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Variables associated with mouth breathing diagnosis in children based on a multidisciplinary assessment

Variáveis associadas ao diagnóstico de respiração oral baseado em uma avaliação multidisciplinar

ABSTRACT

Purpose

: This study was conducted to identify variables associated with mouth breathing diagnosis in children, based on multidisciplinary domains.

Methods

119 children, six to 12 years old, underwent anamnesis, speech therapy (orofacial structures and stomatognathic functions), otorhinolaryngologic (OTRL) with clinical and endoscopic examinations, dental (occlusion) and physiotherapy (body posture and nasal patency) assessments. Nasal patency was evaluated using Peak Nasal Inspiratory Flow (PNIF) and the Nasal Obstruction Symptom Evaluation (NOSE) scale. A multiple logistic regression was performed considering breathing mode as the dependent variable and the co-variables from each multidisciplinary assessment as associated variables.

Results

Association with MB diagnosis was found in each professional domain with: nasal obstruction report (Odds ratio - OR=5.55), time of pacifier use (OR=1.25), convex facial type (OR=3.78), obtuse nasal angle (OR=4.30), half-open or open lip posture (OR=4.13), tongue position on the mouth floor (OR=5.88), reduced hard palate width (OR=2.99), unexpected contraction during mastication (OR=2.97), obstructive pharyngeal tonsils (OR=8.37), Angle Class II malocclusion (OR=10.85) and regular gingival maintenance (OR=2.89).

Conclusion

We concluded that a multidisciplinary diagnosis is important, given that each evaluation domain, including OTRL, dental and speech therapy, presented variables associated with MB diagnosis. Body posture and nasal patency variables were not associated with MB.

Keywords
Mouth Breathing; Nasal Obstruction; Diagnosis; Rhinitis; Child; Logistic Model

RESUMO

Objetivo

Este estudo foi conduzido para identificar as variáveis associadas ao diagnóstico de respiração oral em crianças, baseado nos domínios multidisciplinares.

Método

Cento e dezenove crianças, de seis a 12 anos, realizaram uma avaliação abrangente composta por uma anamnese e exames fonoaudiológico (estruturas orofaciais e funções estomatognáticas), otorrinolaringológico (avaliação clínica e endoscópica), odontológico (conservação oral e oclusão) e fisioterapêutico (postura corporal e permeabilidade nasal). A permeabilidade nasal foi aferida utilizando-se o Pico de Fluxo Inspiratório Nasal (PFIN) e a escala NOSE (Nasal Obstruction Symptom Evaluation). Foi realizada uma regressão logística múltipla, considerando o modo respiratório como variável dependente e as covariáveis de cada avaliação multidisciplinar como variáveis associadas.

Resultados

Foi encontrada uma associação do diagnóstico de respiração oral com variáveis de cada domínio profissional: relato de obstrução nasal (Odds ratio - OR=5,55), tempo de uso de chupeta (OR=1,25), tipo facial convexo (OR=3,78), ângulo nasolabial obtuso (OR=4,30), postura de lábios entreabertos e abertos (OR=4,13), postura de língua no assoalho oral (OR=5,88), largura do palato duro reduzida (OR=2,99), contrações inesperadas durante a mastigação (OR=2,97), tonsilas faríngeas obstrutivas (OR=8,37), má oclusão classe II de Angle (OR=10,85) e estado gengival regular (OR=2,89).

Conclusão

Concluiu-se que o diagnóstico multidisciplinar é importante, uma vez que as avaliações dos domínios fonoaudiológico, otorrinolaringológico e odontológico obtiveram variáveis associadas ao diagnóstico de respiração oral. As variáveis relacionadas à postura corporal e permeabilidade nasal não foram associadas ao diagnóstico de respiração oral.

Descritores
Respiração Bucal; Obstrução Nasal; Diagnóstico; Rinite; Criança; Modelos Logísticos

INTRODUCTION

Mouth breathing (MB) has been an object of interest in various studies during recent decades(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....

2 Junqueira P, Marchesan IQ, Oliveira LR, Ciccone E, Haddad L, Rizzo MC. Speech-language pathology findings in patients with mouth breathing: multidisciplinary diagnosis according to etiology. Int J Orofacial Myology. 2010;36:27-32. PMid:23362600.

3 Milanesi JM, Borin G, Corrêa ECR, Silva AMT, Bortoluzzi DC, Souza JA. Impact of the mouth breathing occurred during childhood in the adult age: biophotogrammetric postural analysis. Int J Pediatr Otorhinolaryngol. 2011;75(8):999-1004. PMid:21632123. http://dx.doi.org/10.1016/j.ijporl.2011.04.018.
http://dx.doi.org/10.1016/j.ijporl.2011....

