Braz. j. . vol.82 número4

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BrazJOtorhinolaryngol.2016;82(4):466---478

www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

REVIEW

ARTICLE

Influence

of

the

breathing

pattern

on

the

learning

process:

a

systematic

review

of

literature

夽

Genef

Caroline

Andrade

Ribeiro

a

_,

_Isadora

_Diniz

_dos

_Santos

a

_,

Ana

Claudia

Nascimento

Santos

a

_,

_Luiz

_Renato

_Paranhos

b

_,

Carla

Patrícia

Hernandez

Alves

Ribeiro

César

a,∗

a_Department_of_Speech_Therapy_and_Audiology,_Universidade_Federal_de_Sergipe_(UFS),_Campus_Prof._Antônio_Garcia_Filho,

Lagarto,SE,Brazil

b_Department_of_Odontology,_Universidade_Federal_de_Sergipe_(UFS),_Campus_Prof._Antônio_Garcia_Filho,_Lagarto,_SE,_Brazil

Received19June2015;accepted7August2015 Availableonline7January2016

KEYWORDS

Mouthbreathing; Learning; Reading; Writing; Mathematics

Abstract

Introduction:Mouthbreathingleadstonegativeconsequencesonqualityoflife,especiallyin school-agechildren.

Objective:Todeterminewhetherthebreathingpatterninfluenceschildren’slearningprocess.

Methods:ThissystematicreviewwascarriedoutaccordingtothePreferredReportingItemsfor SystematicReviewsandMeta-Analyses(PRISMA)instructions,withnorestrictionsregardingthe yearofpublicationandlanguage,createdbasedontheclinicalquestionformulationaccording totheProblem/Patient/Population,Intervention/Indicator,Comparison,Outcome(PICO) strat-egy:‘‘Isthemouth-breathingchildmorelikelytohavelearningdisabilitieswhencomparedto nasal breathers?’’intheSciELO, PubMed,LILACS, andScopus electronicdatabases. Google Scholarwas usedto searchthe grayliterature. The keywords ‘‘learning,’’ ‘‘mouth breath-ing,’’andtheirequivalenttermsinPortuguesewereusedinanintegratedmanner.Thestudies includedinthereview wereobservational,conducted withschoolchildrenaged 7---11years. Afterwards,thestudieswereevaluatedregardingtheirmethodologicalquality.Theresearch wasperformedbytwoeligiblereviewers.

Results:Atotalof357recordswereobtained,ofwhich43recordswereduplicate.After apply-ingtheeligibilitycriteria,tenarticleswereincludedintheresearchscope.Halfofthestudies usedacontrolgroupandotorhinolaryngologicalassessment,whereasaminorityusedvalidated (20%)andsamplecalculationprotocols(10%).Theevaluationprocedureswerevaried.Overall, 80%ofthearticlesshowedahigherincidenceoflearningdisabilitiesamongmouthbreathers.

夽 _Please_cite_this_article_as:_Ribeiro_GCA,_dos_Santos_ID,_Santos_ACN,_Paranhos_LR,_César_CPHAR._Influence_of_the_breathing_pattern_on_the

learningprocess:asystematicreviewofliterature.BrazJOtorhinolaryngol.2016;82:466---78.

∗_{Corresponding}_author.

E-mail:[email protected](C.P.H.A.R.César).

http://dx.doi.org/10.1016/j.bjorl.2015.08.026

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Oralbreathingandlearning:literaturereview 467

Conclusion: Thissystematicreviewhasshownthatmouthbreathersaremorelikelytohave learningdifficultiesthannasalbreathers.

© 2015 Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/).

PALAVRAS-CHAVE

Respirac¸ãobucal; Aprendizagem; Leitura; Escrita; Matemática

Ainfluênciadomodorespiratórionoprocessodeaprendizagem:umarevisão sistemáticadaliteratura

Resumo

Introduc¸ão: Arespirac¸ãooraltrazconsequênciasnegativasparaaqualidadedevidadas pes-soas,principalmenteparaescolares.

Objetivo: Verificarseomodorespiratórioinfluencianoprocessodeaprendizageminfantil.

