Eletromiografia de superfície em musculatura orofacial e cervical de crianças respiradoras orais: revisão integrativa da literatura Surface electromyography in orofacial and cervical musculature in mouth breathing children: an integrative literature review

Purpose: to review, in an integrative manner, studies using surface electromyography in the orofacial and cervical musculature in mouth breathing children aged from three to 11 years and 11 months old. Methods: the survey was conducted in national and international databases, from 1998 to 2018, in Portuguese, English and Spanish. Review articles, dissertations, book chapters, case studies and edito rials were excluded. Results: 86 articles were found, 14 of which met the inclusion criteria. Most of these studies used sur face electromyography to assess and describe the muscle condition of the mouth breathing population. Only one study addressed the influence of myofunctional speech therapy and two studies included phy sical therapy treatment, using electromyographic evaluation before and after the intervention. Given the main categories of analysis, the discussion was based on the year, state of publication and journal, sam ple size, scientific methodology, muscles assessed, assessment protocols used and the results of the publications. Conclusions: surface electromyography has been used mainly in the initial assessment of orofacial and postural myofunctional changes caused by mouth breathing and not as a therapeutic biofeedback, thus, it is important to conduct longitudinal studies using this instrument in mouth breathers.


INTRODUCTION
Nasal breathing plays an important role in the quality of life of humans, as it promotes the filtration, heating and humidification of inspired air in order to reach the lungs in an optimum temperature 1 .This type of breathing also favors the craniofacial growth as well as the development of the individual and the proper functioning of stomatognathic functions 2 .
The literature indicates that any factor that leads to an upper airway (UA) obstruction, such as septum deviation, pharyngeal or palatine tonsil hypertrophy (adenoids and/or tonsils) 3 , or even due to sagging on speech organs and simple parafunctional habits, causes nasal breathing to be replaced by mouth breathing 4 .
Mouth breathing has been studied since the 20 th century with publications focused on Dentistry due to the occlusal consequences 5 .However, as a public health problem, it has generated greater scientific interest in recent years in other health areas due to the multidisciplinary aspects involved 6 .Areas such as otorhinolaryngology, dentistry and speech-language pathology associate mouth breathing with nasal, dental and orofacial motricity aspects 7 .Most studies address mouth breathing in childhood 6 , since the child's craniofacial growth and development occur at this stage and inadequate breathing, depending on its duration, may cause structural, functional, postural and behavioral changes that impact negatively on the individual's quality of life 8 .
As for the aspects of orofacial motricity, the main characteristics of the mouth breather are the lack of lip sealing, arched or high palate, Angle's Class II occlusion, unilateral or bilateral crossbite, open bite, sleep apnea, everted lower lip, retracted upper lip, generalized facial hypotonia, changes in stomatognathic functions, postural changes 9,10 , among others.These postural changes include shoulders rotated forward, head projected forward from the body, forward displacement of the hip, and body weight resting on the belly 11 .
The literature also describes the main signs and symptoms in mouth breathers, such as sleeping with an open mouth, snoring, scratching the nose, difficulty breathing at night or restless sleep, irritability, as well as daytime sleepiness, frequent tiredness, learning issues, learning deficit and behavioral problems 12 .Due to the wide changes found in mouth breathing children, it is important to emphasize the relevance of a multidisciplinary team, composed by otorhinolaryngologist, orthodontist, speech-language pathologist and physiotherapist 13 .
In order to assist in the early assessment and diagnosis of children with respiratory disorders, advances and scientific studies have enabled additional clinical evaluation through instrumental tests, such as the surface electromyography (sEMG) 14 .
The sEMG has been studied for some years in speech-language pathology research as an opportunity to analyze the muscle electrical activity in a quantitative manner, and may help in understanding the patterns of electrical activity of facial and masticatory muscles, leading professionals to an early diagnosis and a more effective intervention in Oral Motricity 15 .
Thus, this article aimed to review, in an integrative manner, studies using surface electromyography in mouth breathing children aged from three to 11 years and 11 months old, in order to understand the purpose of using this instrument and its contribution to the therapeutic intervention and evaluation.

