarks (A, B and C) demarcated on a hemi-face for location of the buccinator muscle. Braz Dent J 19(2) 2008 132 R.H.B. Tavares da Silva et al. respective anatomic landmarks. The C point was demarcated (Fig. 2) by the inner location of the central point of buccinator muscle by means of skin detachment for external pin fixation. Two planes were determined: AC plane: vertical plane that passes simultaneously through points A and C, with the operator at 45º in relation to the sagital plane of the anatomic specimen; BC plane: horizontal plane, that passes simultaneously through points B and C. An angle was obtained at the intersection of these planes (α angle; Fig. 2), measured with a protractor and its values were tabulated for further statistical analysis. Data were analyzed statistically by ANOVA and Tukey test at 5% significance level. Hanawa et al. (9), in a recent study, used electrode location techniques based on the activity of the central site of the cheek. They evaluated the EMG activity recorded from the anterior, central and posterior sites of the cheek. The anterior and posterior sites had interference from other muscles, and the central site showed a remarkable activity when laughing and contaminations of the action potential of other muscles were not observed (9). The location method proposed in the present study, which is based on external facial points, was proved effective by the statistical analysis. The tested method accurately located the central point of the buccinator muscle, which allows a precise positioning RESULTS of the electrodes for EMG analysis. The findings of this experiment showed that the use of anatomic facial Table 1 presents the α angle values obtained at the intersection of planes AC and BC, according to the proposed methodology. The average of the α angle values was 90.33° with a standard deviation of 5.30°. The confidence interval for the average is defined by the landmarks allowed determining the exact point for electrode positioning with 95% degree of reliability. The proposed method offers a simple and non-invasive technique to locate the buccinator muscle for placement of surface electrodes in EMG studies. upper and lower limits, depending on both the t value (tabulated and varying with the number of observations) and the average standard error, which, in this case, was 1.37°. While the standard deviation is a Table 1. Angle (α) obtained at the intersection of planes AC and BC in each anatomic specimen, according to the proposed methodology. measure of original data variability, the stan- Specimen 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 dard error is a measure of the average distribution variability. So, in this study, the angle value Angle 87º 91º 92º 93º 95º 86º 84º 90º 88º 85º 99º 84º 102º 91º 88º obtained from data was 90.33° ± 5.30° and the confidence interval for the average was 90.33° ± 2.96°, for observations with 95% confidence level. This means that the researcher depos- RESUMO its a reliability of 95% that the average value of the angle at issue in an unknown population was in the 93.29° to 87.37° range. Therefore, with a reliability level of 95%, A eletromiografia é frequentemente utilizada para mensurar a atividade dos músculos mastigatórios. Esta análise exige a the angle was considered as being of 90° (13). colocação precisa dos eletrodos, o que requer a localização exata do músculo a ser avaliado. O objetivo do presente estudo foi DISCUSSION investigar a acurácia de um método externo para localização do músculo bucinador. Quinze cadáveres humanos foram avaliados The position of the electrodes for EMG studies of the buccinator muscle used to be determined by the position of certain teeth, such as the second molar (11) and the first molar (12). This technique, however, is limited because the teeth used as a reference can be in e planos foram determinados na face utilizando-se pontos de referência anatômicos. Um ângulo (α) foi obtido na interseção desses planos no ponto central do músculo bucinador e foi medido com um transferidor. O valor do ângulo permite localizar o ponto central do músculo bucinador baseado nos pontos de referência anatômicos da face. A análise estatística dos dados obtidos indicou um ângulo de 90º com 95% de confiabilidade, different positions or can even be absent. confirmando dessa forma a eficácia do método proposto. Braz Dent J 19(2) 2008 External location of the buccinator muscle 133 ACKNOWLEDGEMENTS The authors would like to thank Dr. Lydia S. R. Ruiz for the statistical analysis and Mr. Marcelo Brito Conte for his technical assistance at the Laboratory of Anatomy of the School of Dentistry of Araraquara, São Paulo State University, Brazil. REFERENCES 1 . D’Andrea E, Barbaix E. Anatomic research on the perioral muscles, functional matrix of the maxillary and mandibular bones. Surg Radiol Anat 2006;28:261-266. 2 . Plas E, Deliac P, Garuet Lempirou A, Caix P, Bioulac B. The buccinator muscle: an original morphogenetical study. Morphologie 2004;88:27-30. 3 . Vitti M, Basmajian JV, Ouellette PL, Mitchell DL, Eastmen WP, Seaborn RD. Electromyographic investigations of the tongue and circumoral muscular sling with fine-wire electrodes. J Dent Res 1975;54:844-849. 4 . Takemura T, Takahashi T, Fukuda M, Ohnuki T, Asunuma T, Masuda Y et al. A psychological study on patients with masticatory muscle disorder and sleep bruxism. Cranio 2006;24:191-196. 5 . Pierce CJ, Chrisman K, Bennett ME, Close JM. Stress, anticipatory stress, and psychologic measures related to sleep bruxism. J Orofac Pain 1995;9:51-56. 