Método: Esta revisão sistemática foi realizada seguindo as instruções PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses), sem restrição quanto ao ano depublicaçãoeidioma,elaboradaapartirdaformulaçãodequestãoclínicaelaboradapela estratégiaP.I.C.O.:‘‘Acriançarespiradoraoraltemmaischancesdeapresentardificuldades

de aprendizagemquandocomparada àrespiradoranasal?’’, nasbasesde dadoseletrônicas

SciELO, PubMed,LILACSeScopus.FoiutilizadooGoogleScholarparapesquisadaliteratura cinza.Aspalavras-chave‘‘aprendizagem’’,‘‘respirac¸ãobucal’’,‘‘learning’’e‘‘mouth breath-ing’’foramutilizadasdeformaintegrada.Osestudosincluídosforamobservacionais,realizados comescolaresentreseteeonzeanos.Emseguida,osestudosforamavaliadosquantoàsua qualidademetodológica.Todaapesquisafoirealizadapordoisrevisoresdeelegibilidade.

Resultados: Foramobtidos357registros,sendo314blindados(43registrosemduplicidade). Apósos critérios de elegibilidade,dez artigosintegraramo escopodesta pesquisa. Metade dos estudosusougrupo controlee fezusodeavaliac¸ãootorrinolaringológica,aminoria fez usodeprotocolosvalidados(20%)edecálculoamostral(10%).Osprocedimentosdeavaliac¸ão foramvariados.Deformageral,80%dosartigosevidenciarammaiorocorrênciadedistúrbiode aprendizagememrespiradoresorais.

Conclusão:Estarevisãosistemáticademonstrouqueindivíduoscomrespirac¸ãooralapresentam maiortendênciadedificuldadesnaaprendizagemdoqueosnasais.

© 2015 Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-Facial. Publicado por Elsevier Editora Ltda. Este é um artigo Open Access sob uma licença CC BY (http:// creativecommons.org/licenses/by/4.0/).

Introduction

Learning disorders may occur due to multifactorial rea-sons, among which are auditory information processing alterations,1,2 _attention _deficit, _{interpersonal} _relationship

difficulties, behavioral disorders, cognitive deficits, dis-advantaged socioeconomic background,3 _family _history _of

learningdifficultiesanddisabilities,4_as_well_as_others,_such

asmouthbreathing---whichcancompromiselearning.5

When breathingis performed only throughthe mouth, it can be considered a pathological adaptation resulting fromdifficultyofbreathingthroughthenose,6_and_it_results

in the inspiration of adrier, unfiltered air, at acolder or warmertemperature thantheexpected,which ultimately overwhelmsthetonsilsandthelarynxandcancausechronic inflammation.Ifsuchpathologicaladaptationoccursovera longperiod,itcanresultintonsillarhypertrophyand subse-quently,varyingdegreesofupperairwayobstruction.Thus, there will be resistance to gas flow, permanent increase inenergyexpenditure,andadaptationsthatarestructural

(high-archedpalateanddentalmalocclusion)andfunctional (orofacialmuscleflaccidity,dysphonia,andsleepapnea,for instance),thatcanimpairthequalityofsleep,mood, behav-ior,andschoolperformance,7_although_there_is_no_significant

scientificevidencetosupporttheassociationbetweenthe alteredbreathingpatternandlearningdifficulties.

Consideringthe high prevalence of mouth breathingin childhood8_and_the_possibility_of_its_impact_on_learning,_this

study was designed in order toverify, through a system-aticreviewoftheliterature,whetherthisbreathingpattern influenceschildren’slearningprocess.

Methods

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468 RibeiroGCAetal.

Searchstrategyandeligibilitycriteria

This systematic review study was conducted with no restrictions regarding the year and language of pub-lication. The P.I.C.O strategy was used, considering schoolchildrenwhoweremouthbreathersaged7---11years (P=patient), assessed regarding the aspects related to learning (I=intervention) and compared with schoolchil-drenwhowerenasalbreathers(C=interventioncomparison or control), aiming at verifying the possibility of learn-ing disability in those with altered breathing pattern (O=outcome),usingthefollowingguidingquestion:‘‘Isthe mouth-breathingchildmorelikelytohavelearning disabili-tieswhencomparedtonasalbreathers?’’.

The study designis explainedin Fig.1, withthestudy eligibilitycriteria.Forthestudiesconsideredpreliminarily eligible,thefulltextwasobtainedandassessedinorderto verifywhethertheymetalltheinclusioncriteria.The fol-lowing inclusion criteriawere used: observational studies (controlled, cross-sectional, prospective, or retrospective

longitudinal studies) on the subject, with schoolchildren agedbetween7and11years.