METHODS
An integrative review study was conducted in order to analyze the available scientific evidence, both in the speech-language pathology literature as in other health areas, on the use of sEMG in mouth breathing children upon the following questions: "What is the purpose of using surface electromyography in orofacial and cervical muscles in mouth breathing children?"."What surface electromyography can provide to the assessment and intervention of these children?".The researchers conducted a survey of studies in Portuguese, English and Spanish published in the US National Library of Medicine National Institutes Health (PubMed), Scientific Electronic Library Online (SciELO), Medical Literature Analysis and Retrieval System Online (MEDLINE) and Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS) databases from 1998 to 2018.The descriptors found in the DeCS and MeSH that were used to find the studies in the three languages were: Electromyography OR Electromiografia OR Eletromiografia; Mouth Breathing OR Respiración por la Boca OR Respiração Bucal AND Child, Preschool OR Preescolar OR Pré-Escolar OR Child OR Niño OR Criança.The search was conducted by the association of at least two of the descriptors.
Exclusion criteria were: studies not published in journals indexed in PubMed, SciELO, MEDLINE and LILACS databases; studies not published from electromyography in mouth breathing children; studies with a sample population with an age range different of three to 11 years and 11 months of age; literature review, dissertations, book chapters, case studies and editorials, as well as those that did not have the subject addressed in this review in its title, abstract or text.The study included original research articles published in journals of speech-language pathology and other health areas, such as physical therapy and dentistry.
The selection stages of the articles were: first, a reading of the title of the studies found and the exclusion of those that did not fit the purpose of this study; then, a reading of its abstracts including the use of surface electromyography in the mouth breathing children population and the exclusion of those that did not fit the inclusion criteria.
The search and selection of articles were conducted as follows: 1) initial search for references in databases; 2) selection of references based on inclusion criteria by reading title and abstract; 3) duplicate deletion; 4) exclusion of studies according to the exclusion criteria, by reading the abstract and the methodology.All stages of the study were performed by the researcher student and the professor adviser.
Figure 1 shows the search and selection process of studies until the final design of the database for the analysis process.

LITERATURE REVIEW
Eighty-six references were found from the search descriptors.Out of these, 26 were found in PubMed, 8 in SciELO, 17 in LILACS and 35 in MEDLINE.35 studies were excluded in the third stage due to duplicate databases and 37 studies were excluded when applying the exclusion criteria, resulting in the 14 articles remaining in this study.Although the descriptors were used in the three languages (Portuguese, English and Spanish) in the databases, the final result included only articles published in Brazil.As shown in Figure 2, the studies were initially described by their main characteristics and then characterized in three items, for descriptive statistics of the frequency of each characteristic: scientific production (year of publication, journal of publication and the state in which the study was conducted); population (number of sample subjects, gender and age group) and assessed muscles, according to Tables 1, 2 and 3, respectively.
The year of publication ranged from 1998 to 2015, that is, it can be noticed that the articles found were published in the last 17 years, and no study of the current year met the inclusion criteria.It can also be noted that most studies were published annually from 1998 to 2011.It may be related to the emergence of new devices that makes it easier to perform electromyography and to the training of professionals for the electromyographic technique after the creation of the standardized protocol suggested by the Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles (SENIAN) during the International Society of Electrophysiology and Kinesioly (ISEK), in 2002 16 .Subsequently, the next study is from 2015, which is also the last publication found in the survey.
There was a higher number of publications in the Rio Grande do Sul state with 8 (57.1%) studies published from 2002 to 2015, which is believed to be due to the study group led by the speech-language pathologist Ana Maria Toniolo da Silva with a team of students and colleagues at the Universidade Federal de Santa Maria, RS, Brazil, following a line of research associated with orofacial motricity, mouth breathers and electromyography.Morphofunctional evaluation of the upper medial region of the orbicularis oris muscle, investigating the associations with mouth breathing.Use of lateral cephalometric radiographs and functional evaluation with electromyographic analysis.

Upper medial region of the orbicularis oris muscle
There was no statistically significant difference between the two groups regarding the shape of the upper lip, as well as to the function.

Bilateral anterior temporal and bilateral masseter muscles
The observed level of electrical activity in the mouth breathing group was lower in all analyzed muscles; however, a statistical significance was found only in the left temporal muscle.

Deglutição de respiradores orais e nasais: avaliação clínica fonoaudiológica e eletromiográfica
To assess and compare the swallowing of mouth and nasal breathing subjects, through clinical and electromyographic assessment of the upper and lower orbicularis oris muscles.
The speech-language pathology assessment included the structures and functions of the stomatognathic system, while the electromyographic assessment consisted in capturing the electrical activity of the upper and lower orbicularis oris muscles during isometry and swallowing.

Not reported
Upper and lower orbicularis oris muscles Swallowing changes were observed in the mouth breathers in the clinical evaluation.
On the other hand, electromyographic evaluation showed higher muscle activity in mouth breathers when compared to nasal breathers.

Orbicularis oris, masseter and temporal muscles, bilaterally
There was no significant difference in the muscles studied when comparing the three groups, except for the right masseter muscle at rest, when comparing nasal breathers (NB) and vicious mouth breathers (VMB).

