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Influence of Breathing Modes and Facial Growth Patterns on Electromyographic Fatigue of Masticatory Muscles in Children

Abstract

Introduction

Changes in breathing patterns affect the harmonious development of the structures of the craniofacial system, leading to changes in posture, occlusion, and facial growth patterns. However, little is known about how these changes influence the muscle contraction patterns, either at rest or while functioning, and either in a normal or unbalanced condition.

Objective

To study the masseter and anterior temporal muscles fatigue during mastication in nasal- and mouth-breathing children, also considering their facial growth patterns. Methods: A total of 70 children aged 6 to 12 years old who met the study criteria were assessed. Speech-language-hearing, otorhinolaryngologic, and cephalometric assessments were performed to divide them into groups. In the electromyographic assessment, the children were asked to chew gum following a metronome until they felt fatigued. The median frequency of the muscles was analyzed at 15, 30, 45, and 60seconds of mastication.The reported time of fatigue perception was recorded. The data were analyzed with analysis of variance (ANOVA) and the Kruskal-Wallis and the Mann-Whitney U tests.

Results

There were no median frequency decrease patterns nor differences in the myoelectric manifestations and reported time of fatigue between the groups.

Conclusion

The masticatory muscles did not reveal fatigue in the electromyographic analysis; however, the fatigue time was reported, despite the absence of physiological fatigue. The breathing mode, the facial growth pattern, and the association between them did not interfere with the behavior of the median frequency of the electromyographic signal and the fatigue time perception.

Keywords
masticatory muscles; muscle fatigue; electromyography; mouth breathing; stomatognathic system

Introduction

Little is known so far about the contraction patterns of the facial and masticatory muscles, either in normal or unbalanced conditions.11 Vilela M, Picinato-Pirola MNC, Giglio LD, et al. Bite force in children with posterior crossbite. Audiol Commun Res 2017;22: e1723 In the case of mouth-breathers (MBs), the discussions mainly approach the clinical characteristics of the craniofacial, stomatognathic, and body adaptations, which even affect the quality of life of individuals.22 Bednarz C, Czlusniak GR, Bagarollo MF, Costa CC, de Alencar BLF. Orofacial profile of mouth breathing children previous to adenoidectomy and/or tonsillectomy. Distúrb Comun 2017;29:558–569,33 Souza AFMS, Vargas DS. Síndrome do Respirador Oral: Correlações Anatomoclínicas na integralidade da atenção básica em saúde. Revista Interdisciplinar Pensamento Científico 2019;5;,44 da Silva CFFS, Gomes VCA,VilasBoasLSS, Pezzin AC. Sleepchanges evaluation in children with mouth breathing syndrome. Revista Eletrônica Acervo Saúde. 2019;24:e637

Changes in the breathing mode are known to lead to various changes in the harmony and growth of the craniofacial structures, which result from compensations to make airflow easier. These changes include mandible posture and occlusal changes and influences on the facial growth pattern.55 Silva CR, Geres BS, Kuriki HU, Negrão Filho RF, Alves N, Azevedo FM. Analysis of reliability of EMG signal frequency domain parameters used in the characterization of localized muscle fatigue. Motriz Rev. Educ. Fís. 2012;18:456–464,66 Chambi-Rocha A, Cabrera-Domínguez ME, Domínguez-Reyes A. Breathing mode influence on craniofacial development and head posture. J Pediatr (Rio J) 2018;94(02):123–130,77 Souza V, Paço M, Pinho T. Implicações da Respiração Oral e Deglutição Atípica na Postura Corporal. Nascer e Crescer – Birth and Growth Medical Journal 2017;26:89–94,88 de Mattos FMGF. Orofacial myofunctional characteristics of oral and oronasal breathers. Rev CEFAC 2018;20:459–467,99 Batista DPF, Bargarollo MF. Surface electromyography in orofacial and cervical musculature in mouth breathing children: an inte-grative literature review. Rev CEFAC 2020;22:e19318