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, com-ments,or editorials.Studies regardingsyndromic patients andthosewithintellectualdisabilitieswerealsoexcluded, aswellasregistriesnotdirectlyrelatedtothefinaloutcome ofthisstudy(Fig.1).

The keywords were selected in DeCS (VHL Health Sci-encesDescriptors)andMeSH(PubMed),inordertoidentify relevant studies in the PubMed,SciELO, LILACS, and Sco-pus electronicdatabases.The controlleddescriptorswere ‘‘learning’’and‘‘mouthbreathing,’’‘‘aprendizagem’’and ‘‘respirac¸ãobucal.’’Booleanoperators(ORandAND)were usedfordescriptorcombination.Thisresearchwascarried outonJuly15th,2015.Thegrayliteraturewasidentifiedby searchinginGoogleScholar,byconsultingthefirsthundred recordsofeachcombination.

Data source SciELO, LILACS, PubMed, Scopus and Google Scholar

Eligibility criteria

Inclusion criteria: observational studies on the subject, with children between 7 and 11 years old as the target

and year publication the

for limits No population. language.

of presence results, of ambiguity criteria:

Exclusion

systematic error inthe study, insufficient presentation studies, review

duplicity, study

results, of

and reports, case editorials, communications,

monographs.

Study selection and identification

of consisted which

filter, first the applying After

reading the titles, descriptors, and abstracts, 357 articles were selected (of these, 43 articles were excluded due to duplication in databases);

the reading of consisted applied filter second The

introduction and conclusion of314 articles,of which 81 articles were selected and 233 were excluded;

consisted filter

applied third

The full of reading the

texts and thus, ten articles were selected (three articles from LILACS, one from PubMed, two from SciELO, two from Google scholar, and none from Scopus) and 71 were excluded;

applied filter consisted in reading the ten The fourth

articles, interpreting and analyzing them regarding their methodological strength.

Qualitative analysis

The ten eligible studies were analyzed according to the protocol for methodology qualitative score, modified fromPithonetal.11

METHOD

RELEVANCE TEST

Research question

‘‘Is the mouth-breathing child more likely to have nasal to compared when

disabilities learning

breathers?’’

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Assessmentprocessvalidityanddataextraction

Afterobtainingthelistofthestudies carriedoutwiththe chosendescriptors,therelevancetestwasappliedandeach studywascarefullyanalyzedbytwoeligibilityreviewers(not blindedtotheauthorsandjournals),whoperformedthe sur-veyindependentlyanddecided,byconsensus,whichstudies wouldbeselected.Incaseofdivergenceofresults,athird reviewer wasconsulted to resolve thequestion regarding whetherthestudyshouldbeincluded,assuggestedbythe literature.10

Initially, article titles, descriptors,and abstracts were identified; the first research filter was applied to select them.Subsequently,basedontheobtainedresults,the sec-ondfilterwasappliedbyreadingthestudyintroductionand conclusion.Ifthearticlewasconsideredeligible,thearticle wasreadinfulland,thus,thethirdfilterwasapplied.

Inthispreliminaryphase,theeligibletextswereassessed for theirmethodologicalstrength,representingthefourth andfinalrelevancetestfilterused.Themethodology quali-tativescoreprotocol,modifiedfromPithonetal.,wasused forthisevaluation11_;_it_allows_a_maximum_score_of₁₃_points

(Table1).Atthistime,thereviewwasblindedtotheauthors andjournals,toavoidanyselectionbiasandpossible con-flictsofinterest.

It should be noted that the adaptation occurred only whenestablishingthenumberofsubjectsthatshould par-ticipate in the studies (n), asa basis for the sample size calculation relatedtothe study subject, usingan ‘‘n’’of 147subjects basedonthestudyby Menezesetal.,12 _who

usedthisnumberastheminimumoneforperformingastudy

withmouthbreathersbetweentheagesbetween8and10 yearsold,i.e.,withinthemeanageofthestudiesincluded inthisresearch.

Thestudiesweresynthesizedanddistributedinachart, containingthe following information: year of publication, typeofstudy,diagnosisandtoolsfordatacollection,sample characterization,mainfindings,andconclusionofthestudy, reportedintheresultssession.

