Influence of the breathing pattern on the learning process: a systematic review of literature Please cite this article as: Ribeiro GCA, dos Santos ID, Santos ACN, Paranhos LR, César CPHAR. Influence of the breathing pattern on the learning process: a systematic review of literature. Braz J Otorhinolaryngol. 2016;82:466-78.

Genef Caroline Andrade Ribeiro Isadora Diniz dos Santos Ana Claudia Nascimento Santos Luiz Renato Paranhos Carla Patrícia Hernandez Alves Ribeiro César About the authors

ABSTRACT

INTRODUCTION:

Mouth breathing leads to negative consequences on quality of life, especially in school-age children.

OBJECTIVE:

To determine whether the breathing pattern influences children's learning process.

METHODS:

This systematic review was carried out according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) instructions, with no restrictions regarding the year of publication and language, created based on the clinical question formulation according to the Problem/Patient/Population, Intervention/Indicator, Comparison, Outcome (PICO) strategy: "Is the mouth-breathing child more likely to have learning disabilities when compared to nasal breathers?" in the SciELO, PubMed, LILACS, and Scopus electronic databases. Google Scholar was used to search the gray literature. The keywords "learning," "mouth breathing," and their equivalent terms in Portuguese were used in an integrated manner. The studies included in the review were observational, conducted with schoolchildren aged 7-11 years. Afterwards, the studies were evaluated regarding their methodological quality. The research was performed by two eligible reviewers.

RESULTS:

A total of 357 records were obtained, of which 43 records were duplicate. After applying the eligibility criteria, ten articles were included in the research scope. Half of the studies used a control group and otorhinolaryngological assessment, whereas a minority used validated (20%) and sample calculation protocols (10%). The evaluation procedures were varied. Overall, 80% of the articles showed a higher incidence of learning disabilities among mouth breathers.

CONCLUSION:

This systematic review has shown that mouth breathers are more likely to have learning difficulties than nasal breathers.

Keywords:
Mouth breathing; Learning; Reading; Writing; Mathematics

Resumo

Introdução:

A respiração oral traz consequências negativas para a qualidade de vida das pessoas, principalmente para escolares.

Objetivo:

Verificar se o modo respiratório influencia no processo de aprendizagem infantil.

Método:

Esta revisão sistemática foi realizada seguindo as instruções PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses), sem restrição quanto ao ano de publicação e idioma, elaborada a partir da formulação de questão clínica elaborada pela estratégia P.I.C.O.: ''A criança respiradora oral tem mais chances de apresentar dificuldades de aprendizagem quando comparada à respiradora nasal?'', nas bases de dados eletrônicas SciELO, PubMed, LILACS e Scopus. Foi utilizado o Google Scholar para pesquisa da literatura cinza. As palavras-chave ''aprendizagem'', ''respiração bucal'', ''learning'' e ''mouth breathing'' foram utilizadas de forma integrada. Os estudos incluídos foram observacionais, realizados com escolares entre sete e onze anos. Em seguida, os estudos foram avaliados quanto à sua qualidade metodológica. Toda a pesquisa foi realizada por dois revisores de elegibilidade.

Resultados:

Foram obtidos 357 registros, sendo 314 blindados (43 registros em duplicidade). Após os critérios de elegibilidade, dez artigos integraram o escopo desta pesquisa. Metade dos estudos usou grupo controle e fez uso de avaliação otorrinolaringológica, a minoria fez uso de protocolos validados (20%) e de cálculo amostral (10%). Os procedimentos de avaliação foram variados. De forma geral, 80% dos artigos evidenciaram maior ocorrência de distúrbio de aprendizagem em respiradores orais.

Conclusão:

Esta revisão sistemática demonstrou que indivíduos com respiração oral apresentam maior tendência de dificuldades na aprendizagem do que os nasais.