Fadiga eletromiográfica dos músculos orbiculares da boca durante exercícios em crianças orais e nasais
To study the orbicularis oris muscles fatigue through the median frequency analysis of the electromyographic signal and the reported time of fatigue, according to the respiratory pattern and the facial growth pattern.The sample ranged from 13 to 88 individuals, including children of both genders from 4-12 years old, and the largest age group studied was from 6-12 years old.Even in studies with smaller samples 14,[21][22][23] , the authors reported an electromyographic evidence of both for the improvement of the muscles evaluated after speech-language pathology therapy 23 and physical therapy 21,22 , as for the electrical activity of the upper orbicularis muscle in mouth breathers 14 .No article indicates that a restricted number of subjects may have been a factor that influenced the results.
As for the methodology of the studies, it was found that most studies divided the sample into two groups (mouth and nasal breathers) 14,15,17,19,[21][22][23][24][25][26] with subgroups 18,27,28 to compare the electromyographic findings of the muscles studied in the two populations.As for publication journals, there is a wide variety of journals.Among the 14 studies, one that stands out was found in the "Journal of Electromyography and Kinesiology" 17 , which is the main source of outstanding original articles on the study of muscle contraction and human movement, focused on publishing the best studies in all areas related to electromyography and kinesiology.Two studies were published in the Revista CEFAC, which addresses only articles from the Speech-Language Pathology-related areas 14,18 .Two other studies in the area of Dentistry and Orthodontics were published in the Revista Dental Press de Ortodontia e OrtopediaFacial 19,20 and, finally, two studies in the area of Otorhinolaryngology were published in the Revista de Otorrinolaringologia Pediátrica 21,22 .
A single study addressed the impact of myofunctional therapy by performing an electromyographic assessment before and after a speech-language pathology therapy 23 , and two other studies assessed muscle electrical activity after months of physical therapy sessions 21,22 , while the other studies used the electromyography to complement the initial clinical assessment, detect the muscle activity pattern 14,15,17,18,2 0,24,25,27,28 and to assist in the diagnosis 26 .The literature in the speech-language pathology area understands the sEMG as a reliable tool for a reliable assessment, diagnosis and treatment related to speech-language pathology 24,26 .
Only three of the 14 studies include the etiology of mouth breathing undergoing nasopharyngoscopy and oroscopy to confirm the diagnosis of upper airway obstruction 21,22 and there are reports that few studies classified mouth breathers according to the etiology as obstructive and vicious, making it difficult to discuss its results 18 .In this study, the authors show the importance of knowing the etiology of mouth breathing in order to assist in therapeutic management, as they believe that children with mouth breathing caused by nasal obstruction are more likely to develop more severe muscle changes than children with vicious mouth breathing 18 .
The literature reports that children who have chronic mouth breathing may show significant changes in the craniofacial development, with changes in both bone and muscle tissues, that is, several structural changes of the speech organs, such as: hypotonia of the jaw elevators (masseter muscles) , tongue hypotonia, changes in the tongue resting posture, as well as in the orbicularis oris (the short upper and everted lower lip) 29 and mentalis muscles, all of which impair the stomatognathic functions, such as speech, swallowing and chewing in addition to vocal changes [29][30][31][32][33] .As shown in Table 3, the assessment of the orbicularis oris muscles was included in 9 studies (64.2%) 15,17,20,21,[23][24][25]28,30 and this is due to the fact that the perioral muscles, including the orbicularis oris and mentalis muscles 17,21 , will act more actively in order to restore the lip sealing required to adequate breathing 34,35 , which arouses the interest of researchers to evaluate both subjectively and quantitatively with electromyographic results, correlating with swallowing 14 , chewing 15,18 and speech 24 functions.
There are studies that claim that the compensatory participation of perioral muscles in mouth breathers during the swallowing function, for example, is an adaptation of the stomatognathic system as the chewing muscles do not perform the muscle activity that is required for this function 36,37 .Therefore, two studies among the results of this integrative review evaluated not only the orbicularis oris muscles, but also the temporal and masseter muscles 15,18 in mouth breathers comparing them to the group of mouth breathers.It is believed that the interest of these scholars towards these masticatory muscles in this specific population is due to the fact that the discussions are restricted to chewing development in mouth breathers, and the evaluation is based only on clinical aspects, with the need for a quantitative aspect, through a device to assist in the assessment, diagnosis and a more effective intervention 13 .
Other studies decided to evaluate the sternocleidomastoid (SCM) and trapezius muscles in both relaxation and maximal voluntary contraction 25 and during oral and nasal inspiration 18 in order to understand the level of muscle activity since, as mentioned, mouth breathing children change the position of the head and neck 11 to reduce the narrowing of the airways 25 , and the SCM muscle is considered a tool for inspiratory movement.These authors found greater SCM muscle activity in mouth breathing children during nasal inspiration, attributing this increased activity to the effort to increase lung volumes 18 .Regarding this action of accessory muscles during nasal breathing in mouth breathers, some authors 17 concluded that the therapy aimed at this population should not be performed only for orofacial changes, as there are also changes in the cervical muscles.Thus, other studies 21,22 using sEMG on cervical muscles (sternocleidomastoid, subocciptal and upper trapezius) were also found to verify the effectiveness of physical therapy sessions after a period of treatment.However, there is a consensus that there are few publications involving these muscles, and the authors suggest the development of further studies to verify the level of cervical muscle activity after postural and respiratory care.
The following category of analysis refers to the evaluation protocols used for both the evaluation, especially of the stomatognathic system, as for the use of the surface electromyography.None of the 14 studies mentioned any of the various types of surface electromyography protocols created by the Professor Hilton Justino da Silva 38 and other authors of the book "Protocolos de Eletromiografia de Superfície em Fonoaudiologia", published by Pró Fono 38 This book has electromyographic assessment protocols in phonation, an electromyographic assessment protocol for cervical muscles, among others, that could and should be present in studies using surface electromyography as a complementary tool for evaluation, diagnosis and clinical intervention.Only one speechlanguage pathology study 30 reported the use of the MBGR protocol (Protocol of Orofacial Myofunctional evaluation with scores) 39 that addresses general aspects of the stomatognathic system, as well as breathing, chewing and swallowing functions, for the clinical evaluation of the study population.
Referring to the results analyzed in the studies included in this integrative review, it was found that there were data showing the increased electrical activity of the orbicularis oris muscles with and without lip contact in mouth breathers when compared to nasal breathers, with a statistically significant difference 19 in line with the findings of another study 29 .However, the electromyographic activity was lower 24 during the speech test (production of syllables with bilabial and labiodental phonemes) in the same muscles evaluated, and it is believed that this is due to the hypotonia of the speech organs.Two of the studies assessed only the upper orbicularis oris muscle and found that there was no statistically significant difference between the subgroups 27 evaluated, as well as for the shape of the upper lip in relation to function 20 .On the other hand, the literature shows an increase in the activity of the lower orbicularis oris muscle due to the joint action of the mentalis muscle, in order to compensate the hypofunctionality observed in mouth breathers 40 .This activation of the lower orbicularis oris muscle seen in the literature is in line with the results reported also in the study that composes this integrative review, in which when evaluating the vicious mouth breathing (VMB) and the obstructive mouth breathing (OBM) at rest, the authors found that the lower orbicularis oris muscle in OBMs were electrically more active than in nasal breathers 18 .
Finally, regarding the electromyographic findings of the temporal muscles evaluated, there was also an increased electrical activity of the left temporal muscle in OMBs during masticatory isometry 18 , similar result was found in another study 14 that evaluated the maximum intercuspidal position and during habitual chewing 1814 In this regard, the literature explains that due to the anterior head posture in mouth breathers, which occurs in order to facilitate the air flow through the oropharynx, the temporal muscles have increased electrical activity in an attempt to compensate the lower activity of the masseter muscles.In addition, the greater activity of the left temporal muscle in relation to the right one may be related to the chewing lateral preference pattern 18 .As for the SCM, subocciptal and trapezius muscles, the studies found a significant reduction in the electrical activity of the muscles evaluated during the relaxed position, aligned posture 21 and nasal breathing 22 of mouth breathers after physical therapy treatment