Dataanalysis

Dataanalysiswasperformedqualitatively,asthemethods usedinthestudieswereheterogeneous.

Results

Researchstrategyandmethodologicalassessment

Using the keywords ‘‘respirac¸ão bucal’’ AND ‘‘aprendizagem,’’sevenarticlesfromtheLILACSdatabase were obtained, 2440 articles from the Google Scholar database (of these,the first hundredwere analyzed), six articlesfromScopus,andonefromSciELO.Usingthe key-words ‘‘mouthbreathing’’ AND‘‘learning,’’eightarticles fromLILACS, 147,000 from Google Scholar (of these, the first hundred were analyzed), five from SciELO, and 30 fromthePubMeddatabasewereobtained.Thus,theinitial samplecomprised357articles.

Afterapplyingthefiltersdesignedinthemethod,43 arti-cleswereexcludedafterthefirstfilterwasapplieddueto

Table1 Protocolfor themethodology qualitativescore,modifiedfrom Pithonetal.,11 _with_a_maximum _score_of_thirteen points.a

1.Studycharacterization(maximumscore:nine)

A.Adequatedescriptionofthepopulation(maximumscore:two)

Analyzeditems:age,gender,andpatientstatus: Twopointswhenallitemshavebeenachieved; Onepointwhentwoitemshavebeenachieved; Zeropointswhenoneornoitemhasbeenachieved.

B.Descriptionoftheselectioncriteria(maximumscore:one)b

C.Samplesize(maximumscore:two)

Analyzeditem:numberofparticipants:

Twopointswhenthesamplewasequaltoorhigherthan147participants; Onepointwhenthesamplewasbetween117and147participants; Zeropointswhentherewerelessthan117participants.

D.Comparisonwithcontrolgroup(maximumscore:one)b

E.Statedrandomization(maximumscore:one)b

F.Descriptionoftheevaluationcriteriaofthereading,writing,andmathematicsassessment(maximumscore:one)b

G.Descriptionofbreathingassessment(maximumscore:one)b

2.Descriptionofthestudymeasurements(maximumscore:two)

H.Appropriatemethodinrelationtothearticleobjective(maximumscore:one)b

Blindstudyforexaminersandstatistics(maximumscore:one)b 3.Statisticalanalysis(maximumscore:two)

J.Appropriatestatisticaltest(maximumscore:one)b

K.p-Valuepresentation(maximumscore:one)b

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470 RibeiroGCAetal.

duplicationinthe databasesand304 for addressing other subjects such as prevalence, behavioral assessment, pos-ture,hearingskills,malocclusion,adultstudies,andstudies inanimals andtreatment (233after thesecond filterand 71 afterthe third), as shown in Fig.1. Thus, the sample consistedoftenarticles.

As for the methodological strength, all (100%) of theincluded studies13---22 _showed_moderate_{methodological}

strength(Table2).

Characteristicsoftheincludedstudies

Of the ten included studies, half (50%) used a control group.13,17,19,20,22_The_studies_were_published_between₂₀₀₃

and2015, withpeakconcentrations in 2003 (two studies, 20%)13,14 _and _in ₂₀₁₃ _(two _studies, _20%).20,21 _The _use _of

samplesizecalculationwasachievedinonestudy(10%).22 Table3showsthemaincharacteristicsoftheselected stud-ies.

Theageofthesamplesrangedbetween2and16years, withameanof9.28years.Regardinggender(fromthe stud-iesthatreportedit),mostsubjectsweremales(52.28%).

The proceduresusedforthe assessmentof the partici-pantswere:analysisofrecords/files:two(20%)16,20_;

inter-view:four(40%)16,17,19,22_;_{questionnaires:}_six_(60%)13---16,18,21_;

clinical evaluation or observation: six (60%)13,15---17,20,21_;

otorhinolaryngologicalassessmentdisclosingmouth breath-ing:five(50%),15,17,19,20,22_specific_tests:_six_(60%)15,17---19,21,22_;

andpuretoneaudiometry:two(20%).17,22

Regardingthedatacollectiontools,theuseofvalidated protocolswasattainedintwostudies17,22_(20%_of_the_sample)

andUemaetal.17 _used,_among_several_tests,_a _grapheme

recognitiontask,throughthelettercancelationtest,while Kuroishiet al.22 _used_the _Academic _Performance _Test, _in

partialform.