PALAVRAS-CHAVE:
Respiração bucal; Aprendizagem; Leitura; Escrita; Matemática

Introduction

Learning disorders may occur due to multifactorial reasons, among which are auditory information processing alterations,11. Pinheiro FH, Capellini SA. Desenvolvimento das habilidades auditivas de escolares com distúrbio de aprendizagem, antes e após treinamento auditivo, e suas implicações educacionais. Rev Psicopedag. 2009;26:231-41. Available from: http://pepsic.bvsalud.org/scielo.php?pid=S0103-4862009000200008&script=sciarttext [cited 10.06.15].
http://pepsic.bvsalud.org/scielo.php?pid...
and22. Wiemes GRM, KozlowskiL, Mocellin M, Hamerschmidt R, Schuch LH. Potencial evocado cognitivo e desordem de processa-mento auditivo em crianc¸as com distúrbios de leitura e escrita. Braz J Otorhinolaryngol. 2012;78:91-7, http://dx.doi.org/10.1590/S1808-86942012000300016 [cited 10.06.15].
https://doi.org/10.1590/S1808-8694201200...
attention deficit, interpersonal relationship difficulties, behavioral disorders, cognitive deficits, disadvantaged socioeconomic background,33. Figueiredo VLM, Quevedo L, Gomes G, Pappen L. Habilidades cognitivas de crianc¸as e adolescentes com distúrbio de apren-dizagem. Psico-USF. 2007;12:281-90. Available from: http://pepsic.bvsalud.org/scielo.php?pid=S1413-82712007000200016&script=sciarttext [cited 10.06.15].
http://pepsic.bvsalud.org/scielo.php?pid...
family history of learning difficulties and disabilities,44. Tabaquim MLM. Avaliação neuropsicológica nos distúrbios de aprendizagem. In: Ciasca SM, editor. Distúrbios de aprendizagem: proposta de avaliação interdisciplinar. São Paulo: Casa do Psicólogo; 2003. p. 91-111. as well as others, such as mouth breathing - which can compromise learning.55. Chedid KAK, Di Francesco RC, Junqueira PAS. A influência da respiração oral no processo de aprendizagem da leitura e escrita em crianc¸as pré-escolares. Rev Psicopedag. 2004;21:157-63. Available from: http://pepsic.bvsalud.org/pdf/psicoped/v21n65/v21n65a08.pdf [cited 10.06.15].
http://pepsic.bvsalud.org/pdf/psicoped/v...

When breathing is performed only through the mouth, it can be considered a pathological adaptation resulting from difficulty of breathing through the nose,66. Di Francesco RC. Consequências da respiração oral. In: Krakauer LH, Di Francesco RC, Marchesan IQ, editors. Conhecimento para atender bem a respiração oral. São José dos Campos: Pulso; 2003. p. 19-25. and it results in the inspiration of a drier, unfiltered air, at a colder or warmer temperature than the expected, which ultimately overwhelms the tonsils and the larynx and can cause chronic inflammation. If such pathological adaptation occurs over a long period, it can result in tonsillar hypertrophy and subsequently, varying degrees of upper airway obstruction. Thus, there will be resistance to gas flow, permanent increase in energy expenditure, and adaptations that are structural (high-arched palate and dental malocclusion) and functional (orofacial muscle flaccidity, dysphonia, and sleep apnea, for instance), that can impair the quality of sleep, mood, behavior, and school performance,77. Lee JH. O respirador bucal na visão da pediatria. In: Coelho-Ferraz MJP, editor. Respirador buccal: uma visão multidisciplinar. São Paulo: Lovise; 2005. p. 79-83. although there is no significant scientific evidence to support the association between the altered breathing pattern and learning difficulties.

Considering the high prevalence of mouth breathing in childhood88. De Paula MVQ, Leite ICG, Werneck RR. Prevalência de por-tadores da síndrome da respiração bucal na rede escolar do município de Juiz de Fora - MG. H U Rev. 2008;34:33-8. Avail-able from: Erro! A referência de hiperlink não é válida./ Erro! A referência de hiperlink não é válida. [cited 10.06.15]. and the possibility of its impact on learning, this study was designed in order to verify, through a systematic review of the literature, whether this breathing pattern influences children's learning process.

Methods

The methodological approach used in this review follows, including article search strategy and eligibility criteria, the data collection phase, and analysis. This systematic review was carried out following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.99. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336-41, http://dx.doi.org/10.1371/journal.pmed.1000097 [cited 15.07.15].
https://doi.org/10.1371/journal.pmed.100...

