The impact of oronasal breathing on perioral musculature

ABSTRACT

Purpose:

to compare the behavior of perioral muscles in nasal, oral and oronasal respirators.

Methods:

a sample consisting of three distinct groups, equally subdivided into Nasal, Oral and Oronasal Respirators. The behavior of the orbicular muscle of the mouth (upper part) and mentual one was measured by surface electromyography at rest, swallowing and labial isometry.

Results:

in all situations investigated, the orbicular muscle of the mouth (upper part) and mental muscle showed no significant difference in relation to Root Means Square, that is, average electrical activity between Oral and Oronasal Respirators. The data showed a significant difference in In Nasal Respirators, as compared to the other groups.

Conclusion:

similarity was seen in the comparison of perioral muscles behavior between oral and oronasal respirators, however, a significant difference in relation to nasal respirators.

Keywords:
Electromyography; Respiration; Muscle

RESUMO

Objetivo:

comparar o comportamento dos músculos periorais em respiradores nasais, orais e oronasais.

Métodos:

amostra constituída por três grupos distintos, igualmente subdivididos em Respiradores Orais, Nasais e Oronasais. Com faixa etária entre 6 e 12 anos de ambos gêneros. O comportamento dos músculos orbicular da boca (parte superior) e mentual foi mensurado por meio da eletromiografia de superfície no repouso, deglutição e isometria labial.

Resultados:

em todas as situações investigadas o músculo orbicular da boca (parte superior) e músculo mentual não revelaram diferença significante em relação ao Root Means Square, ou seja, atividade elétrica média entre os Respiradores Orais e Oronasais. Já nos Respiradores Nasais os dados comprovaram diferença significante em relação aos demais grupos.

Conclusão:

na comparação do comportamento dos músculos periorais entre os respiradores orais e oronasais houve similaridade mas diferença muito significante em relação aos respiradores nasais.

Descritores:
Eletromiografia; Respiração; Músculo

Introduction

The breath, physiological, vital and innate function of the human being, protects the upper airway and allows the satisfactory development of the craniofacial complex if performed correctly^1-4. For proper nasal breathing, lip sealing is indispensable for generating a differentiation system of intra and extra-oral pressures in the so-called Oronasopharyngeal Space. This system, in turn, is responsible for the adequate maintenance of muscle tone⁵ that favors the correct development of the oral cavity, since there is a bone and dental response to muscle action^6,7.

When, however, nasal respiratory failure due to obstructive or non-obstructive causes occurs, compensatory mechanisms such as oral breathing can be triggered^8,9. In this case, a new pressure condition is generated and the musculature needs to be readapted⁵. In the literature, damages caused by oral breathing due to a new muscular condition are already consecrated¹⁰. As well as the new condition sequelae: open bite, retrognathism, high and narrow palate among others¹¹.

Although, in the oronasal respirator - also called vicious^12,13, mixed ¹⁴ or partial^8,15 - even after clearing the upper airways, the systematic nasal breathing does not occur. Either by habit or muscle memory the mouth remains ajar. In these cases, muscle activity has never been investigated. Perhaps because it is considered that intra and extra-oral pressure differentiation does not interfere with muscular behavior¹⁶. Or because it is associated with chronic diseases of difficult treatment and continuous control such as rhinitis^17,18. Thus, albeit the oronasal respirator is considered a distinct group¹⁹, it is often disregarded or grouped as an oral respirator.

If, however, the musculature in the oronasal respirator is compromised in the same way as in the oral respirator, some care must be guaranteed, once the incidence of chronic diseases^20,21 is high, such as rhinitis in children, from 26.6% to 53.3%²². Unfortunately, when untreated, they can cause similar morphological damage to the mouth respirator, besides compromising orthodontic interventions with relapses or treatment limitations due to inadequate muscular action²³.

In particular, two muscles have a significant participation with the oral cavity development, the orbicularis muscle of the mouth (upper part) and the mental muscle²⁴. When lip sealing does not occur the orbicularis muscle of the mouth (upper part) is shortened, a condition that favors dental protrusion and imbalance in facial morphology¹³. Studies have also shown that the muscles in these cases perform more effort in activities such as suction and swallowing^23,24. On the other hand, the mental muscle^23,25, which is responsible for positioning and directing the lower lip²³, is hypertrophied in the oral respirator due to its excessive recruitment when sealing the lips²⁶. With a volume increase, it tends to accentuate the eversion of the lower lip²³ and the buccal inclination of the incisive teeth²⁷, since its insertion lies in the alveolar eminence of the canine teeth to the lateral incisors ²⁵.