Some studies have shown that MBs typically have an elongated face,55 Silva CR, Geres BS, Kuriki HU, Negrão Filho RF, Alves N, Azevedo FM. Analysis of reliability of EMG signal frequency domain parameters used in the characterization of localized muscle fatigue. Motriz Rev. Educ. Fís. 2012;18:456–464 while others have found mesofacial1010 Biazzetto LC, Zenaro OS, Assencio-Ferreira VJ. Caracterização da Tipologia Facial em indivíduos portadores de hipertrofia das tonsilas palatinas. Rev CEFAC 2001;3:123–126,1111 Frasson JMD, Magnani MBBA, Nouer DF, de Siqueira VC, Lunardi N. Comparative cephalometric study between nasal and predominantly mouth breathers. Rev Bras Otorrinolaringol (Engl Ed) 2006;72(01):72–81 and brachyfacial growth patterns1212 Busanello-Stella AR, Blanco-Dutra AP, Corrêa ECR, Silva AMT. Electromyographic fatigue of orbicular oris muscles during exercises in mouth and nasal breathing children. CoDAS 2015;27(01): 80–88 as a characteristic of this population. All these imbalances may potentialize speech,1313 Borox T, Leite APD, Bagarollo MF, Alencar Bde, Czlusniak GR. Speech production assessment of mouth breathing children with hypertrophy of palatines and/or pharyngeal tonsils. Rev CEFAC 2018;20:468–477 swallowing,22 Bednarz C, Czlusniak GR, Bagarollo MF, Costa CC, de Alencar BLF. Orofacial profile of mouth breathing children previous to adenoidectomy and/or tonsillectomy. Distúrb Comun 2017;29:558–569,99 Batista DPF, Bargarollo MF. Surface electromyography in orofacial and cervical musculature in mouth breathing children: an inte-grative literature review. Rev CEFAC 2020;22:e19318 and mastication changes.99 Batista DPF, Bargarollo MF. Surface electromyography in orofacial and cervical musculature in mouth breathing children: an inte-grative literature review. Rev CEFAC 2020;22:e19318,1414 Silva MAA, Natalini V, Ramires RR, Ferreira LP. Comparative analysis of mastication in children with nasal and mouth breathing with first teething. Rev CEFAC 2007;9:190–198,1515 Nagaiwa M, Gunjigake K, Yamaguchi K. The effect of mouth breathing on chewing efficiency. Angle Orthod 2016;86(02): 227–234

Regarding mastication, specifically, mouth breathing may impair its efficiency. Because of the need to breathe through the mouth, mastication is interrupted, and the person takes longer to finish the masticatory movements. Changes in lip posture and masticatory muscle action (which is often underused) also appear when eating.99 Batista DPF, Bargarollo MF. Surface electromyography in orofacial and cervical musculature in mouth breathing children: an inte-grative literature review. Rev CEFAC 2020;22:e19318,1414 Silva MAA, Natalini V, Ramires RR, Ferreira LP. Comparative analysis of mastication in children with nasal and mouth breathing with first teething. Rev CEFAC 2007;9:190–198,1515 Nagaiwa M, Gunjigake K, Yamaguchi K. The effect of mouth breathing on chewing efficiency. Angle Orthod 2016;86(02): 227–234 However, the literature disagrees whether the masseter and temporal muscles are hypofunctional in MBs,1414 Silva MAA, Natalini V, Ramires RR, Ferreira LP. Comparative analysis of mastication in children with nasal and mouth breathing with first teething. Rev CEFAC 2007;9:190–198,1616 Boton LM, Silva AMT, Bolzan GP, Corrêa ECR, Busanello AR. Electromyographic study on facial muscles of nasal breathers, obstructive and vicious oral breathers. Rev CEFAC 2011;13:27–34 and little is known about the extent to which this musculature can be required while maintaining an efficient motor performance.1717 Silva BARS, Martínez FG, Pacheco AM, Pacheco I. Effects of the exercise-induced muscular fatigue on the time of muscular reaction of the fibularis in healthy individuals. Rev Bras Med Esporte 2006;12:85–89 Hence, researching this muscle fatigue can help understand this issue.