6 . Koyano K, Tsukiyama Y, Ichiki R. Local factors associated with parafunction and prosthodontics. Int J Prosthodont 2005;18:293-294. 7. Trenouth MJ. Undefined relationships. Br Dent J 2007;202:644. 8 . Ahlgren J. EMG studies of lip and cheek activity in sucking habits. Swed Dent J 1995;19:95-101. 9 . Hanawa S, Tsuboi A, Watanabe M, Sasaki K. EMG study for perioral facial muscles function during mastication. J Oral Rehab 2008;35:159-170. 10. Basmajian JV, Luca LJ. Muscles Alive: their functions revealed by electromyography. 5th ed. Baltimore: Willians & Wilkins; 1985. 11. Basmajian JV, Newton WJ. Feedback training of parts of buccinator muscle in man. Psychophysiol 1974;11:92-92. 12. Lundquist DO. An electromyographic analysis of the function of the buccinator muscle as an aid to denture retention and stabilization. J Prosthet Dent 1959;9:44-52. Accepted March 17, 2008 Braz Dent J 19(2) 2008 equilibrium value of MeCpG steps (,+14 deg.) [31,44]. In comparison, methylation has a significantly lower stability cost when happening at major groove positions, such as 211 and 21 base pair from dyad (mutations 9 and 12), where the roll of the nucleosome bound conformation (+10 deg.) is more compatible with the equilibrium geometry of MeCpG steps. The nucleosome destabilizing effect of cytosine methylation increases with the number of methylated cytosines, following the same position dependence as the single methylations. The multiple-methylation case reveals that each major groove meth- PLOS Computational Biology | 3 November 2013 | Volume 9 | Issue 11 | e1003354 DNA Methylation and Nucleosome Positioning ylation destabilizes the nucleosome by around 1 kJ/mol (close to the average estimate of 2 kJ/mol obtained for from individual methylation studies), while each minor groove methylation destabilizes it by up to 5 kJ/mol (average free energy as single mutation is around 6 kJ/mol). This energetic position-dependence is the reverse of what was observed in a recent FRET/SAXS study [30]. The differences can be attributed to the use of different ionic conditions and different sequences: a modified Widom-601 sequence of 157 bp, which already contains multiple CpG steps in mixed orientations, and which could assume different positioning due to the introduction of new CpG steps and by effect of the methylation. The analysis of our trajectories reveals a larger root mean square deviation (RMSD) and fluctuation (RMSF; see Figures S2– S3 in Text S1) for the methylated nucleosomes, but failed to detect any systematic change in DNA geometry or in intermolecular DNA-histone energy related to methylation (Fig. S1B, S1C, S4–S6 in Text S1). The hydrophobic effect should favor orientation of the methyl group out from the solvent but this effect alone is not likely to justify the positional dependent stability changes in Figure 2, as the differential solvation of the methyl groups in the bound and unbound states is only in the order of a fraction of a water molecule (Figure S5 in Text S1). We find however, a reasonable correlation between methylation-induced changes in hydrogen bond and stacking interactions of the bases and the change in nucleosome stability (see Figure S6 in Text S1). This finding suggests that methylation-induced nucleosome destabilization is related to the poorer ability of methylated DNA to fit into the required conformation for DNA in a nucleosome. Changes in the elastic deformation energy between methylated and un-methylated DNA correlate with nucleosomal differential binding free energies To further analyze the idea that methylation-induced nucleosome destabilization is connected to a worse fit of methylated DNA into the required nucleosome-bound conformation, we computed the elastic energy of the nucleosomal DNA using a harmonic deformation method [36,37,44]. This method provides a rough estimate of the energy required to deform a DNA fiber to adopt the super helical conformation in the nucleosome (full details in Suppl. Information Text S1). As shown in Figure 2, there is an evident correlation between the increase that methylation produces in the elastic deformation energy (DDE def.) and the free energy variation (DDG bind.) computed from MD/TI calculations. Clearly, methylation increases the stiffness of the CpG step [31], raising the energy cost required to wrap DNA around the histone octamers. This extra energy cost will be smaller in regions of high positive roll (naked DNA MeCpG steps have a higher roll than CpG steps [31]) than in regions of high negative roll. Thus, simple elastic considerations explain why methylation is better tolerated when the DNA faces the histones through the major groove (where positive roll is required) that when it faces histones through the minor groove (where negative roll is required). Nucleosome methylation can give rise to nucleosome repositioning We have established that methylation affects the wrapping of DNA in nucleosomes, but how does this translate into chromatin structure? As noted above, accumulation of minor groove methylations strongly destabilizes the nucleosome, and could trigger nucleosome unfolding, or notable changes in positioning or phasing of DNA around the histone core. While accumulation of methylations might be well tolerated if placed in favorable positions, accumulation in unfavorable positions would destabilize the nucleosome, which might trigger changes in chromatin structure. Chromatin could in fact react in two different