Due to the expressive participation of the orbicular muscles of the mouth and mentual muscles in skeletal and dental development, this study aims to compare the behavior of the perioral muscles in nasal, oral and oronasal respirators.

Methods

The study was approved by the Research Ethics Committee of UNICAMP under No. 1,125,115 according to Resolution 466/12 of the National Health Council (CNS). The legal representatives of the selected patients signed the Free and Informed Consent Form for the authorization of data collection.

Sample

It’s consisted of 48 patients, divided equally into three groups: Nasal Respirators (RN), Oral Respirators (ORO) and Oronasal Respirators (RON), aged between 6 and 12 years old, male and female, selected from the waiting list of a Basic Health Unit.

• Inclusion Criteria: Medical records of otorhinolaryngological evaluation of the upper airways.

NASAL RESPIRATOR: clearing of the upper airways with effortlessly sealed lips during rest, chewing and with the tongue contained in the oral cavity²⁸.

ORAL RESPIRATOR: obstruction of the upper airways, breathing with difficulty through the nose, showing signs of fatigue, dyspnea and needing to open the mouth to inspire when at rest and chewing²⁸.

ORONASAL RESPIRATOR: clearing of the upper airways, breathing through the mouth and nose, but being able to breathe through the nose without showing signs of fatigue or dyspnea²⁸.

• Exclusion Criteria: Neurological, cognitive impairment, peripheral and/or central facial paralysis, syndromes, lip and palate cleft, making use of myo relaxing medicine, facial trauma, submitted to myotherapic and/or orthodontic and/or facial orthopedic treatment.

Procedures

The evaluation consisted of the analysis of the medical records for the investigation of otorhinolaryngological opinion regarding the respiratory mode, protocol of Miofunctional Evaluation with Scores (AMIOFE)²⁸ and electromyographic examination. AMIOFE was also used to define the respiratory mode²⁸, being this protocol applied integrally once the observation of the patient throughout the evaluation is necessary to define different respiratory modes.

Figure 1 measures the different respiratory modes. However, in this study, mild oronasal breathing was considered Oronasal Respiration and severe oronasal breathing, Oral Respiration.

Figure 1:
AMIOFE Protocol. Specific cut-off of the "functions" criterion for respiratory mode

In order to define the different respiratory modes, the protocol considers the following characteristics:

• Nasal Respiration (normal nasal breathing): lips sealed effortlessly during rest and chewing with the tongue contained in the oral cavity.

• Oronasal breathing (mild oronasal breathing): breathing through the nose and mouth without showing signs of fatigue or dyspnea.

• Oral Respiration (severe oronasal breathing): breathing with difficulty, showing signs of fatigue, dyspnea and needing to open the mouth to breathe at rest and chewing.

Surface Electromyography

The study was carried according to the recommendations of the European Applications of Surface Electromyography (SENIAM)²⁹. Myosystem and Myosystem BRI software, version 2.52, 12-bit resolution signal conditioner with 112 dB Common Rejection Mode, 60 Hz and Myosystem Digital Analog Converter, model PCI-DAS 1200, were used.

Bipolar disposable electrodes of Chicopee MA01 (Meditrace, Kendall-LTP) with a diameter of 1cm were coupled to a preamplifier (model PA 1010-VA, 20-fold gain) to form a differential circuit. This circuit subtracts the common signal and amplifies the differential signal of interest to attenuate artifacts and avoid crosstalk^30,31. The monopolar stainless steel reference electrode was attached to the sternum of the patient. In the other muscles, the inter-electrode distance was 1cm, and in the mental muscle it was positioned in its womb to 2mm below the edge of the lower lip and in the orbicularis muscle of the mouth (upper part) in its midline¹³.

To capture the signal, the sampling frequency was 2 kHz. After collecting, the signals were submitted to a Butterworth filter, bandpass of 20-500 Hz, rectification with low-pass filter of 4 Hz and calculation of the average electrical activity of the signal through Root Means Square (RMS)^31,32.