Muscle fatigue, which is a natural muscle mechanism, occurs when it is incapable of maintaining high force levels over time.1717 Silva BARS, Martínez FG, Pacheco AM, Pacheco I. Effects of the exercise-induced muscular fatigue on the time of muscular reaction of the fibularis in healthy individuals. Rev Bras Med Esporte 2006;12:85–89,1818 De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163,1919 Cram JR, Kasman GS, Holtz J. Introduction to Surface Electromyography. Maryland: Aspen Publishers; 1998,2020 Oliveira JHP, Dourado FMG, Lima NS, Silva HJ, Marcelino FM. Relationship of the thickness and electric activity of the masseter muscle with bite force: a morphological and electrophysiological study. Rev CEFAC 2016;18:589–600,2121 Oliveira LF, Palinkas M, Vasconcelos PB, et al. Influence of age on the electromyographic fatigue threshold of the masseter and temporal muscles of healthy individuals. Arch Oral Biol 2017; 84:1–5 The fatigue depends on the type, duration, and intensity of the exercise; the muscle fiber type; the training level of the individual; and the environmental conditions where the exercise is performed.55 Silva CR, Geres BS, Kuriki HU, Negrão Filho RF, Alves N, Azevedo FM. Analysis of reliability of EMG signal frequency domain parameters used in the characterization of localized muscle fatigue. Motriz Rev. Educ. Fís. 2012;18:456–464 This variable can be analyzed through electrical activity patterns, mainly obtained with surface electromyography (EMG) by means of isometric contractions, which causes this phenomenon more easily11 Vilela M, Picinato-Pirola MNC, Giglio LD, et al. Bite force in children with posterior crossbite. Audiol Commun Res 2017;22: e1723,2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167,2323 Tomonari H, Seong C, Kwon S, Miyawaki S. Electromyographic activity of superficial masseter and anterior temporal muscles during unilateral mastication of artificial test foods with different textures in healthy subjects. Clin Oral Investig 2019;23(09): 3445–3455–although usual isotonic situations are also investigated.11 Vilela M, Picinato-Pirola MNC, Giglio LD, et al. Bite force in children with posterior crossbite. Audiol Commun Res 2017;22: e1723,2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167,2323 Tomonari H, Seong C, Kwon S, Miyawaki S. Electromyographic activity of superficial masseter and anterior temporal muscles during unilateral mastication of artificial test foods with different textures in healthy subjects. Clin Oral Investig 2019;23(09): 3445–3455 Isotonicity nears the usual training of the masticatory muscles,2424 Pinheiro DLDSA, Alves GÂDS, Fausto FMM, et al. Effects of electrostimulation associated with masticatory training in individuals with down syndrome. CoDAS 2018;30(03):e20170074,2525 Prado DGA, Berretin-Felix G, Migliorucci RR, et al. Effects of orofacial myofunctional therapy on masticatory function in individuals submitted to orthognathic surgery: a randomized trial. J Appl Oral Sci 2018;26:e20170164 which is why the present study seeks to investigate this situation more in depth.

One of the ways to measure muscle fatigue is the analysis of the EMG frequency spectrum, more specifically the median frequency (MF), which is an objective measure of the muscle fatigue process.2626 Wanshi Arnoni V, Batista de Vasconcelos P, Sousa LG, et al. Evaluation of the electromyographic fatigue of the masseter and temporalis muscles in individuals with osteoporosis. Cranio 2019;37(04):254–263 Much research approaching different pathologies has studied the muscle fatigue threshold. Using MF enables the verification of muscle susceptibility to induced physiological fatigue - that is, the desired force production momentum can no longer be maintained, and contractile fatigue is observed.2121 Oliveira LF, Palinkas M, Vasconcelos PB, et al. Influence of age on the electromyographic fatigue threshold of the masseter and temporal muscles of healthy individuals. Arch Oral Biol 2017; 84:1–5,2626 Wanshi Arnoni V, Batista de Vasconcelos P, Sousa LG, et al. Evaluation of the electromyographic fatigue of the masseter and temporalis muscles in individuals with osteoporosis. Cranio 2019;37(04):254–263

Surface EMG is an important tool in the objective analysis of facial and masticatory muscle activity. Various methodologies are used to understand the signs and symptoms of muscle fatigue, making the analysis between results more difficult and, consequently, hindering the definition of parameters to choose orofacial muscle training exercises.2727 Gawda P, Ginszt M, Ginszt A, Pawlak H, Majcher P. Differences in myoelectric manifestations of fatigue during isometric muscle actions. Ann Agric Environ Med 2018;25(02):296–299

Thus, the objective of the present research is to study the fatigue, during mastication, of the masseter and anterior temporal muscles of nasal-breathing (NB) and MB children, also considering their facial growth patterns.