4 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
-55 Pacheco MCT, Fiorott BS, Finck NS, Araújo MTM. Craniofacial changes and symptoms of sleep-disordered breathing in healthy children. Dental Press J Orthod. 2015;20(3):80-7. PMid:26154460. http://dx.doi.org/10.1590/2176-9451.20.3.080-087.oar.
http://dx.doi.org/10.1590/2176-9451.20.3...
) and has been considered a public health problem in Brazil, with prevalence in school-age children varying between 55 and 60%(66 Felcar JM, Bueno IR, Massan ACS, Torezan RP, Cardoso JR. Prevalence of mouth breathing in children from an elementary school. Cien Saude Colet. 2010;15(2):437-44. PMid:20414610. http://dx.doi.org/10.1590/S1413-81232010000200020.
http://dx.doi.org/10.1590/S1413-81232010...
). MB etiologic factors may be obstructive, such as palatine and pharyngeal tonsillary hypertrophy and nasal septum deviation. They can also be described as functional, when resulting from prolonged oral habits, muscular alterations, transitory edema of nasal mucosa such as intermittent rhinitis, and repaired airway obstruction(77 Lee SY, Guilleminault C, Chiu HY, Sullivan SS. Mouth breathing, “nasal disuse,” and pediatric sleep-disordered breathing. Sleep Breath. 2015;19(4):1257-64. PMid:25877805. http://dx.doi.org/10.1007/s11325-015-1154-6.
http://dx.doi.org/10.1007/s11325-015-115...

8 Basheer B, Hegde KS, Bhat SS, Umar D, Baroudi K. Influence of mouth breathing on the dentofacial growth of children: a cephalometric study. J Int Oral Health. 2014;6(6):50-5. PMid:25628484.
-99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
). Understanding its etiology may be decisive to obtain a clear MB clinical picture(44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
).

MB consequences may include not only craniofacial changes, but also changes throughout the whole body(33 Milanesi JM, Borin G, Corrêa ECR, Silva AMT, Bortoluzzi DC, Souza JA. Impact of the mouth breathing occurred during childhood in the adult age: biophotogrammetric postural analysis. Int J Pediatr Otorhinolaryngol. 2011;75(8):999-1004. PMid:21632123. http://dx.doi.org/10.1016/j.ijporl.2011.04.018.
http://dx.doi.org/10.1016/j.ijporl.2011....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
). The most commonly described characteristics are an increased lower third of the face, deep and narrow palate, Angle Class II malocclusion, posterior crossbite, anterior openbite, shortened upper lip, everted lower lip and forward head posture(33 Milanesi JM, Borin G, Corrêa ECR, Silva AMT, Bortoluzzi DC, Souza JA. Impact of the mouth breathing occurred during childhood in the adult age: biophotogrammetric postural analysis. Int J Pediatr Otorhinolaryngol. 2011;75(8):999-1004. PMid:21632123. http://dx.doi.org/10.1016/j.ijporl.2011.04.018.
http://dx.doi.org/10.1016/j.ijporl.2011....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
,99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
,1010 Cattoni DM, Fernandes FDM, Di Francesco RC, Latorre MRDO. Quantitative evaluation of the orofacial morphology: anthropometric measurements in healthy and mouth-breathing children. Int J Orofacial Myology. 2009;35:44-54. PMid:20572437.). Nevertheless, the association of some of these alterations with mouth breathing has still not been completely verified.

MB diagnosis is predominantly clinical, given that it is a condition including several organic systems. Some exams and tests may be complementary, identifying its etiologic factors(66 Felcar JM, Bueno IR, Massan ACS, Torezan RP, Cardoso JR. Prevalence of mouth breathing in children from an elementary school. Cien Saude Colet. 2010;15(2):437-44. PMid:20414610. http://dx.doi.org/10.1590/S1413-81232010000200020.
http://dx.doi.org/10.1590/S1413-81232010...
). There are uncertainties regarding MB diagnosis, given that etiologic factors may be concomitant, acting intermittently or continuously, in addition to the complexity of quantifying its magnitude/severity(1111 Pacheco MCT, Casagrande CF, Teixeira LP, Finck NS, Araújo MTM. Guidelines proposal for clinical recognition of mouth breathing children. Dental Press J Orthod. 2015;20(4):39-44. PMid:26352843. http://dx.doi.org/10.1590/2176-9451.20.4.039-044.oar.
http://dx.doi.org/10.1590/2176-9451.20.4...
,1212 Rossi RC, Rossi NJ, Rossi NJC, Yamashita HK, Pignatari SN. Dentofacial characteristics of oral breathers in different ages: a retrospective case–control study. Prog Orthod. 2015;16(23):1-10. PMid:26174032.). A recent study has investigated MB perception by orthodontists, as well as proposed and tested guidelines for MB recognition, through visual assessment, semi-structured interview and breathing tests(1111 Pacheco MCT, Casagrande CF, Teixeira LP, Finck NS, Araújo MTM. Guidelines proposal for clinical recognition of mouth breathing children. Dental Press J Orthod. 2015;20(4):39-44. PMid:26352843. http://dx.doi.org/10.1590/2176-9451.20.4.039-044.oar.
http://dx.doi.org/10.1590/2176-9451.20.4...
).