The duration of the records was 5 seconds at rest, swallowing and labial isometry, with one-minute interval between the abstractions³³. For swallowing, 1ml of water was inserted into the patient's mouth with a syringe and after 60 seconds the swallowing was requested. Finally, for isometry the patient maintained an eccentric contraction of the lips for 5 seconds. The tests used were Chi-Square, Fisher, ANOVA and Box Plot, and the value considered significant was p <0.05.

Results

Sample Characterization

In the comparison between NG, GO and GON - regarding to the male and female gender - there was no significant difference between the groups, according to Table 1 below:

Table 1
Gender-specific sampling in different respiratory patterns

Gender	Groups			Total
	RN	RO	RON
Female (freq.)	5	6	4	15
%	31.25	37.50	25
Male (freq.)	11	10	12	33
%	68.75	62.50	75.00
TOTAL	16	16	16	48

• RN: Nasal Respirator, RO: Oral Respirator; RON: Oronasal Respirator p: 0.7476 (Chi-Square and Fisher, p <0.05), frequency: %, percentage.

Regarding age, the data also showed no significant difference between the groups, according to Table 2.

Table 2
Sampling in relation to age

Group	N	Mean	Median	SD	Minimum	Maximum
RN	16	7.94	7.5	2.05	6.0	12
RO	16	6.69	6.0	1.01	6.0	9
RON	16	7.00	6.0	1.37	6.0	10

• N: Sample, SD: Standard Deviation, RN: Nasal Respirator, RO: Oral Respirator, RON: Oronasal Respirator, p: 0.1550 (ANOVA test, p <0.05).

Table 3 below quantified the values of the electromyographic examination in the Group / Muscle ratio.

Table 3:
Quantitative description of Root Means Square (RMS), mean electric activity of the Groups / Muscle ratio in electromyography (ANOVA for repeated measures)

Group	Variable	N	Mean	Mediam	SD	Minimum	Maximum
RN	rephab (m.orbicular)	16	4.23	3.61	2.30	1.25	7.89
	rephab (m.mentual)	16	6.64	7.44	3.36	0.77	11.31
	degl (m.orbicular)	16	5.87	5.28	3.57	0.77	13.82
	degl (m.mentual)	16	10.88	9.87	9.32	1.74	39.15
	labial isometry (m.orbicular)	16	6.72	6.01	5.23	0.65	18.04
	labial isometry (m.mentual)	16	30.46	10.82	42.07	2.81	160.77
RO	rephab (m.orbicular)	16	10.33	8.10	7.10	4.09	31.39
	rephab (m.mentual)	16	22.32	16.37	21.49	5.45	92.53
	degl (m.orbicular)	16	28.37	19.45	28.92	6.42	103.68
	degl (m.mentual)	16	52.88	50.07	19.21	27.53	91.48
	labial isometry (m.orbicular)	16	69.14	55.02	63.48	6.79	220.53
	labial isometry (m.mentual)	16	101.27	70.45	60.16	30.90	205.78
RON	rephab (m.orbicular)	16	6.36	5.67	5.37	1.32	20.08
	rephab (m.mentual)	16	15.84	13.76	10.97	5.04	41.13
	degl (m.orbicular)	16	25.76	24.53	21.96	3.25	79.66
	degl (m.mentual)	16	40.77	43.65	17.87	6.23	71.01
	labial isometry (m.orbicular)	16	66.73	48.44	53.36	9.32	168.80
	labial isometry (m.mentual)	16	91.25	69.62	61.31	21.56	258.11

• N: sample, SD: Standard Deviation, RN: Nasal Respirator, RO: Oral Respirator, RON: Oronasal Respirator, m: muscle, degl: deglutition

In the electromyographic data between the groups there was similarity between ORO and RON, and a significant difference in relation to RN. Also a significant difference between both muscles. However, there was no correlation between the group and muscle factor.