ways in response to significant levels of methylation in unfavorable positions: i) the DNA could either detach from the histone core, leading to nucleosome eviction or nucleosome repositioning, or ii) the DNA could rotate around the histone core, changing its phase to place MeCpG steps in favorable positions. Both effects are anticipated to alter DNA accessibility and impact gene expression regulation. The sub-microsecond time scale of our MD trajectories of methylated DNAs bound to nucleosomes is not large enough to capture these effects, but clear trends are visible in cases of multiple mutations occurring in unfavorable positions, where unmethylated and methylated DNA sequences are out of phase by around 28 degrees (Figure S7 in Text S1). Due to this repositioning, large or small, DNA could move and the nucleosome structure could assume a more compact and distorted conformation, as detected by Lee and Lee [29], or a slightly open conformation as found in Jimenez-Useche et al. [30]. Using the harmonic deformation method, we additionally predicted the change in stability induced by cytosine methylation for millions of different nucleosomal DNA sequences. Consistently with our calculations, we used two extreme scenarios to prepare our DNA sequences (see Fig. 3): i) all positions where the minor grooves contact the histone core are occupied by CpG steps, and ii) all positions where the major grooves contact the histone core are occupied by CpG steps. We then computed the elastic energy required to wrap the DNA around the histone proteins in unmethylated and methylated states, and, as expected, observed that methylation disfavors DNA wrapping (Figure 3A). We have rescaled the elastic energy differences with a factor of 0.23 to match the DDG prediction in figure 2B. In agreement with the rest of our results, our analysis confirms that the effect of methylation is position-dependent. In fact, the overall difference between the two extreme methylation scenarios (all-in-minor vs all-in-major) is larger than 60 kJ/mol, the average difference being around 15 kJ/ mol. We have also computed the elastic energy differences for a million sequences with CpG/MeCpG steps positioned at all possible intermediate locations with respect to the position (figure 3B). The large differences between the extreme cases can induce rotations of DNA around the histone core, shifting its phase to allow the placement of the methylated CpG steps facing the histones through the major groove. It is illustrative to compare the magnitude of CpG methylation penalty with sequence dependent differences. Since there are roughly 1.5e88 possible 147 base pairs long sequence combinations (i.e., (4n+4(n/2))/2, n = 147), it is unfeasible to calculate all the possible sequence effects. However, using our elastic model we can provide a range of values based on a reasonably large number of samples. If we consider all possible nucleosomal sequences in the yeast genome (around 12 Mbp), the energy difference between the best and the worst sequence that could form a nucleosome is 0.7 kj/mol per base (a minimum of 1 kJ/mol and maximum of around 1.7 kJ/mol per base, the first best and the last worst sequences are displayed in Table S3 in Text S1). We repeated the same calculation for one million random sequences and we obtained equivalent results. Placing one CpG step every helical turn gives an average energetic difference between minor groove and major groove methylation of 15 kJ/ mol, which translates into ,0.5 kJ/mol per methyl group, 2 kJ/ mol per base for the largest effects. Considering that not all nucleosome base pair steps are likely to be CpG steps, we can conclude that the balance between the destabilization due to CpG methylation and sequence repositioning will depend on the PLOS Computational Biology | 4 November 2013 | Volume 9 | Issue 11 | e1003354 DNA Methylation and Nucleosome Positioning Figure 3. Methylated and non-methylated DNA elastic deformation energies. (A) Distribution of deformation energies for 147 bplong random DNA sequences with CpG steps positioned every 10 base steps (one helical turn) in minor (red and dark red) and major (light and dark blue) grooves respectively. The energy values were rescaled by the slope of a best-fit straight line of figure 2, which is 0.23, to source of circulating FGF-21. The lack of association between circulating and muscle-expressed FGF-21 also suggests that muscle FGF-21 primarily works in a local manner regulating glucose metabolism in the muscle and/or signals to the adipose tissue in close contact to the muscle. Our study has some limitations. The number of subjects is small and some correlations could have been significant with greater statistical power. Another aspect is that protein levels of FGF-21 were not determined in the muscles extracts, consequently we cannot be sure the increase in FGF-21 mRNA is followed by increased protein expression. In conclusion, we show that FGF-21 mRNA is increased in skeletal muscle in HIV patients and that FGF-21 mRNA in muscle correlates to whole-body (primarily reflecting muscle) insulin resistance. These findings add to the evidence that FGF-21 is a myokine and that muscle FGF-21 might primarily work in an autocrine manner. Acknowledgments We thank the subjects for their participation in this study. 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External location of the buccinator muscle to facilitate electromyographic analysis
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