Methods

Sample

The present cross-sectional study encompassed 70 children. Of these, 36 were NBs (21 girls and 15 boys) and 34 were MBs (13 girls and 21 boys), aged 6 years and 0 months to 12 years and 11 months old (mean NB = 9.6 years ±22 months old; mean MB = 8.9 years ±21 months old). The inclusion criteria were as follows: presenting agreement between the speech-language-hearing and otorhinolaryngological diagnoses for MB and NB; having the permanent upper first molars already erupted; and having body mass index (BMI) within the normal range for the age.2828 Organização Mundial da Saúde. 2006 The exclusion criteria were as follows: having a history of speech-language-hearing and/or orthodontic treatment; missing more than three teeth; presenting with signs suggestive of pathological bruxism; having craniofacial syndromes or malformations; and having a neuromuscular impairment. Sex and age homogeneity between the groups was tested with the chi-squared test; no statistical differences between them were found (respectively, p = 0.05 and p = 0.17). They were divided into three age ranges to group children with structural similarities.

After obtaining this sample, the sample calculation was made, based on Callegari-Jacques,2929 Callegari-Jacques SM. Bioestatística: princípios e aplicações. Art Med 2007 considering the highest standard deviation found (36.18), 5% significance level, and 15-Hz sample error. The resulting minimum sample size was 23 subjects in each group, which had already been obtained.

The age range of the study participants was defined considering that it is potentially difficult to submit children < 6 years old to EMG assessment and that the first molars erupt at 6 or 7 years old. The BMI of the children was also delimited between 5 and 85 percent, considering that larger fat layers under the skin may interfere with the EMG signal pickup.1818 De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163,2828 Organização Mundial da Saúde. 2006,3030 Conde WL, Monteiro CA. Body mass index cutoff points for evaluation of nutritional status in Brazilian children and adolescents. J Pediatr (Rio J) 2006;82(04):266–272

Mouth breathing was diagnosed with the agreement between the speech-language-hearing and otorhinolaryngologic assessments; if they did not agree, the subject was excluded. The speech-language-hearing assessment was based on the MBGR Protocol,3131 Marchesan IQ, Berretin-Félix G, Genaro KF. MBGR protocol of orofacial myofunctional evaluation with scores. Int J Orofacial Myology 2012;38:38–77 with information on breathing, occlusion, other treatments, and signs suggestive of craniofacial syndromes or neuromuscular impairment. The otorhinolaryngologic assessment investigated breathing changes and, as performed by Berwig et al.3232 Berwig LC, da Silva AMT, Côrrea ECR, de Moraes AB. Quantitative analysis of the hard palate in different facial typologies in nasal and mouth breathers. Rev CEFAC 2012;14:616–625 and Ritzel et al.,3333 Ritzel RA, Berwig LC, da Silva AM, Corrêa ECR, Serpa EO. Correlation between nasopharyngoscopy and cephalometry in the diagnosis of hyperplasia of the pharyngeal tonsils. Int Arch Otorhinolaryngol 2012;16(02):209–216 encompassed oroscopy, anterior rhinoscopy, and otoscopy, followed by fiberoptic nasopharyngoscopy, when necessary. When cephalometry was enough to determine the degree of pharyngeal tonsil hypertrophy, the fiberoptic nasopharyngoscopy was not performed. After this assessment, the children were divided into NB (nasal breathing mode, without signs and symptoms of daytime and/or nighttime mouth breathing) and MB (oronasal or mouth breathing mode, with at least three signs and symptoms of daytime and/or nighttime mouth breathing, such as open mouth/open lips, dry lips, infraorbital dark circles, sagging/ drooping face, among others). Of the 34 MB children, 15 were diagnosed from symptoms related to mouth breathing and 17 underwent cephalometry or fiberoptic nasopharyngoscopy, being classified as grades I, II or III of obstruction.

The children were also grouped according to their facial growth patterns. This diagnosis was based on Ricketts cephalometry analysis, performed with lateral teleradiography, using 18 x 24 cm Kodak film and a cephalostat to standardize the head position in ray emission, at a distance of 1.5 meters. The VERT index3434 Ricketts RM, Roth RH, Chaconas SJ, Schulhof RJ, Engel GA. Orthodontic Diagnosis and Planning their Roles in Preventive and Rehabilitative Dentistry. 1. ed. Denver: Rocky Mountain; 1982: 269 p. was calculated, determining the following facial types: brachyfacial (index value > +0.5), mesofacial (index value between - 0.5 and + 0.5), and dolichofacial (index value < - 0.5).

Hence, the groups were initially formed with NB and MB children; they were afterward subdivided into brachyfacial (Br), mesofacial (Me), and dolichofacial (Do), totaling six groups.