Search strategy and eligibility criteria

This systematic review study was conducted with no restrictions regarding the year and language of publication. The P.I.C.O strategy was used, considering schoolchildren who were mouth breathers aged 7-11 years (P = patient), assessed regarding the aspects related to learning (I = intervention) and compared with schoolchildren who were nasal breathers (C = intervention comparison or control), aiming at verifying the possibility of learning disability in those with altered breathing pattern (O = outcome), using the following guiding question: "Is the mouth-breathing child more likely to have learning disabilities when compared to nasal breathers?".

The study design is explained in Fig. 1, with the study eligibility criteria. For the studies considered preliminarily eligible, the full text was obtained and assessed in order to verify whether they met all the inclusion criteria. The following inclusion criteria were used: observational studies (controlled, cross-sectional, prospective, or retrospective longitudinal studies) on the subject, with schoolchildren aged between 7 and 11 years.

Figure 1
Search strategy flowchart and article selection.

The exclusion criteria were: ambiguous results, poor presentation of results, study duplication based on the database search, review studies, communications, case reports, scientific meeting abstracts, monographs, comments, or editorials. Studies regarding syndromic patients and those with intellectual disabilities were also excluded, as well as registries not directly related to the final outcome of this study (Fig. 1).

The keywords were selected in DeCS (VHL Health Sciences Descriptors) and MeSH (PubMed), in order to identify relevant studies in the PubMed, SciELO, LILACS, and Scopus electronic databases. The controlled descriptors were "learning" and "mouth breathing," "aprendizagem" and "respiração bucal." Boolean operators (OR and AND) were used for descriptor combination. This research was carried out on July 15th, 2015. The gray literature was identified by searching in Google Scholar, by consulting the first hundred records of each combination.

Assessment process validity and data extraction

After obtaining the list of the studies carried out with the chosen descriptors, the relevance test was applied and each study was carefully analyzed by two eligibility reviewers (not blinded to the authors and journals), who performed the survey independently and decided, by consensus, which studies would be selected. In case of divergence of results, a third reviewer was consulted to resolve the question regarding whether the study should be included, as suggested by the literature.1010. McDonald S, Crumley E, Eisinga A, Villanueva E. Search strategies to identify reports of randomized trials in Medline: protocol for a Cochrane review. Oxford: The Cochrane Library; 2006. Available from: http://www.researchgate.net/profile/ElmerVillanueva/publication/230285759SearchstrategiestoidentifyreportsofrandomizedtrialsinMEDLINE/links/02bfe50eb83296203c000000.pdf [cited 10.06.15].

Initially, article titles, descriptors, and abstracts were identified; the first research filter was applied to select them. Subsequently, based on the obtained results, the second filter was applied by reading the study introduction and conclusion. If the article was considered eligible, the article was read in full and, thus, the third filter was applied.

In this preliminary phase, the eligible texts were assessed for their methodological strength, representing the fourth and final relevance test filter used. The methodology qualitative score protocol, modified from Pithon et al., was used for this evaluation1111. Pithon MM, Sant'Anna LIDA, Baião FCS, Santos RL, Coqueiro RC, Maia LC. Assessment of the effectiveness of mouthwashes in reducing cariogenic biofilm in orthodontic patients: a sys-tematic review. J Dent. 2015;43:297-308, http://dx.doi.org/10.1016/j.jdent.2014.12.010 [cited 01.07.15].
https://doi.org/10.1016/j.jdent.2014.12....
; it allows a maximum score of 13 points (Table 1). At this time, the review was blinded to the authors and journals, to avoid any selection bias and possible conflicts of interest.

Table 1
Protocol for the methodology qualitative score, modified from Pithon et al.,11 with a maximum score of thirteen points.a

It should be noted that the adaptation occurred only when establishing the number of subjects that should participate in the studies (n), as a basis for the sample size calculation related to the study subject, using an "n" of 147 subjects based on the study by Menezes et al., 1212. Menezes VA, Leal RB, Pessoa RS, Pontes RMES. Prevalência e fatores associados à respiração oral em escolares par-ticipantes do projeto Santo Amaro-Recife, 2005. Rev Bras Otorrinolaringol. 2006;72:394-9, http://dx.doi.org/10.1590/S0034-72992006000300017 [cited 01.07.15].
https://doi.org/10.1590/S0034-7299200600...
who used this number as the minimum one for performing a study with mouth breathers between the ages between 8 and 10 years old, i.e., within the mean age of the studies included in this research.