Thus, in the separated analysis the mental muscle presented a difference between the groups; and the orbicularis muscle of the mouth (upper part) presented similarity between ORO and RON, and a significant difference in relation to RN. Finally, in the analysis separated by group only RN did not present significant difference between the muscles, according to Figure 2 below:

Figure 2:
Electromyographic data between the groups and analysis dismembered by muscle; with variables: RPH (rest in usual position), DEGL (swallowing) and ISOM. LAB (labial isometry)

The results showed that in the mental and orbicular muscles of the mouth there was a significant difference for the three studied groups with smaller measures for NG and similar for GO and GON. However, there was no significant difference in relation to the orbicular muscles of the mouth (upper part) and mentual muscles, but in GO and GON groups there was a significant difference with larger measures in the mental muscle, as shown in Figures 3, 4 and 5.

Figure 3:
Box Plot for the distribution of the average electrical activity of the electromyographic record in relation to RMS (Root Means Square) in the usual rest (repc) of the mentual muscle, orbicularis muscle of the mouth (upper part) of nasal, oronasal. ANOVA for repeated measurements. Significant difference * (Tukey's test). * RN ≠ RO / RON

Figure 4:
Box Plot for the distribution of the average electrical activity of the electromyographic record in relation to RMS (Root Means Square) in the swallowing of the mentual muscle, orbicularis muscle of the mouth (upper part) of the nasal, oral and oronasal respirators. ANOVA for repeated measurements. Significant difference * (Tukey's test). * RN ≠ RO / RON

Figure 5:
Box Plot for the distribution of the average electrical activity of the electromyographic record in relation to the RMS (Root Means Square) in the situation of lip isometry of the mentual muscle, orbicularis muscle of the mouth (upper part) of the nasal, oral and oronasal respirators. ANOVA for repeated measurements. Significant difference * (Tukey's test). * RN ≠ RO / RON

Discussion

The data revealed that the behavior of the perioral musculature in the oronasal respirator is similar and in some muscles even more intense than in the oral respirator. To characterize RON as a distinct group some care was taken. Besides the otorhinolaryngological evaluation, a specific protocol - Myofunctional Orofacial Evaluation with Scores²⁸ - was used to define qualitatively and quantitatively different breathing modes (Figure 1). The protocol determined to use only this age group of patients: between 6 and 12 years old. The average age obtained in the study was ± 7.21 years old, with no significant difference between RN, ORO and RON, p: 0.1550 (Table 2). Similarly with gender, among the groups RN, ORO, RON, p: 0.07476 (Table 1), whose data go against literature^1,2 which disregards the equal distribution of gender in the group and only stands out the classification to presence or absence of nasal obstruction.

However, in the behavior investigation between muscles and RN / ORO / RON groups, there was no correlation between both. The factors were then analyzed separately (Figure 2). The criterion Root Means Square (RMS) was used to measure the average electrical activity of the signal ¹⁹. The orbicularis muscle of the mouth (upper part) presented similarity between ORO and RON, and significant difference in relation to RN. In the mental muscle, a significant difference was found in all the situations investigated³⁴ (Figures 3, 4, 5).

In the usual rest, the literature considers absence of muscular activity values of up to 5μv³⁵. In this study, the orbicularis muscle of the mouth (upper part) presented an average RMS value of 3.61μv considered normal, and the mental muscle, 7.44μv, close to the normality pattern. In ORO and RON groups, RMS values were much higher in the orbicularis muscle of the mouth (upper part) and in the mentual³⁴ (Table 3). These results confirm that not only intra-oral pressure is different in the inefficient labial sealing, as well as the behavior of the perioral muscles⁵.

During swallowing and labial isometry there was also a pattern of similar behavior: GRN low values, GRO and GRON elevated (Figures 3, 4). As muscular dynamics influences skeletal and occlusal development, the obtained data in the GRO and GRON agree with studies associating ORO with cases such as retrognathism and open bite²⁷. The results are reaffirmed as the three situations - habitual rest, swallowing and lip isometry - presented a profile of similar behavior with progressive increase of RMS when performed in this sequence due to the need for greater recruitment so the activities could be performed²⁶ (Figures 3, 4, 5).

Another significant difference found was regarding the mental muscle. In the analysis between muscles in ORO and RON groups, in swallowing and isometry, their activity was high and significant (Figures 3, 4, 5)²³. Such findings are probably related to two aspects: anatomical location and function exerted by the muscle. In other words, the insertion in the inferior incisor muscle, which in turn has the function of the labial depression, in the case of ORO, requires the mental muscle to be more recruited to maintain the lip seal. About the function of positioning and directing the lower lip, there is also a need for greater effort because the lips are half open²³.