All the children and their parents/guardians agreed to their participation in the study and signed the informed consent form - which had been previously approved by the Research Ethics Committee of the institution under approval protocol number 08105512.0.0000.5346.

Electromyography

The EMG signals were picked up with equipment available in the market- Miotool (Miotec- Brazil), with 8 input channels, 14-bit A/D converter - and saved in a portable computer not plugged into the electrical outlet. Active sensors with differential input (manufactured by Miotec) were connected to Ag/AgCl double electrodes (Hal Indústria e Comércio ltda.), placed on the belly of the right (RM) and left masseter muscles (LM) and of the right anterior (RT) and left anterior temporal muscles (LT). To better locate the muscle bellies, a function test was conducted with the isometric contraction of the mandibular elevator muscles. These disc-shaped electrodes have a fixed 20-mm distance from each other, 20x gain, 10 GΩ input impedance, and common-mode rejection rate > 100dB.3535 Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 2000;10(05):361–374 To decrease skin impedance,1919 Cram JR, Kasman GS, Holtz J. Introduction to Surface Electromyography. Maryland: Aspen Publishers; 1998 the sites where the electrodes would be positioned were cleaned with 70% ethyl alcohol and cotton; if necessary, the hair in the region was removed.

The collection room was also treated, having its floor covered with paviflex rubber flooring.1818 De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163 As a precaution, equipment that might interfere electromagnetically with the examination was put aside and turned off. The reference electrode (connected to the ground wire) was positioned on the glabela of the patient. The signal was picked up with 20-to 500-Hz filter and a maximum acquisition capacity of 2,000 samples/second/channel. This assessment was performed always by the same researcher to avoid deviations and differences in the collection procedure.

Fatigue Assessment Protocol

The children sat comfortably, hip, knees, and ankles flexed 90°, following the Frankfurt plane. They were instructed on the examination procedures, collection room setting, and equipment and were trained on the procedures before the collection.1212 Busanello-Stella AR, Blanco-Dutra AP, Corrêa ECR, Silva AMT. Electromyographic fatigue of orbicular oris muscles during exercises in mouth and nasal breathing children. CoDAS 2015;27(01): 80–88 Isotonicity (mastication) was used to test muscle fatigue, as this function is often trained in clinical practice to strengthen the masticatory muscles.2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167,2424 Pinheiro DLDSA, Alves GÂDS, Fausto FMM, et al. Effects of electrostimulation associated with masticatory training in individuals with down syndrome. CoDAS 2018;30(03):e20170074,2525 Prado DGA, Berretin-Felix G, Migliorucci RR, et al. Effects of orofacial myofunctional therapy on masticatory function in individuals submitted to orthognathic surgery: a randomized trial. J Appl Oral Sci 2018;26:e20170164,3636 Mendonça RG, Oliveira AS, Pedroni CR, Bérzin F. Electromyography assessment of chewing induced fatigue in temporomandibular disorders patients – a pilot study. Braz J Oral Sci 2005;4(15): 894–898,3737 Caria PH, Bigaton DR, de Oliveira AS, Bérzin F. Fatigue analysis in the masseters and temporalis muscles in patients with temporomandibular disorder during short period of mastication. Acta Odontol Latinoam 2009;22(02):87–91

The mastication test was performed three times in sequence, with 2-minute intervals in between them.1818 De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163 A digital 80-bpm metronome was used (Mendonça et al, 2005), as well as chewing gum (Plic Ploc - Brazil) because it best resembles food without deteriorating or producing residues that might interfere with the assessment. Two portions of chewing gum were placed on the molars, one on the right and one on the left side of the arch. Initially, the children were asked to chew the gum freely for 40 seconds, without removing it from the sides, to diminish and standardize its resistance. After some rest, they should chew rhythmically until they felt fatigued - that is, the first sign of discomfort in this musculature.2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167,3636 Mendonça RG, Oliveira AS, Pedroni CR, Bérzin F. Electromyography assessment of chewing induced fatigue in temporomandibular disorders patients – a pilot study. Braz J Oral Sci 2005;4(15): 894–898

Electromyography Signal Analysis

This analysis was performed with the Miograph 2.0 software, for 60 seconds of activity divided into four 15-second intervals (T1, T2, T3, and T4), encompassing ~ 18 mastication cycles. In these intervals, the signal MF was analyzed, considering the moments of activation and inactivation of the cycle together. Of the three mastication collections, the one with the best signal quality was selected (analyzed with the fast Fourier transform [FFT]). Then, the initial 0.5 seconds were excluded to make the assessment period homogeneous. The time reported by the children when they began to feel muscle fatigue was analyzed by recording the moment when it occurred and then comparing them later. The researcher was unaware of the group identification for record analysis.