The studies were synthesized and distributed in a chart, containing the following information: year of publication, type of study, diagnosis and tools for data collection, sample characterization, main findings, and conclusion of the study, reported in the results session.

Data analysis

Data analysis was performed qualitatively, as the methods used in the studies were heterogeneous.

Results

Research strategy and methodological assessment

Using the keywords "respiração bucal" AND "aprendizagem," seven articles from the LILACS database were obtained, 2440 articles from the Google Scholar database (of these, the first hundred were analyzed), six articles from Scopus, and one from SciELO. Using the keywords "mouth breathing" AND "learning," eight articles from LILACS, 147,000 from Google Scholar (of these, the first hundred were analyzed), five from SciELO, and 30 from the PubMed database were obtained. Thus, the initial sample comprised 357 articles.

After applying the filters designed in the method, 43 articles were excluded after the first filter was applied due to duplication in the databases and 304 for addressing other subjects such as prevalence, behavioral assessment, posture, hearing skills, malocclusion, adult studies, and studies in animals and treatment (233 after the second filter and 71 after the third), as shown in Fig. 1. Thus, the sample consisted of ten articles.

As for the methodological strength, all (100%) of the included studies1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
,2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
showed moderate methodological strength (Table 2).

Table 2
Scores obtained after applying the Methodology Qualitative Score Protocol, adapted from Pithon et al.11

Characteristics of the included studies

Of the ten included studies, half (50%) used a control group.1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
The studies were published between 2003 and 2015, with peak concentrations in 2003 (two studies, 20%)1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
and1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
and in 2013 (two studies, 20%).2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
The use of sample size calculation was achieved in one study (10%).2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
Table 3 shows the main characteristics of the selected studies.

Table 3
Summary of the ten articles that comprised the study sample on the subject "mouth breathing and learning".

The procedures used for the assessment of the participants were: analysis of records/files: two (20%)1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
and2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
; interview: four (40%)1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
; questionnaires: six (60%)1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
and2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
; clinical evaluation or observation: six (60%)1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
; otorhinolaryngological assessment disclosing mouth breathing: five (50%),1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
specific tests: six (60%)1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
; and pure tone audiometry: two (20%).1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...

Regarding the data collection tools, the use of validated protocols was attained in two studies1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
(20% of the sample) and Uema et al.1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
used, among several tests, a grapheme recognition task, through the letter cancelation test, while Kuroishi et al.2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
used the Academic Performance Test, in partial form.

Mouth breathers showed greater difficulty in solving mathematical operations than nasal breathers.1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
However, some researchers2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
found no difficulty regarding mathematical operations in their study.

Reading comprehension was considered worse in the mouth breathers,2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
as well as writing.2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...

Overall, eight studies (80%)1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
reported learning disabilities in mouth breathers, with three (30%) related to tonsillar or inferior turbinate hypertrophy,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
three (30%) due to sleep-disordered breathing,1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
and1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
two (20%) to nasal obstruction2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
and allergic rhinitis (20%),1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
and1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
one (10%) associated with attention deficit hyperactivity disorder (ADHD),1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
one (10%) due to asthma,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
and one (10%) to septal deviation.2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
Of the studies that found no association between mouth breathing and learning disability (n = 2; 20%), 1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
and2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
one was related to nasal obstruction1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
and another2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
did not divide the groups between mouth and nasal breathers, classifying the participants as having respiratory impairment features, without specifying the cause.