A lack of standardization of MB diagnosis makes it hard to establish a comparison between studies and the application of a global clinical approach. Some relevant factors have been found to define this diagnosis, which may consist of predictors for MB recognition, such as a lack of lip sealing associated with typical signs and symptoms(99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
,1313 Neiva PD, Kirkwood RN, Godinho R. Orientation and position of head posture, scapula and thoracic spine in mouth-breathing children. Int J Pediatr Otorhinolaryngol. 2009;73(2):227-36. PMid:19056131. http://dx.doi.org/10.1016/j.ijporl.2008.10.006.
http://dx.doi.org/10.1016/j.ijporl.2008....
), as well as multidisciplinary evaluation(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
) or association of these items with respiratory tests, such as graded mirror or water retention tests(55 Pacheco MCT, Fiorott BS, Finck NS, Araújo MTM. Craniofacial changes and symptoms of sleep-disordered breathing in healthy children. Dental Press J Orthod. 2015;20(3):80-7. PMid:26154460. http://dx.doi.org/10.1590/2176-9451.20.3.080-087.oar.
http://dx.doi.org/10.1590/2176-9451.20.3...
,88 Basheer B, Hegde KS, Bhat SS, Umar D, Baroudi K. Influence of mouth breathing on the dentofacial growth of children: a cephalometric study. J Int Oral Health. 2014;6(6):50-5. PMid:25628484.).

This study was conducted to identify variables associated with MB diagnosis, based on multidisciplinary domains, including anamnesis, speech therapy, otorhinolaryngologic, odontologic and physiotherapeutic assessments.

METHODS

The present study has an observational and cross-sectional design. It was derived from a Project titled “Integrated characterization and evaluation of orofacial motricity and body posture diseases – phase II”, approved by the Ethics and Research Committee of the aforementioned institution, under protocol 08105512.0.0000.5346.

Sample size calculation, based on the prevalence of approximately 55% of mouth breathers in school-age children(66 Felcar JM, Bueno IR, Massan ACS, Torezan RP, Cardoso JR. Prevalence of mouth breathing in children from an elementary school. Cien Saude Colet. 2010;15(2):437-44. PMid:20414610. http://dx.doi.org/10.1590/S1413-81232010000200020.
http://dx.doi.org/10.1590/S1413-81232010...
), and with a significance level of 0.05 and absolute precision of 0.08, resulted in an expected number of 149 subjects.

Study participants were recruited from an elementary school, by written invitation sent to parents. To meet the ethics requirements, children's parents or tutors were informed about the study objective and procedures, in addition to signing the Consent Form, according to 466/12 resolution of Conselho Nacional de Saúde (CNS).

The inclusion criteria consisted of: age six to 12 years old, mixed or permanent dentition and normal ventilatory function, verified by spirometry. The spirometric evaluation (One Flow – Clement Clarke) was carried out, according to the American Thoracic Society(1414 ATS: American Thoracic Society. Lung function testing: selection of reference values and interpretative strategies. Am Rev Respir Dis. 1991;144(5):1202-18. PMid:1952453. http://dx.doi.org/10.1164/ajrccm/144.5.1202.
http://dx.doi.org/10.1164/ajrccm/144.5.1...
) and Sociedade Brasileira de Pneumologia e Tisiologia(1515 SBPT: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para testes de função pulmonar. J Bras Pneumol. 2002;28(3):S1-238.). The exclusion criteria were: signs and symptoms of exacerbated rhinitis; antihistaminic or corticoid therapy (oral or topic) in the last thirty days; currently undergoing or having undergone orthodontic treatment, physiotherapy or speech therapy; facial surgery or trauma or evident signs of neurological disease and/or craniofacial malformation.

Participants underwent speech therapy, otorhinolaryngologic (OTRL), dental and physiotherapy assessments. Breathing mode was defined by the agreement of three conditions: parent report(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
) and OTRL(1616 Uhlig SE, Marchesi LM, Duarte H, Araújo MTM. Association between respiratory and postural adaptations and self-perception of school-aged children with mouth breathing in relation to their quality of life. Braz J Phys Ther. 2015;19(3):201-10. PMid:26083601. http://dx.doi.org/10.1590/bjpt-rbf.2014.0087.
http://dx.doi.org/10.1590/bjpt-rbf.2014....
) and speech therapist(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
) assessments, without taking into account orofacial and postural features. The following aspects were considered for mouth breathing categorization: report of open mouth throughout the majority of the day, open mouth at night, nocturnal drooling or snoring for more than six months and breathing through the mouth, confirmed by speech therapist and OTRL examinations.

An anamnesis investigating problems related to nasal obstruction, by NOSE scale, and clinical history from MBGR orofacial protocol(1717 Marchesan IQ, Berretin-Félix G, Genaro KF. MBGR protocol of orofacial myofunctional evaluation with scores. Int J Orofacial Myology. 2012;38:38-77. PMid:23362752.) was carried out. The following aspects were investigated: physical activity, frequent cold, throat problems, halitosis, asthma/bronchitis, pneumonia, restless and fragmented sleep, artificial and breastfeeding time, oral habits (pacifier, baby bottle and finger sucking), learning difficulties, lack of attention and concentration, difficulty at school or in relationships. Children answered five questions of the NOSE scale with the help of their parents, related to nasal obstruction and how much it represented a problem during the month prior. NOSE scale scores vary from zero (no problem) to 100 (highest severity problem)(1818 Bezerra TF, Padua FG, Pilan RR, Stewart MG, Voegels RL. Cross-cultural adaptation and validation of a Quality of Life questionnaire: the Nasal Obstruction Symptom Evaluation questionnaire. Rhinology. 2011;49(2):227-31. PMid:21743882.).