Conclusion

In the comparison of the behavior of the perioral muscles between oral and oronasal respirators, there was similarity but very significant difference in relation to nasal respirators.

Acknowledgements

The authors would like to thank Dr Claudia Maria de Felício - Faculdade de Medicina de Ribeirão Preto/ Universidade de São Paulo - Speech Pathology and Audiology undergrade course, for her technical support in the application of the AMIOFE protocol.

References

• ¹
  Hitos S, Arakaki R, Solé D, Weckx LLM. Oral breathing and speech disorders in children. J Pediatr. 2013;89(4):361-5.
• ²
  Berwig LC, Silva AMT, Côrrea ECR, Moraes AB, Montenegro M, Ritzel RA. Quantitative analysis of the hard palate in different facial typologies in nasal and mouth breathers. Rev. CEFAC. 2012;14(4):616-25.
• ³
  Rodrigues JA, Silva BNS, Baldrighi SEZM, Paranhos LR, César CPHAR. Interference of mouth breathing with orthodontic treatment duration in Angle Class II, Division 1. Rev. odontol. UNESP. 2017;46(3):184-8.
• ⁴
  Busanello SAR, Dutra APB, Corrêa ECR, Silva AMT. Electromyographic fatigue of orbicular oris muscles during exercises in mouth and nasal breathing children. CoDAS. 2015;27(1):80-8.
• ⁵
  Knösel M, Jung K, Kinzinger G, Buss O, Engelke W. A controlled evaluation of oral screen effects on intra-oral pressure curve characteristics. European Journal of Orthodontics. 2010;32(5):535-41.
• ⁶
  Malhotra S, Gupta V, Pandey RK, Singh SK, Nagar A. Dental consequences of mouth breathing in the pediatric age group. Int J Oral Health Sci. 2013;3(2):79-83.
• ⁷
  Bueno SB, Bittar TO, Vazquez FL, Meneghim MC, Pereira AC. Association of breastfeeding, pacifier use, breathing pattern and malocclusions in preschoolers. Dental Press J Orthod. 2013;18(1):30.e1-6.
• ⁸
  Oliveira RLB, Noronha WP, Bonjardim LR. Masticatory performance evaluation in patients with nasal and mouth breathing. Rev. CEFAC. 2012;14(1):114-21.
• ⁹
  Machado PG, Mezzomo CL, Badaró AFV. Body posture and the stomatognathic functions in mouth breathing children: a literature review. Rev. CEFAC. 2012;14(3):553-65.
• ¹⁰
  Marson A, Tessitore A, Sakano E, Nemr K. Effectiveness of speech and language therapy and brief intervention proposal in mouth breathers. Rev. CEFAC. 2012;14(6):1153-66.
• ¹¹
  Pacheco AB, Silva AMT, Mezzomo CL, Berwig LC, Neu AP. Relation between oral breathing and nonnutritive sucking habits and stomatognathic system alterations. Rev. CEFAC. 2012;14(2):281-9.
• ¹²
  Migliorucci RR, Passos DCBOF, Berretin-Felix G. Orofacial myofunctional therapy program for individuals undergoing orthognathic surgery. Rev. CEFAC. 2017;19(2):277-88.
• ¹³
  Rezende MS, Carvalho LC, Prado RAM, Rocha CBJ, Silva VR, Lunes DH. Isostretching method effects on lung function and posture of mouth breathers. ConScientiae Saúde. 2016;15(1):89-95.
• ¹⁴
  Brustolin JP, Dalpian DM, Zanatta FBB, Casagrande L. Associação entre história de aleitamento e relatos de hábitos orais e alergia em crianças. Rev. Fac. Odontol. Porto Alegre. 2012;53(2):11-4.
• ¹⁵
  Andrada e Silva MA, Marchesan IQ, Ferreira LP, Schmidt R, Ramires RR. Posture, lips and tongue tone and mobility of mouth breathing children. Rev. CEFAC. 2012;14(5):853-60.
• ¹⁶
  Engelke W, Jung K, Knösel M. Intra-oral compartment pressure: a biofunctional model and experimental measurements under different conditions of posture. Clin. Oral Investig. 2011;15(2):165-76.