Discussion

School failures occur for different reasons; according to the last census, conducted by Instituto Nacional de Estudos e Pesquisas Educacionais Anísio Teixeira2323. Brasil. Ministério da Educação. Instituto Nacional de Estudos e Pesquisas Educacionais Anísio Teixeira. Taxa de aprovação - 2013. Brasília: INEP; 2013. (INEP, BRASIL, 2013), in 2013, 6.1% of students fail to pass on to the following grade, with one of the reasons being the presence of learning disabilities. Literature has described several factors for its emergence, such as hearing,11. Pinheiro FH, Capellini SA. Desenvolvimento das habilidades auditivas de escolares com distúrbio de aprendizagem, antes e após treinamento auditivo, e suas implicações educacionais. Rev Psicopedag. 2009;26:231-41. Available from: http://pepsic.bvsalud.org/scielo.php?pid=S0103-4862009000200008&script=sciarttext [cited 10.06.15].
http://pepsic.bvsalud.org/scielo.php?pid...
and22. Wiemes GRM, KozlowskiL, Mocellin M, Hamerschmidt R, Schuch LH. Potencial evocado cognitivo e desordem de processa-mento auditivo em crianc¸as com distúrbios de leitura e escrita. Braz J Otorhinolaryngol. 2012;78:91-7, http://dx.doi.org/10.1590/S1808-86942012000300016 [cited 10.06.15].
https://doi.org/10.1590/S1808-8694201200...
attention, interpersonal relationships, behavior and cognition disabilities, socioeconomic status,33. Figueiredo VLM, Quevedo L, Gomes G, Pappen L. Habilidades cognitivas de crianc¸as e adolescentes com distúrbio de apren-dizagem. Psico-USF. 2007;12:281-90. Available from: http://pepsic.bvsalud.org/scielo.php?pid=S1413-82712007000200016&script=sciarttext [cited 10.06.15].
http://pepsic.bvsalud.org/scielo.php?pid...
family history,44. Tabaquim MLM. Avaliação neuropsicológica nos distúrbios de aprendizagem. In: Ciasca SM, editor. Distúrbios de aprendizagem: proposta de avaliação interdisciplinar. São Paulo: Casa do Psicólogo; 2003. p. 91-111. as well as mouth breathing.55. Chedid KAK, Di Francesco RC, Junqueira PAS. A influência da respiração oral no processo de aprendizagem da leitura e escrita em crianc¸as pré-escolares. Rev Psicopedag. 2004;21:157-63. Available from: http://pepsic.bvsalud.org/pdf/psicoped/v21n65/v21n65a08.pdf [cited 10.06.15].
http://pepsic.bvsalud.org/pdf/psicoped/v...

This respiratory pattern is considered a pathological adaptation66. Di Francesco RC. Consequências da respiração oral. In: Krakauer LH, Di Francesco RC, Marchesan IQ, editors. Conhecimento para atender bem a respiração oral. São José dos Campos: Pulso; 2003. p. 19-25., which can affect the quality of sleep, mood, behavior, and school performance77. Lee JH. O respirador bucal na visão da pediatria. In: Coelho-Ferraz MJP, editor. Respirador buccal: uma visão multidisciplinar. São Paulo: Lovise; 2005. p. 79-83.; however, there are few studies that show such interrelation. Moreover, the prevalence of mouth breathing is considered high in childhood88. De Paula MVQ, Leite ICG, Werneck RR. Prevalência de por-tadores da síndrome da respiração bucal na rede escolar do município de Juiz de Fora - MG. H U Rev. 2008;34:33-8. Avail-able from: Erro! A referência de hiperlink não é válida./ Erro! A referência de hiperlink não é válida. [cited 10.06.15]. and, thus, the present systematic review was carried out.

As shown by the sample composition, little has been investigated on the subject (2.8% of 357 studies), demonstrating the need for further studies in this area.

Half of the studies in the sample used a control group,1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
and it is noteworthy that Kajihara and Nishimura1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
compared their results with the control group of another study, although they belonged to the same research group. Thus, it is suggested that studies on the subject with control groups be performed to attain greater result reliability. Additionally, for evidence-based practice, that is, for a professional decision to be made based on the obtained scientific results, according to Muir Gray2424. Muir Gray JA. Evidence-based healthcare: how to make health policy and management decision. Edinburgh: Churchill Living- stone; 1997. it is ideal when such studies show high evidence strength, which are usually controlled and randomized studies; such randomized controlled studies were not identified in our sample.

As for the nosological diagnosis confirming the etiology of mouth breathing, half of the researchers we studied1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
submitted their sample groups to otorhinolaryngological assessment, demonstrating obstructive mouth breathing, although with different etiologies. It should also be noted that Abreu et al.1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
stated that the study group underwent medical assessment, but did not mention which specialty performed such assessment or what procedures were performed.