FINAL CONSIDERATIONS
Given all of the above, the study contributes to the area of Orofacial Motricity as well as other areas of health, such as physical therapy, since only a few studies have been published in the last 20 years including the use of surface electromyography to complement the clinical evaluation, assist in the diagnosis and, mainly, in the therapeutic intervention of mouth breathing children within the age group of the inclusion criteria.Specifically in the field of speechlanguage pathology, only one study focused on using sEMG in orofacial muscles, in order to demonstrate the therapeutic efficacy.Similarly, only two papers, among the physical therapy studies, included the use of sEMG in cervical muscles in the study population, after postural exercise sessions, suggesting that the main purpose of the instrument would be the initial assessment of myofunctional and postural changes caused by mouth breathing, and not as a therapeutic biofeedback.
Therefore, the researchers recommend the publication of further longitudinal studies including the use of sEMG, in order to understand the electrical activity of various muscle groups a given time after the surgical and/or therapeutic intervention, in mouth breathers, that may assist professionals in the therapeutic planning.

number of studies Figure 1. Organization chart of the literature search and selection process
N: Figure 2. Main findings in the literature on the use of surface electromyography in mouth breathing children

Table 1 .
Main findings in the literature on the use of surface electromyography in mouth breathing children Frequency of scientific production characteristics of surface electromyography in mouth breathers

Table 2 .
Frequency of sample population characteristics N: number of studies, %: percentage

Table 3 .
Frequency of muscles assessed M: muscles, N: number of studies, %: percentage