• ¹⁷
  Lopes TSP, Moura LFAD, Lima MCMP. Association between breastfeeding and breathing pattern in children: a sectional study. J Pediatr. 2014;90(4):396-402.
• ¹⁸
  Popoaski C, Marcelino TF, Sakae TM, Schmitz LM, Correa LHL. Avaliação da qualidade de vida em pacientes respiradores orais. Arq Int Otorrinolaringol. 2012;16(1):74-81
• ¹⁹
  Nagae MH, Alves MC, Kinoshita RL, Bittencourt ZZLC, Gagliardo H. Life quality for mouth and oronasa lbreathing subjects. Rev. CEFAC. 2013;15(1):105-10.
• ²⁰
  Imbaud TCS, Mallozi MC. Frequência de rinite e alterações orofaciais em pacientes com má oclusão dentária. Rev Paul Pediatr. 2016;34(2):184-8.
• ²¹
  Brandão HV, Vieira GO, Vieira TO, Cruz AA, Guimarães AC, Camargos CTP et al. Acute viral bronchiolitis and risk of asthma in schoolchildren: analysis of a Brazilian newborn cohort. J. Pediatr. 2017;93(3):223-9.
• ²²
  Barros JR, Becker HM, Pinto JA. Evaluation of atopy among mouth-breathing pediatric patients referred for treatment to a tertiary care center. J. Pediatr. 2006;82(6):458-64.
• ²³
  Brodie AG. Muscular factors in the diagnosis and treatment of malocclusions. Angle Orthodontist. 1953;23(2):71-7.
• ²⁴
  Sinno MD , Zide BM. Chin ups and downs: Avoiding bad results in chin reoperation. Aesthetic Surgery Journal. 2017;37(3):257-63.
• ²⁵
  Hur MS, Kim HJ, Choi BY, Hu KS, Kim HJ, Lee KS. Morphology of the mentalis muscle and its relationship with the orbicularis oris and incisivus labii inferioris muscles. Journal of Craniofacial Surgery. 2013;24(2):602-4.
• ²⁶
  Schievano D, Rontani RMP, Berzin F. Influence of myofunctional therapy on the perioral muscles. Clinical electromyographic evaluations. J. Oral Rehabil. 1999;26(7):264-9.
• ²⁷
  Graber TM. Orthodontics, principles and pratice. 3th ed. Philadelphia: Saunders; 1972.
• ²⁸
  Felicio CM, Ferreira CLP. Protocolof orofacial myofunctional evaluation with scores. Int J Pediatr Otorhinolaryngol. 2008;72(3):367-78.
• ²⁹
  Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electr Kinesiol. 2000;10(5):361-74.
• ³⁰
  Cai C, Au IP, An W, Cheung RT. Facilitatory and inhibitory effects of Kinesio tape: fact or fad? J Sci Med Sport. 2016;19(2):109-12.
• ³¹
  Nagae MH, Bérzin F, Alves MC. Exacerbated activity of the buccinator muscle in subjects Angle Class III malocclusion. Rev Odontol UNESP. 2012;41(6):384-9.
• ³²
  Oliveira LF, Palinkas M, Vasconcelos PB, Regalo IH, Cecilio FA, Oliveira EF et al. Influence of age on the electromyographic fatigue threshold of the masseter and temporal muscles of healthy individuals . Archives of Oral Biology. 2017;84:1-5. Doi: https://doi.org/10.1016/j.archoralbio.2017.09.004
  » https://doi.org/https://doi.org/10.1016/j.archoralbio.2017.09.004
• ³³
  Po JMC, Kiser JÁ, Gallo LM, Tésenyi AJ, Herbison P, Farella M. Time frequency analysis of chewing activity in the natural environment. J. Dent. Res. 2011;90(10):1206-10.
• ³⁴
  Souza DR, Semeghini LB, Bérzin F. Oral myofunctional and electromyographic evaluation of the orbicularis oris and mentalis muscles in patients with class II/1 a division malocclusion submitted to first premolar extraction. J. Appl. Oral Sci. 2008;16(3):226-31.
• ³⁵
  Soderberg GL, Cook TM. Electromyography in biomechanics. PhysTher Alexandria. 1994;64(12):1813-20.

Publication Dates

• Publication in this collection
  Dec 2017

History

• Received
  11 Aug 2017
• Accepted
  20 Oct 2017