Perilo et al.2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
sent a Questionnaire for Assessment of Respiratory Characteristics, consisting of 22 closed questions with yes/no answers to the parents/guardians. However, the authors' study, due to the absence of the otorhinolaryngological evaluation to confirm the etiology of the altered breathing pattern, did not mention the number of affirmative questions that should have been marked in order to consider the subject a possible mouth breather. Such bias was minimized by observing labial sealing for 5 min, observed by two evaluators during a distractor task. Thus, they did not divide the sample into mouth and nasal breathers, analyzing the respiratory characteristics of the sample and comparing them with the cognitive-linguistic skills.

The assessed studies that comprised the sample used non-probabilistic samples, chosen intentionally or by convenience, that can result in bias in data interpretation as it depends on the researcher's appraisal. Despite the abovementioned fact, Kuroishi et al.2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
carried out a sample calculation study to determine the sample size that would provide a more representative population and more accurate results.2525. Normando D, Almeida MADO, Quintão CCA. Análise do emprego do cálculo amostral e do erro do método em pesquisas científicas publicadas na literatura ortodôntica nacional e inter-nacional. Dental Press J Orthod. 2011;16:33e1-9. Available from: http://www.scielo.br/pdf/dpjo/v16n6/a06v16n6.pdf [cited 10.06.15].
http://www.scielo.br/pdf/dpjo/v16n6/a06v...

Although school failure is a complex analysis variable since other aspects can influence its occurrence, it is inferred that students with learning disorders have a greater chance for failure. Therefore, it would be worthwhile for studies to show whether the sample consisted of students that did or did not fail school. The research by Fensterseifer et al.2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
established a minimum of two years, and the study by Vera et al.1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
reported complaints (by most of the family members of mouth breathers) of learning difficulties, while 39% had failed (from one to three times), more often in elementary school. Other studies1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
did not mention school failure, and in the study by Abreu et al.,1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
the students were required to be at the appropriate school year for age, i.e., those students who failed were not included in the study, which may be considered a weakness.

Another important factor for analysis is the place where the selected studioes occurred and the time period during which the studies were performed, since climate change must be taken into account.2626. Ribeiro WC, Impactos das mudanc¸as climáticas em cidades no brasil. Parcerias Estratégicas. 2008;27:297-321. Avail-able from: http://www.cetesb.sp.gov.br/userfiles/file/mudancasclimaticas/proclima/file/publicacoes/metropoles/ribeiroimpactos.pdf [cited 10.06.15].
http://www.cetesb.sp.gov.br/userfiles/fi...
Most studies in our sample were carried out by Brazilian researchers,1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
,2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
which justifies our interest in the subject. Only four studies (40%)1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
and2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
indicated the period (in months or years) during which the sample selection was obtained.

Researchers2727. Goncalves FLT, Coelho MDSZS. Variação da morbidade de doenc¸as respiratórias em função da variação da temperatura entre os meses de abril e maio em São Paulo. Ciênc Nat. 2010;32:103-18. Available from: http://cascavel.ufsm.br/revistas/ojs2.2.2/index.php/cienciaenatura/article/viewFile/9500/5649 [cited 10.06.15].
http://cascavel.ufsm.br/revistas/ojs2.2....
have emphasized the impact of climate change on upper airway (UA) disorders in children younger than 13 years in the metropolitan region of São Paulo, in the months that correspond to the start of winter. They added that the peak of respiratory disease morbidity occurs in May, possibly due to thermoregulation problems in subjects adapted to the milder climate/weather of April, explaining that people with thermoregulation problems are more sensitive to respiratory and cardiovascular diseases, especially the pediatric population.

There is an increase in hospital consultations2727. Goncalves FLT, Coelho MDSZS. Variação da morbidade de doenc¸as respiratórias em função da variação da temperatura entre os meses de abril e maio em São Paulo. Ciênc Nat. 2010;32:103-18. Available from: http://cascavel.ufsm.br/revistas/ojs2.2.2/index.php/cienciaenatura/article/viewFile/9500/5649 [cited 10.06.15].
http://cascavel.ufsm.br/revistas/ojs2.2....
during this period and, consequently, a higher probability of school absenteeism, which can impair academic performance, depending on the chronicity of the condition.