Mouth breathers showed greater difficulty in solving mathematical operations than nasal breathers.19,22

How-ever, some researchers21 _found _no _difficulty _regarding

mathematicaloperationsintheirstudy.

Reading comprehension was considered worse in the mouthbreathers,22_as_well_as_writing.21

Overall,eightstudies(80%)14---20,22_reported_learning

dis-abilities in mouth breathers, with three (30%) related to tonsillar or inferior turbinate hypertrophy,15,19,22 _three

(30%) due to sleep-disordered breathing,14,17,18 _two _(20%)

tonasalobstruction20,22_and_allergic_rhinitis_(20%),15,19 _one

(10%)associatedwithattentiondeficithyperactivity disor-der (ADHD),16 _one _(10%) _due _to _asthma,18 _and _one _(10%)

to septal deviation.22 _Of _the _studies _that _found _no

asso-ciation between mouth breathing and learning disability (n=2;20%),13,21 _one_was_related_to_nasal_obstruction13 _and

another21_did_not_divide_the_groups_between_mouth_and_nasal

breathers,classifyingtheparticipantsashavingrespiratory impairmentfeatures,withoutspecifyingthecause.

Discussion

School failures occur for different reasons; according to the last census,conducted by Instituto Nacional de Estu-dosePesquisasEducacionaisAnísioTeixeira23_(INEP,_BRASIL,

2013),in2013,6.1% ofstudentsfailtopass ontothe fol-lowing grade,withoneofthe reasonsbeingthe presence of learning disabilities. Literature has described several factors for its emergence, such as hearing,1,2 _attention,

interpersonalrelationships,behaviorandcognition disabili-ties,socioeconomicstatus,3_family_history,4_as_well_as_mouth

breathing.5

This respiratory pattern is considered a pathological adaptation6_,_which_can _affect_the _quality_of_sleep,_mood,

behavior,andschoolperformance7_;_however,_there_are_few

studiesthat showsuchinterrelation.Moreover,the preva-lenceof mouthbreathingis considered highin childhood8

and,thus,thepresentsystematicreviewwascarriedout. As shown by the sample composition, little has been investigatedonthesubject(2.8% of357 studies), demon-stratingtheneedforfurtherstudiesinthisarea.

Half of the studies in the sample used a control group,13,17,19,20,22 _and _it _is _noteworthy _that _Kajihara _and

Nishimura19_compared_their_results_with_the_control_group_of

anotherstudy,althoughtheybelongedtothesameresearch group.Thus,itissuggestedthatstudiesonthesubjectwith controlgroupsbeperformedtoattaingreaterresult reliabil-ity.Additionally,forevidence-basedpractice,thatis,fora professionaldecisiontobemadebasedontheobtained sci-entificresults,accordingtoMuirGray24_it_is_ideal_when_such

studiesshowhighevidencestrength,whichareusually con-trolledandrandomizedstudies;suchrandomizedcontrolled studieswerenotidentifiedinoursample.

Table2 ScoresobtainedafterapplyingtheMethodologyQualitativeScoreProtocol,adaptedfromPithonetal.11