The sample selection, evaluation methods and analyzed data of the study are shown in Figure 1 (Flowchart).

Figure 1
Flowchart with selection, evaluation methods and variables

A stomatognathic system exam carried out by an experienced speech therapist in orofacial motricity using MBGR protocol(1717 Marchesan IQ, Berretin-Félix G, Genaro KF. MBGR protocol of orofacial myofunctional evaluation with scores. Int J Orofacial Myology. 2012;38:38-77. PMid:23362752.), evaluated structures and masticatory, deglutition and speech functions. Procedural guidelines were followed, and photographs and filming were made (Sony Cyber Shot 7.2 Megapixels). Nasal expiratory flow testing was carried out using a graduated mirror (ProFono®, Brazil). Disposable items such as procedural gloves, cotton, tongue depressor and transparent glass were also used.

Children were also examined by an otorhinolaryngologist, who considered aspects such as palatine and pharyngeal tonsillary hypertrophy, nasal septum deviation and nasal mucosa edema, using oroscopy and anterior rhinoscopy. Exams such as nasoendoscopy or lateral cavum X-ray were carried out, depending on the child’s acceptance. The palatine and pharyngeal tonsil assessments adopted Brodsky and Koch(1919 Brodsky L, Koch RJ. Anatomic correlates of normal and diseased adenoids in children. Laryngoscope. 1992;102(11):1268-74. PMid:1405989. http://dx.doi.org/10.1288/00005537-199211000-00013.
http://dx.doi.org/10.1288/00005537-19921...
) and Parikh et al.(2020 Parikh SR, Coronel M, Lee JJ, Brown SM. Validation of a new grading system for endoscopic examination of adenoid hypertrophy. Otolaryngol Head Neck Surg. 2006;135(5):684-7. PMid:17071294. http://dx.doi.org/10.1016/j.otohns.2006.05.003.
http://dx.doi.org/10.1016/j.otohns.2006....
) classifications, respectively. Rhinitis signs and symptoms were also investigated and, for rhinitis classification, ARIA (Allergic Rhinitis and its Impact on Asthma) initiative(2121 Bousquet J, Khaltaev N, Cruz AA, Denburg J, Fokkens WJ, Togias A, et al. Allergic Rhinitis and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA(2)LEN and AllerGen). Allergy. 2008;63(Suppl 86):8-160. PMid:18331513. http://dx.doi.org/10.1111/j.1398-9995.2007.01620.x.
http://dx.doi.org/10.1111/j.1398-9995.20...
), related to frequency (intermittent or persistent) and symptom intensity (mild or moderate/severe), was used.

Dental evaluation was carried out by an experienced orthodontist based on MBGR protocol criteria. The examination was carried out at school, with the child sitting on a normal chair, following the items described in the flowchart.

The Peak Nasal Inspiratory Flow (PNIF) measure was used for objective nasal patency assessment. PNIF was evaluated by a physical therapist using InCheck Inspiratory Flow Meter (Clement Clarke International, the United Kingdom). A Residual Volume (RV) technique was performed, i.e., a complete expiration followed by a nasal deep inspiration as fast and as strong as possible, with closed mouth and well-fitted mask to face. The highest value obtained from three repetitions was considered(99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
). The values obtained were transformed into a percentage of predicted values of PNIF, established by Ibiapina et al.(2222 Ibiapina CC, Andrade CR, Camargos PAM, Alvim CG, Cruz AA. Reference values for peak nasal inspiratory flow in children and adolescents in Brazil. Rhinology. 2011;49(3):304-8. PMid:21858260.), according to sex and stature.

Selected children were evaluated using photographic records with biophotogrammetric analysis, using the Software of Postural Evaluation (SAPo v.0.68). Body posture evaluation (photographs and analyses) was performed by an experienced physiotherapist. The photographs were obtained in orthostatic posture in right lateral view(33 Milanesi JM, Borin G, Corrêa ECR, Silva AMT, Bortoluzzi DC, Souza JA. Impact of the mouth breathing occurred during childhood in the adult age: biophotogrammetric postural analysis. Int J Pediatr Otorhinolaryngol. 2011;75(8):999-1004. PMid:21632123. http://dx.doi.org/10.1016/j.ijporl.2011.04.018.
http://dx.doi.org/10.1016/j.ijporl.2011....
,2323 Weber P, Corrêa ECR, Milanesi JM, Soares JC, Trevisan MA. Craniocervical posture: cephalometric and biophotogrammetric analysis. Braz J Oral Sci. 2012;11(3):416-21.). The postural measures used for analysis are shown in Figure 2.