In Brazil, respiratory diseases accounted for 5% of the years of life lost due to premature death,2828. Schramm JMA, Oliveira AF, Costa Leite I, Valente JG, Gadelha ÂMJ, Portela MC, et al. Transição epidemiológica e o estudo de carga de doenc¸a no Brasil. Ciênc Saúde Coletiva. 2004;9:897-908, http://dx.doi.org/10.1590/S1413-81232004000400011 [cited 10.06.15].
https://doi.org/10.1590/S1413-8123200400...
emphasizing the importance of public health measures to reduce this percentage.

Another analysis variable concerns the impact of urbanization on the living conditions and health of the Brazilian population. It can be observed that of the ten selected studies, half were performed in capital cities1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1717. Uema SFH, Pignatari SSN, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L. Avaliação da função cognitiva da aprendizagem em crianc¸as com distúrbios obstrutivos do sono. Rev Bras Otorrinolaringol. 2007;73:315-20, http://dx.doi.org/10.1590/S0034-72992007000300005 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200700...
,2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
and2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
and the other half1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
,1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
in well-developed cities. In large Brazilian cities, according to Maricato,2929. Maricato E. Urbanismo na periferia do mundo globalizado: metrópoles brasileiras. São Paulo Perspect. 2000;14:21-33, http://dx.doi.org/10.1590/S0102-88392000000400004 [cited 10.06.15].
https://doi.org/10.1590/S0102-8839200000...
there has been an increase in ecological social inequality, a situation in which there is an uncontrolled growth of cities, with population increase in the outskirt regions. Usually, the individuals living in the outskirts of Brazilian cities have a low socioeconomic status (as demonstrated by research)3030. Carvalho MP. Quem são os meninos que fracassam na escola? Cad Pesqui. 2004;34:11-40. Available from: http://www.scielo.br/pdf/cp/v34n121/a02n121.pdf [cited 10.06.15].
http://www.scielo.br/pdf/cp/v34n121/a02n...
and, thus, are more vulnerable to factors that can compromise quality of life and health.

In addition to the aforementioned facts, it can be observed that school failure is higher in boys than in girls, predominantly among African-descendants and/or those from low-income families.3030. Carvalho MP. Quem são os meninos que fracassam na escola? Cad Pesqui. 2004;34:11-40. Available from: http://www.scielo.br/pdf/cp/v34n121/a02n121.pdf [cited 10.06.15].
http://www.scielo.br/pdf/cp/v34n121/a02n...
This study sample was mostly comprised of boys, confirming what literature has shown, both with respect to school failure and the possibility of the presence of a comorbidity factor, such as ADHD.1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...

Thus, it is possible to conclude that the understanding of the determinants of learning and its failure are multifactorial and complex; moreover, there are few validated tools to investigate learning disorders, and that creates difficulty when comparing the procedures. Only two studies2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
used validated tools, another2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
used a published protocol that was adapted to Brazilian students, and another1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
applied an evaluation test that was used in a different non-validated study; the remaining studies1313. Abreu ACB, Morales DA, Ballo MBJF. A respiração oral influen-cia o rendimento escolar. Rev Cefac. 2003;5:69-73. Available from: http://www.cefac.br/revista/revista51/Artigo%2011.pdf [cited 15.07.15].
http://www.cefac.br/revista/revista51/Ar...
,1414. Goodwin JL, Babar SI, Kaemingk KL, Rosen GM, Morgan WJ, Sherrill DL, et al. Symptoms related to sleep-disordered breath-ing in white and Hispanic children: the Tucson Children's Assessment of Sleep Apnea Study. Chest J. 2003;124:196-203, http://dx.doi.org/10.1378/chest.124.1.196 [cited 15.07.15].
https://doi.org/10.1378/chest.124.1.196...
,1515. Di Francesco RC, Passerotii G, Paulucci B, Miniti A. Respiração oral na crianc¸a: repercussões diferentes de acordo com o diag-nóstico. Rev Bras Otorrinolaringol. 2004;70:665-70, http://dx.doi.org/10.1590/S0034-72992004000500014 [cited 15.07.15].
https://doi.org/10.1590/S0034-7299200400...
,1616. Vera CFD, Conde GES, Wajnsztejn R, Nemr K. Transtornos de aprendizagem e presenc¸a de respiração oral em indivíduos com diagnóstico de transtornos de déficit de atenção/hiperatividade (TDAH). Rev Cefac. 2006;8:441-55, http://dx.doi.org/10.1590/S1516-18462006000400005 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846200600...
,1818. Petry C, Pereira MU, Pitrez P, Jones MH, Stein RT. Prevalência de sintomas de distúrbios respiratórios do sono em esco-lares brasileiros. J Pediatr. 2008;84:123-9, http://dx.doi.org/10.1590/S0021 [cited 15.07.15].
https://doi.org/10.1590/S0021...
and2020. Fensterseifer GS, Carpes O, Weckx LLM, Martha VF. Respiração bucal em crianc¸as com dificuldade de aprendizado. Braz J Otorhinolaryngol. 2013;79:620-4, http://dx.doi.org/10.5935/1808-8694.20130111 [cited 15.07.15].
https://doi.org/10.5935/1808-8694.201301...
did not use assessment protocols with the students, but instead used school failure records or questionnaires applied to family members or teachers, increasing the analysis bias in such studies.