Statistical Analysis

After testing the normality of the variables with the Shapiro-Wilk test, the repeated measure analysis of variance (ANOVA) was conducted, with the Tukey post hoc test. For the reported fatigue time, without normal distribution, the Mann-Whitney U test and Kruskal-Wallis test were applied, according to the category of each group. The analyses were made in Statistica 9.0 software, with the significance level set at 5% (p < 0.05).

Results

Electromyography Signal

The evolution of the MF of the masticatory muscles throughout the mastication, regardless of the groups, is shown in ►Table 1. A statistical significance was found for RT (p < 0.01), LM (p = 0.018), and LT (p = 0.02). The post hoc analysis showed that this occurred mainly between 15 and 60seconds of activity. However, there was no defined MF decrease pattern.

Table 1
Distribution of means and standard deviations of the median frequency and statistical analysis found in the tests of the masticatory muscles, regardless of the groups, throughout the different collection moments (T1, T2, T3, and T4)

The MF of the masticatory muscles in interaction with the breathing mode (►Table 2) revealed no MF continuous decrease. Only the LM and MB had statistical significance (p < 0.05), although it referred to an MF increase, instead of a decrease.

Table 2
Distribution of means and standard deviations of the median frequency found for the masticatory muscles during mastication and statistical analysis of the interaction with the breathing mode, throughout the different collection moments (T1, T2, T3, and T4)

Considering the interaction with the facial growth pattern (►Table 3) and with its association with the breathing mode (►Table 4), there was likewise no decreasing MF pattern or statistical significance.

Table 3
Distribution of means and standard deviation of the median frequency found for the masticatory muscles during mastication and statistical analysis of the interaction with the facial growth pattern, throughout the different collection moments (T1, T2, T3, and T4)
Table 4
Distribution of means and standard deviations of the median frequency found for the masticatory muscles during mastication and statistical analysis of the interaction with the breathing mode in association with the facial growth pattern, throughout the different collection moments (T1, T2, T3, and T4)

Perception of Fatigue

The analysis of the reported time of fatigue of the masticatory muscles, in the three group interactions, is shown in ►Table 5. There was no significant difference in either of the cases regarding the time when these groups perceived muscle fatigue. In the breathing mode, the MB perceived the fatigue sooner (mean of 95seconds). In the facial growth pattern, dolichofacial and mesofacial children perceived it sooner (mean of 93seconds). And in the association of the groups, the MB children with mesofacial patterns were the firstonesto perceiveit (78seconds). In all cases, the standard deviations (SDs) were high.

Table 5
Distribution of means and standard deviations of the reported fatigue time (in seconds) found for the masticatory muscles during mastication and statistical analysis of the interaction with the groups

Discussion

The analysis of the masticatory muscles, regardless of the interaction with the groups, showed that RT, LM, and LT had a significant change in MF, particularly between 15 and 60seconds of mastication. However, it was not a decreasing change and therefore was not suggestive of muscle fatigue. These findings corroborate two aspects reported in the literature: the fiber arrangement of this musculature and the dynamic test condition. In the masticatory muscles, more specifically the masseter, there is a predominance of type I3838 Stål P, Eriksson PO, Thornell LE. Differences in capillary supply between human oro-facial, masticatory and limb muscles. J Muscle Res Cell Motil 1996;17(02):183–197 and hybrid fibers,3939 Sciote JJ, Horton MJ, Rowlerson AM, Link J. Specialized cranial muscles: how different are they from limb and abdominal muscles? Cells Tissues Organs 2003;174(1-2):73–86 which are both more resistant to muscle fatigue because they have an aerobic pattern of energy production.