Figure 2
Postural Measures. (A) HHA: Horizontal Head Alignment; (B) CD: Cervical Distance; LD: Lumbar Distance; (C) FE: Flexion-extension head position

Data analysis

For data analysis, STATISTICA 9.1 (Statistica for Windows – release 9.1 Stat Soft) and SPSS 13.0 (Statistical Package for the Social Sciences) software programs were used. Data related to sex, age and BMI were presented by descriptive measures. The data homogeneity between groups was tested by Chi-squared for sex and t-Student for age and BMI.

A multiple logistic regression was carried out considering breathing mode (nasal or mouth) as the dependent variable (outcome) and co-variables related to anamnesis (26 items), OTRL exam (11 items), speech therapist evaluation (78 items), dental evaluation (9 items) and physiotherapeutic assessment (11 items) as independent variables (associated factors).

For selection of independent variables suitable for the multiple model, a 5% significance level was adopted. Four multiple model proposals were elaborated, using “enter” method, one for each evaluated professional domain. A 5% significance level was adopted.

RESULTS

Multiple models were elaborated with a total sample of 119 children with mean age of 8.5 ± 1.62 years old, 64 boys and 55 girls. The nasal breathing group was constituted by 49 children and the mouth breathing group by 70 children. Both groups were homogeneous relative to age (p=0.377), sex (p=0.210) and BMI (p=0.245).

Four multiple models, one for each multidisciplinary domain, were elaborated. In the physiotherapy domain, single regression did not present any variable suitable for a multiple model.

Table 1 shows a multiple model proposal based on anamnesis for MB diagnosis. Six variables were selected for single regression and, of these, two remained in the multiple model, which were nasal obstruction (OR 5.55) and pacifier use (OR 1.25), both associated with MB diagnosis.

Table 1
Anamnesic data associated with mouth breathing diagnosis

The multiple model proposal related to the speech therapy evaluation (Table 2) showed a greater number of variables associated with the MB diagnosis. According to the results, convex facial type (OR 3.78), obtuse nasolabial angle (OR 4.30), half-open or open lip posture (OR 4.13), habitual tongue position on the mouth floor (OR 5.88), reduced hard palate width (OR 2.99) and unexpected contractions during mastication (OR 2.97) were associated with MB diagnosis.

Table 2
Speech therapy variables associated with mouth breathing diagnosis

Table 3 presents the multiple model proposal derived from the OTRL exam variables, with obstructive pharyngeal tonsils (OR 8.37) and report of nasal obstruction (OR 7.95) showing an association with MB diagnosis.

Table 3
Otorhinolaryngological variables associated with mouth breathing diagnosis

Table 4 presents the multiple model proposal for dental variables, with Angle Class II subdivision 1 malocclusion on left (OR 10.85) and regular gingival maintenance (OR 2.89) showing an association with MB diagnosis .

Table 4
Dental variables associated with mouth breathing diagnosis

DISCUSSION

Given that there is no consensus in the literature concerning MB diagnosis, a comprehensive and careful multidisciplinary clinical evaluation was conducted. A multiple model proposal for each professional area was elaborated.

Based on anamnesis, an association between nasal obstruction and MB was verified, i.e., children with nasal obstruction presented a likelihood 5.55-times higher of MB diagnosis, compared to children without obstruction. Regarding pacifier use, for each year of use, the probability of MB diagnosis increased by 25%. Another study observed higher nasal resistance in mist (oronasal) breathing children, concluding that it leads to mouth breathing(2424 Fujimoto S, Yamaguchi K, Gunjigake K. Clinical estimation of mouth breathing. Am J Orthod Dentofacial Orthop. 2009;136(5):630.e1-7. PMid:19892274. http://dx.doi.org/10.1016/j.ajodo.2009.03.034.
http://dx.doi.org/10.1016/j.ajodo.2009.0...
). Nevertheless, it was not always the case that a mouth breather will have higher nasal resistance, as an MB child may have prolonged oral habits, which are also etiological factors for this breathing mode(2525 Nihi VS, Maciel SM, Jarrus ME, Nihi FM, Salles CL, Pascotto RC, et al. Pacifier-sucking habit duration and frequency on occlusal and myofunctional alterations in preschool children. Braz Oral Res. 2015;29(1):1-7. PMid:25493658. http://dx.doi.org/10.1590/1807-3107BOR-2015.vol29.0013.
http://dx.doi.org/10.1590/1807-3107BOR-2...
).

Pacifier use was associated with reduced maxillary intercanine distance and altered resting tongue position, showing that this habit may be associated with alterations in hard palate shape. An association of resting lip position (partially closed at rest/closed with tension), posterior crossbite and inadequate swallowing with pacifier was also observed, demonstrating a need for awareness about the risks of prolonged pacifier-use(2525 Nihi VS, Maciel SM, Jarrus ME, Nihi FM, Salles CL, Pascotto RC, et al. Pacifier-sucking habit duration and frequency on occlusal and myofunctional alterations in preschool children. Braz Oral Res. 2015;29(1):1-7. PMid:25493658. http://dx.doi.org/10.1590/1807-3107BOR-2015.vol29.0013.
http://dx.doi.org/10.1590/1807-3107BOR-2...
).