The School Achievement Test (Teste de Desempenho Escolar - TDE), developed by Lilian Stein,3131. Stein LM. TDE - teste de desempenho escolar: manual para aplicação e interpretação. São Paulo: Casa do Psicólogo; 2011. was partially used in one study (10%).2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
The study compared the experimental group with a control group and the subjects were matched for age and educational level, with part of the sample showing mouth breathing. It was verified that such students had lower school performance than the control group in reading comprehension, arithmetic, and working memory tasks (except for numbers).

Regarding the assessment of mathematical skills, two1919. Kajihara OT, Nishimura CM. Respiração oral: um fator que pode prejudicar a aprendizagem da matemática. Rev Série-Estudos. 2012;33:101-18. Available from: http://www.serie-estudos.ucdb.br/index.php/serie-estudos/article/viewFile/78/173 [cited 15.07.15].
http://www.serie-estudos.ucdb.br/index.p...
and2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
of the studies that applied tests found results indicating difficulties in mouth breathers, while the other one did not.2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...
Reading comprehension was considered worse in mouth breathers,2222. Kuroishi RCS, Garcia RB, Valra FCP, Anselmo-Lima WT, Fukuda MTH. Déficits de memória operacional, compreensão de leitura e habilidades aritméticas em crianc¸as com síndrome da respiração oral: estudo transversal analítico. São Paulo Med J. 2015;133:78-83, http://dx.doi.org/10.1590/1516-3180.2013.7630011 [cited 15.07.15].
https://doi.org/10.1590/1516-3180.2013.7...
as well as writing skills in subjects with respiratory disorder characteristics, when compared with those without such disorders.2121. Perilo TVC, Freitas CS, Cardoso NC, Motta AR, Alves LM. Habil-idades cognitivo-linguísticas e sua relação com características respiratórias. Rev Cefac. 2013;15:579-91, http://dx.doi.org/10.1590/S1516-18462012005000065 [cited 15.07.15].
https://doi.org/10.1590/S1516-1846201200...

Therefore, in general, most researchers reported learning difficulties in subjects with abnormal breathing pattern.

Thus, studies involving mouth breathing and learning require further investigation, since the number of studies for analysis was small and showed diverse evaluation procedures. Controlled, interdisciplinary studies, with the inclusion of standardized assessments, using validated tools and uniform sample groups must be performed so that a systematic meta-analysis review study can be carried out and, thus, more scientific evidence will become available, both for clinical practice and for the implementation of public health and education policies.

Conclusions

There is evidence that the breathing pattern can influence the learning process. This systematic review showed that mouth breathers are more likely to have learning difficulties than nasal breathers. Further studies are needed in order to increase the scientific evidence for clinical practice, and for the implementation of public health and education policies.

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  • Please cite this article as: Ribeiro GCA, dos Santos ID, Santos ACN, Paranhos LR, César CPHAR. Influence of the breathing pattern on the learning process: a systematic review of literature. Braz J Otorhinolaryngol. 2016;82:466-78.

Publication Dates

  • Publication in this collection
    Jul-Aug 2016

History

  • Received
    19 June 2015
  • Accepted
    07 Aug 2015
Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-Facial. Sede da Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico Facial, Av. Indianópolia, 1287, 04063-002 São Paulo/SP Brasil, Tel.: (0xx11) 5053-7500, Fax: (0xx11) 5053-7512 - São Paulo - SP - Brazil
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