Regarding the use of chewing gum in the mastication test, the literature reports that the EMG activity of the masseter and temporal muscles is associated with the mechanical properties of the selected foods. In this case, chewing gum enables stable mandible movements and EMG activity, which are considered adequate to analyze the masticatory pattern. Moreover, as the muscle blood flow is not interrupted, isotonicity would not easily cause fatigue.2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167,2323 Tomonari H, Seong C, Kwon S, Miyawaki S. Electromyographic activity of superficial masseter and anterior temporal muscles during unilateral mastication of artificial test foods with different textures in healthy subjects. Clin Oral Investig 2019;23(09): 3445–3455,3737 Caria PH, Bigaton DR, de Oliveira AS, Bérzin F. Fatigue analysis in the masseters and temporalis muscles in patients with temporomandibular disorder during short period of mastication. Acta Odontol Latinoam 2009;22(02):87–91

The interaction of the masticatory muscles with the breathing mode revealed that only the LM had a difference in MF throughout the mastication in the MB group. However, since it referred to its increase, rather than decrease, it was likewise not suggestive of muscle fatigue.1818 De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135–163 Studies with EMG have shown that MBs tends to have less masseter and temporal muscle activity than NBs.1515 Nagaiwa M, Gunjigake K, Yamaguchi K. The effect of mouth breathing on chewing efficiency. Angle Orthod 2016;86(02): 227–234,4040 Ferla A, Silva AMT, Corrêa ECR. Electrical activity of the anterior temporal and masseter muscles in mouth and nasal breathing children. Rev Bras Otorrinolaringol (Engl Ed) 2008;74(04): 588–595 In another study, children without changes had a diminished masseter and temporal muscle behavior, which may be associated with immature motor coordination, resulting in incapacity to maintain high force levels.2121 Oliveira LF, Palinkas M, Vasconcelos PB, et al. Influence of age on the electromyographic fatigue threshold of the masseter and temporal muscles of healthy individuals. Arch Oral Biol 2017; 84:1–5

The diminished muscle behavior in MB may be caused by the hypofunctioning of the masticatory muscles of these subjects, especially the mandibular elevators, as the mouth remains open for breathing.55 Silva CR, Geres BS, Kuriki HU, Negrão Filho RF, Alves N, Azevedo FM. Analysis of reliability of EMG signal frequency domain parameters used in the characterization of localized muscle fatigue. Motriz Rev. Educ. Fís. 2012;18:456–464,88 de Mattos FMGF. Orofacial myofunctional characteristics of oral and oronasal breathers. Rev CEFAC 2018;20:459–467 The masticatory preference pattern and changed head posture of MBs can also interfere with the asymmetry of the musculature, though with no defined pattern.1616 Boton LM, Silva AMT, Bolzan GP, Corrêa ECR, Busanello AR. Electromyographic study on facial muscles of nasal breathers, obstructive and vicious oral breathers. Rev CEFAC 2011;13:27–34,4040 Ferla A, Silva AMT, Corrêa ECR. Electrical activity of the anterior temporal and masseter muscles in mouth and nasal breathing children. Rev Bras Otorrinolaringol (Engl Ed) 2008;74(04): 588–595 Thus, it was hypothesized that the possible asymmetry in the masticatory muscles of this population can also interfere with muscle fatigue – which, however, was not observed.

The perception time of masticatory muscle fatigue reported by the sample children was not statistically different between NBs and MBs, with an approximate mean of 102 and 95seconds, respectively, and a SD of 63 and 65, respectively. Other authors2222 Buzinelli RV, Bérzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil 2001;28(12):1165–1167 researched reports of the masseter and temporal fatigue feeling and likewise observed large SDs of the means, suggesting great subjectivity in this variable.

Each facial pattern determines specific characteristics regarding the soft and hard structures, which influence the development of the stomatognathic functions.3232 Berwig LC, da Silva AMT, Côrrea ECR, de Moraes AB. Quantitative analysis of the hard palate in different facial typologies in nasal and mouth breathers. Rev CEFAC 2012;14:616–625,4141 Ramires RR, Ferreira LP, Marchesan IQ, Cattoni DM, Silva, Marta AA. Facial types applied to Speech-Language Pathology: literature review. Rev Soc Bras Fonoaudiol 2010;15:140–145 As for the clinical aspects, people with a brachyfacial pattern have thicker and more powerful mandibular elevator muscles. The opposite occurs with the dolichofacial pattern, in whom these muscles are feebler and less strong.3232 Berwig LC, da Silva AMT, Côrrea ECR, de Moraes AB. Quantitative analysis of the hard palate in different facial typologies in nasal and mouth breathers. Rev CEFAC 2012;14:616–625