The literature describes a wide range of characteristics commonly attributed to mouth breathers. The most frequent are dolichofacial type or long face(44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
,55 Pacheco MCT, Fiorott BS, Finck NS, Araújo MTM. Craniofacial changes and symptoms of sleep-disordered breathing in healthy children. Dental Press J Orthod. 2015;20(3):80-7. PMid:26154460. http://dx.doi.org/10.1590/2176-9451.20.3.080-087.oar.
http://dx.doi.org/10.1590/2176-9451.20.3...
), convex facial profile(2626 Migliorucci RR, Sovinski SR, Passos DC, Bucci AC, Salgado MH, Nary H Fo, et al. Orofacial functions and quality of life in oral health in subjects with dentofacial deformity. CoDAS. 2015;27(3):255-9. PMid:26222942. http://dx.doi.org/10.1590/2317-1782/20152014162.
http://dx.doi.org/10.1590/2317-1782/2015...
), deep and narrow hard palate(55 Pacheco MCT, Fiorott BS, Finck NS, Araújo MTM. Craniofacial changes and symptoms of sleep-disordered breathing in healthy children. Dental Press J Orthod. 2015;20(3):80-7. PMid:26154460. http://dx.doi.org/10.1590/2176-9451.20.3.080-087.oar.
http://dx.doi.org/10.1590/2176-9451.20.3...
,99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
), open lip posture and lowered tongue(2626 Migliorucci RR, Sovinski SR, Passos DC, Bucci AC, Salgado MH, Nary H Fo, et al. Orofacial functions and quality of life in oral health in subjects with dentofacial deformity. CoDAS. 2015;27(3):255-9. PMid:26222942. http://dx.doi.org/10.1590/2317-1782/20152014162.
http://dx.doi.org/10.1590/2317-1782/2015...
), everted lower lip(1010 Cattoni DM, Fernandes FDM, Di Francesco RC, Latorre MRDO. Quantitative evaluation of the orofacial morphology: anthropometric measurements in healthy and mouth-breathing children. Int J Orofacial Myology. 2009;35:44-54. PMid:20572437.), Angle Class II and posterior crossbyte malocclusion(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
), changes in stomatognathic functions(2727 Souza JF, Grechi TH, Anselmo-Lima WT, Trawitzki LV, Valera FC. Mastication and deglutition changes in children with tonsillar hypertrophy. Rev Bras Otorhinolaryngol. 2013;79(4):424-8. PMid:23929140. http://dx.doi.org/10.5935/1808-8694.20130076.
http://dx.doi.org/10.5935/1808-8694.2013...
) and postural misalignments(33 Milanesi JM, Borin G, Corrêa ECR, Silva AMT, Bortoluzzi DC, Souza JA. Impact of the mouth breathing occurred during childhood in the adult age: biophotogrammetric postural analysis. Int J Pediatr Otorhinolaryngol. 2011;75(8):999-1004. PMid:21632123. http://dx.doi.org/10.1016/j.ijporl.2011.04.018.
http://dx.doi.org/10.1016/j.ijporl.2011....
). Nevertheless, concerning the MB mode, which affects various body systems and craniofacial growth, there was no agreement to describe this condition.

In the present study, it was observed that the main features associated with mouth breathing diagnosis confirmed the literature findings. The probability of a mouth breathing (MB) diagnosis was 3.78-times higher in children with convex facial related to straight profile and 4.30-times higher in children with obtuse nasolabial compared to neutral angle (90 to 110˚). A cephalometric study found no difference between mouth and nasal breathing children in nasolabial angle, however convex facial type and diagnosis for MB were associated(88 Basheer B, Hegde KS, Bhat SS, Umar D, Baroudi K. Influence of mouth breathing on the dentofacial growth of children: a cephalometric study. J Int Oral Health. 2014;6(6):50-5. PMid:25628484.). Convex facial type was associated with mouth and mist breathing mode, chronic unilateral masticatory pattern, excessive contraction of mentalis and perioral musculature during mastication and forward tongue and head movement during swallowing(2626 Migliorucci RR, Sovinski SR, Passos DC, Bucci AC, Salgado MH, Nary H Fo, et al. Orofacial functions and quality of life in oral health in subjects with dentofacial deformity. CoDAS. 2015;27(3):255-9. PMid:26222942. http://dx.doi.org/10.1590/2317-1782/20152014162.
http://dx.doi.org/10.1590/2317-1782/2015...
).

MB diagnosis was 4.13-times higher in children with half-open or open lip posture and 5.88-times higher in children with tongue position on the mouth floor. Open, lowered or forward lip posture or with inadequate tongue tonus were also observed in a study with MB children(22 Junqueira P, Marchesan IQ, Oliveira LR, Ciccone E, Haddad L, Rizzo MC. Speech-language pathology findings in patients with mouth breathing: multidisciplinary diagnosis according to etiology. Int J Orofacial Myology. 2010;36:27-32. PMid:23362600.). Another study, which induced mouth breathing in rats, demonstrated that a partial nasal obstruction may produce a forward tongue position to improve nasal patency and, combined with the lip incompetence, contribute to morphological changes to the craniofacial complex(2828 Uchima Koecklin KH, Kato C, Funaki Y, Hiranuma M, Ishida T, Fujita K, et al. Effect of unilateral nasal obstruction on tongue protrusion forces in growing rats. J Appl Physiol. 2015;118(9):1128-35. PMid:25767036. http://dx.doi.org/10.1152/japplphysiol.01152.2014.
http://dx.doi.org/10.1152/japplphysiol.0...
).

In children presenting reduced hard palate width, MB diagnosis is 2.99-times higher compared to those with normal width. Authors found a strong association of narrow and deep hard palate with MB(55 Pacheco MCT, Fiorott BS, Finck NS, Araújo MTM. Craniofacial changes and symptoms of sleep-disordered breathing in healthy children. Dental Press J Orthod. 2015;20(3):80-7. PMid:26154460. http://dx.doi.org/10.1590/2176-9451.20.3.080-087.oar.
http://dx.doi.org/10.1590/2176-9451.20.3...
,99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
). A narrower and deeper hard palate was observed in MB adults than in nasal breathing adults. Such findings were explained by the lack of expansion function of the tongue and reduced orofacial muscle tonus in MB individuals(99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
). In the present research, hard palate depth was not related to MB diagnosis. However, it should be emphasized that these features were clinically assessed rather than using quantitative measurements as was the case in the study mentioned.

Among stomatognathic functions, only mastication presented one variable associated with MB diagnosis, that is, the presence of unexpected contraction of orbicularis and mentalis muscles during mastication with a 2.97-times greater probability for this outcome. As mentioned above, chronic unilateral masticatory pattern and excessive contraction of mentalis and perioral musculature during mastication were related to convex facial type, an MB characteristic also found in the present study(2626 Migliorucci RR, Sovinski SR, Passos DC, Bucci AC, Salgado MH, Nary H Fo, et al. Orofacial functions and quality of life in oral health in subjects with dentofacial deformity. CoDAS. 2015;27(3):255-9. PMid:26222942. http://dx.doi.org/10.1590/2317-1782/20152014162.
http://dx.doi.org/10.1590/2317-1782/2015...
). During mastication, unsystematic lip sealing, tongue interposition and tension in mentalis and orbicularis oris muscles, necessary to keep food inside the mouth for swallowing, were also observed in the MB child group(2727 Souza JF, Grechi TH, Anselmo-Lima WT, Trawitzki LV, Valera FC. Mastication and deglutition changes in children with tonsillar hypertrophy. Rev Bras Otorhinolaryngol. 2013;79(4):424-8. PMid:23929140. http://dx.doi.org/10.5935/1808-8694.20130076.
http://dx.doi.org/10.5935/1808-8694.2013...
).

The OTRL variables that showed greatest association with MB diagnosis were nasal obstruction and obstructive pharyngeal tonsils, with MB diagnosis being 8.37 and 7.95 - times more likely, respectively. The highest nasal flow resistance, due to cold, nasal allergies, prolonged rhinitis and adenoid hypertrophy, impairs posterior palatal sealing by soft palate and tongue, hampering airflow passing through the mouth(2929 Ikenaga N, Yamaguchi K, Daimon S. Effect of mouth breathing on masticatory muscle activity during chewing food. J Oral Rehabil. 2013;40(6):429-35. PMid:23566154. http://dx.doi.org/10.1111/joor.12055.
http://dx.doi.org/10.1111/joor.12055...
). Therefore, it is clear that nasal obstruction, resulting from adenoid hypertrophy or rhinitis, seems to have an important role in MB diagnosis, with a greater impact stemming from the first condition.

Regarding dental examination, the multiple model proposal included two variables. Angle Class II subdivision 1 (on the left side) malocclusion and regular gingival maintenance presenting, respectively, a 10.85 and 2.89-times greater chance of MB diagnosis. A current study with 487 children, 5-12 year old, has investigated an association between dental and skeletal variables and MB(1212 Rossi RC, Rossi NJ, Rossi NJC, Yamashita HK, Pignatari SN. Dentofacial characteristics of oral breathers in different ages: a retrospective case–control study. Prog Orthod. 2015;16(23):1-10. PMid:26174032.), finding Angle class II malocclusion, mandibular retrusion and short mandible as factors that increase the probability of MB diagnosis. Previous studies also found an association between Angle Class II and MB(11 Souki BQ, Pimenta GB, Souki MQ, Franco LP, Becker HM, Pinto JA. Prevalence of malocclusion among mouth breathing children: do expectations meet reality? Int J Pediatr Otorhinolaryngol. 2009;73(5):767-73. PMid:19282036. http://dx.doi.org/10.1016/j.ijporl.2009.02.006.
http://dx.doi.org/10.1016/j.ijporl.2009....
,44 Franco LP, Souki BQ, Cheib PL, Abrão M, Pereira TBJ, Becker HMG, et al. Are distinct etiologies of upper airway obstruction in mouth-breathing children associated with different cephalometric patterns? Int J Pediatr Otorhinolaryngol. 2015;79(2):223-8. PMid:25563906. http://dx.doi.org/10.1016/j.ijporl.2014.12.013.
http://dx.doi.org/10.1016/j.ijporl.2014....
).