Concerning the myoelectrical manifestations in the facial types, the literature only researched EMG approaching the amplitude and, even so, with disagreements. Some authors did not find differences in the masticatory muscles between the various facial patterns during mastication,4242 Trawitzki LVV, Felício CM, Puppin-Rontani RM, Matsumoto MAN, Vitti M. Mastication and electromyographic activity in children with posterior crossbite. Rev CEFAC 2009;11:334–340 whereas others observed that the masseter muscles of the dolichofacial patternwere more active in this function.4343 de Miranda ALR, Marilena MannoVieira, Silvana Bommarito, Brasília MariaChiari. Avaliação da atividade eletromiográfica do músculo masseter em diferentes tipos facial. Rev Odontol 2009; 17:17–25 Since there is a muscle imbalance, especially in the brachyfacial and dolichofacial patterns,66 Chambi-Rocha A, Cabrera-Domínguez ME, Domínguez-Reyes A. Breathing mode influence on craniofacial development and head posture. J Pediatr (Rio J) 2018;94(02):123–130,3232 Berwig LC, da Silva AMT, Côrrea ECR, de Moraes AB. Quantitative analysis of the hard palate in different facial typologies in nasal and mouth breathers. Rev CEFAC 2012;14:616–625,4242 Trawitzki LVV, Felício CM, Puppin-Rontani RM, Matsumoto MAN, Vitti M. Mastication and electromyographic activity in children with posterior crossbite. Rev CEFAC 2009;11:334–340 it was hypothesized that the masticatory muscles could also have fatigue differences – which, however, was not proved.

There was no difference in the reported time of masticatory muscle fatigue of the children between the facial growth patterns. Another study4444 Farella M, Bakke M, Michelotti A, Rapuano A, Martina R. Masseter thickness, endurance and exercise-induced pain in subjects with different vertical craniofacial morphology. Eur J Oral Sci 2003;111 (03):183–188 investigated reports of pain and fatigue in the masseter muscle of people with different types of craniofacial morphology and observed that people with normal and elongated facial patterns have greater resistance and take longer to start feeling pain. The authors pointed out, as a plausible explanation for the observed differences, the theory of mechanical advantage, in which subjects with an elongated face have a smaller mechanical advantage in the mandibular elevator muscles. Hence, those with a short face have more occlusal force and consequently greater intramuscular pressure. This may limit the muscle blood flow, which is necessary to maintain force. This disagreement may be explained by the difference between samples, as the one in the present study encompassed children, whereas the one in the literature encompassed adults. Furthermore, the subjectivity of this variable may indicate greater perception difficulty in children.

The breathing mode was also considered along with the facial growth pattern because it was believed that changes in these two aspects may potentialize each other. Nevertheless, although the sample distribution into these new groups showed their stomatognathic characteristics in further detail, it did not occur in myoelectric terms for the masticatory muscles. The analysis of the MF and the fatigue perception time for this musculature throughout the collection time revealed no difference.

Thus, it seems clear to say that the masticatory muscles are rather resistant to fatigue, especially in dynamic situations, which elongate the muscle belly and consequently increase the blood flow. This increases the muscle temperature and metabolism, further removing the substrates that cause fatigue.4545 Basmajian JV, De Luca CJ. Muscles Alive: Their Functions Revealed by Electromyography. 5th ed. Baltimore: Williams e Wilkins; 1985 However, future studies should address other aspects neither investigated nor controlled in the present study – such as the amplitude of the EMG signal –, aiming at a more precise interpretation of these findings.

It is important to highlight that the present study has some limitations, such as the small sample size when the six groups were analyzed separately and the muscle fatigue analysis based exclusively on the EMG signal frequency, without its amplitude – which is already being addressed in other studies of this research group.

Conclusion

The EMG analysis of the masticatory muscles during mastication showed that they were not suggestive of fatigue. However, the fatigue time was reported despite the absence of physiological fatigue. The breathing mode, the facial growth pattern, and the association between them seemed not to influence the behavior of the MF of the EMG signal and the fatigue time perception.

  • The present work was conducted at the Laboratório de Motricidade Orofacial of the Phonoaudiology Department of the Universidade Federal de Santa Maria.
  • Funding
    Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

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Publication Dates

  • Publication in this collection
    04 Dec 2023
  • Date of issue
    June 2023

History

  • Received
    28 Feb 2022
  • Accepted
    19 Aug 2022
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