Postural measurements, evaluated by a physiotherapist, showed no association with MB diagnosis. Nevertheless, despite no association being observed, it should be highlighted that postural changes, mainly in the craniocervical region, represent important clinical aspects for an MB therapeutic approach, given that respiratory and postural adaptations may increase the chance of mouth breathing persistence(1616 Uhlig SE, Marchesi LM, Duarte H, Araújo MTM. Association between respiratory and postural adaptations and self-perception of school-aged children with mouth breathing in relation to their quality of life. Braz J Phys Ther. 2015;19(3):201-10. PMid:26083601. http://dx.doi.org/10.1590/bjpt-rbf.2014.0087.
http://dx.doi.org/10.1590/bjpt-rbf.2014....
). Postural adaptations are also considered a compensatory mechanism to assist the breathing function(3030 Okuro RT, Morcillo AM, Sakano E, Schivinski CIS, Ribeiro MAGO, Ribeiro JD. Exercise capacity, respiratory mechanics and posture in mouth breathers. Rev Bras Otorhinolaryngol. 2011;77(5):656-62. PMid:22030977. http://dx.doi.org/10.1590/S1808-86942011000500020.
http://dx.doi.org/10.1590/S1808-86942011...
). In cases of MB diagnosis, children should be referred for physiotherapy evaluation.

Concerning subjective and objective nasal obstruction measurements, NOSE scale and PNIF, respectively, only the NOSE scores were associated with MB diagnosis in single regression. Peak Nasal Inspiratory Flow (PNIF) is an objective, reliable and easy-to-use instrument, applicable by any health professional(99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
,2222 Ibiapina CC, Andrade CR, Camargos PAM, Alvim CG, Cruz AA. Reference values for peak nasal inspiratory flow in children and adolescents in Brazil. Rhinology. 2011;49(3):304-8. PMid:21858260.). The volitional character of PNIF exam, mainly with children, should be considered. Additionally, presence of nasal obstruction was associated with MB diagnosis in the multiple model. These results indicate that subjective aspects seem to be more related to MB diagnosis. However, in a previous study, a negative and moderate correlation between PNIF and NOSE scale was found in MB adults(99 Trevisan ME, Bellinaso JH, Pacheco AB, Augé LB, Silva AM, Corrêa ECR. Respiratory mode, nasal patency and palatine dimensions. CoDAS. 2015;27(2):201-6. PMid:26107087. http://dx.doi.org/10.1590/2317-1782/20152014177.
http://dx.doi.org/10.1590/2317-1782/2015...
).

Some variables related to swallowing, speech, body posture and nasal patency showed no association with MB. It is noticeable that orofacial and postural compensations deriving from MB may vary among children, besides being influenced by genetic factors and craniofacial growth.

The observational and qualitative nature of orofacial evaluation may be a limitation in this study, however MBGR consists of a systematic and standardized procedure used for MB evaluation. In addition, no quantitative parameters were determined for this evaluation. Due to the diversity of variables and professionals involved in the assessments, the expected sample size was not achieved. Therefore, some variables of this study presented a wide confidence interval, suggesting care in the interpretation of the results.

The criteria used for MB and nasal breathing group definition were nocturnal drooling, snoring and breathing through mouth throughout the majority of the day and night, according to parent reports. These aspects were not included as suitable variables for the multiple model, as they are set as MB typical characteristics.

Based on these findings, in addition to the typical characteristics, the variables that constituted the multiple models presented in this research are suggested for MB diagnosis.

CONCLUSION

Variables associated with MB diagnosis in each professional domain were: nasal obstruction report, time of pacifier use, convex facial type, obtuse nasal angle, half-open or open lip posture, tongue position on the mouth floor, reduced hard palate width, unexpected contraction of orbicularis and mentalis muscles during mastication, obstructive pharyngeal tonsils, Angle Class II malocclusion and regular gingival maintenance.

Therefore, we concluded that a multidisciplinary diagnosis is important, given that each evaluation domain, including OTRL, dental and speech therapy, presented variables associated with MB diagnosis. Body posture and nasal patency variables were not associated with MB.

ACKNOWLEDGEMENTS

The authors would like to thank Kátia Sebalhos and Shalina Cecchin for the English revision.

  • Study carried out at the Programa de Pós-graduação em Distúrbios da Comunicação Humana, Universidade Federal de Santa Maria – UFSM - Santa Maria (RS), Brasil.
  • Financial support: nothing to declare.

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Publication Dates

  • Publication in this collection
    2018

History

  • Received
    20 Apr 2017
  • Accepted
    31 July 2017
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