Author(year) A B C D E F G H I J K Total Quality

Abreuetal.(2003)13 ₀ ₁ ₂ ₁ ₀ ₀ ₀ ₀ ₀ ₁ ₁ ₆ _Moderate

Goodwinetal.(2003)14 ₂ ₁ ₂ ₀ ₀ ₀ ₀ ₁ ₀ ₁ ₀ ₇ _Moderate

DiFrancescoetal.(2004)15 ₂ ₁ ₁ ₀ ₀ ₀ ₁ ₁ ₀ ₀ ₀ ₆ _Moderate

Veraetal.(2006)16 ₂ ₁ ₀ ₀ ₀ ₀ ₁ ₁ ₀ ₁ ₁ ₇ _Moderate

Uemaetal.(2007)17 ₁ ₁ ₀ ₁ ₀ ₀ ₁ ₁ ₀ ₁ ₁ ₇ _Moderate

Petryetal.(2008)18 ₁ ₀ ₂ ₀ ₀ ₀ ₁ ₁ ₀ ₁ ₁ ₇ _Moderate

KajiharaandNishimura(2012)19 ₂ ₀ ₀ ₁ ₀ ₀ ₀ ₁ ₀ ₁ ₁ ₆ _Moderate

Fensterseiferetal.(2013)20 ₂ ₁ ₀ ₁ ₀ ₀ ₁ ₁ ₀ ₁ ₀a ₇ _Moderate

Periloetal.(2013)21 ₁ ₁ ₁ ₀ ₀ ₁ ₁ ₁ ₀ ₁ ₁ ₈ _Moderate

Kuroishietal.(2015)22 ₁ ₁ ₀ ₁ ₀ ₁ ₁ ₁ ₀ ₁ ₁ ₈ _Moderate

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Table3 Summaryofthetenarticlesthatcomprisedthestudysampleonthesubject‘‘mouthbreathingandlearning’’.

Author,year, andplaceof study

Diagnosisandinstrumentfordata collection

Samplecharacterization Mainresults Studyconclusion

Abreuetal. (2003),13_Sao Paulo,Sao Paulo,Brazil

-Questionnairesaddressedat:teachers onschoolperformance(2ndhalfof 2001)andparents/guardians; -Medicalandclinicalassessment(the proceduresusedwerenotmentioned); -Statisticalanalysis:chi-squaredtest, withsignificancelevelof5%

-330students(ages,means,and genderdistributionwerenot mentioned);

-30mouthbreatherswithupper airwayobstruction;

-300nasalbreathers(control); -ElementarySchoolStudents(2nd to4thgraders)and

-Studentswererequiredtobe attendingtheappropriateschool yearforage

-Changesinacademicperformance werementionedin20%(n=6)of studentsinthestudygroupandin14% (n=42)ofthecontrolgroup,showinga p-value>5%

Mouthbreathingdid notinfluenceschool performanceofthe assessedchildren

Goodwinetal. (2003),14 Tucson, Arizona, UnitedStates ofAmerica

-Standardizedquestionnaire,not validated,addressedto

parents/guardiansonsleephabits (TuCASA);

-Polysomnographyathomeand -Statisticalanalysis:chi-squared(5%of significance),simplelogisticregression, andoddsratiocalculation(confidence intervalnotstated)

1494CaucasianandHispanic children;

-613malesand601females(280 formswithoutgender

identification);

-Groupsdividedbyagerange:1) Between4and7years(n=763, 53.9%)andbetween8and11 years(n=653;46.1%); -78formswithoutage

identification.Themeanageof thegroupswasnotmentioned

-Therewasnosignificantdifference betweengroupsforthepresenceof snoring,excessivedaytimesleepiness andwitnessedapnea,buttherewere significantdifferencesregardingthese characteristicswiththereported learningdisabilities;

-Significantprevalenceoflearning disabilitiesinthegroupofolder children;

-Therewerenosignificantresultswhen comparingthelearningdisabilitieswith thegendervariable

-Hispanicchildren hadahigher frequencyof symptomsof sleep-disordered breathing,snoring, excessivedaytime sleepiness,witnessed apneaandlearning disordersthanwhite children;

-Childrenwith learningdisorder complaintshadhigher chancesofhaving snoring(2.4×)

excessivedaytime sleepiness(2.5×)and

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GCA

et

al.

Table3(Continued)

DiFrancesco etal. (2004),15_Sao Paulo,Sao Paulo,Brazil

-Historyandphysicalexamination characteristicofallergicrhinitis(signs andsymptoms);

-Standardizedquestionnaireappliedto theparents/guardiansonthenocturnal symptoms;

-Physicalexamination;

-Positivehypersensitivitytest(allergic rhinitis);

-Profileteleradiographytoassess nasopharyngealobstructionand -Statisticalanalysisnotdescribedinthe method,butspecifiedinthetablesof results,usingANOVA(statistical significancevaluewasnotdeclared), Kruskal---Wallis,Mann---Whitneyand Spearman(allwith5%significance)

-142patients;

-Agesbetween2and16years (mean:7.2);

-92malesand50females; -Studygroupssubdividedinto three:

1)Allergicrhinitis(n=51); 2)Isolatedtonsilarandpharyngeal hypertrophy(n=25)

3)Tonsilarhypertrophy(n=66)

-Snoring,apnea,nocturnalrestlessness, bruxismandenuresisweremore frequentinthegroupwithtonsilar hyperplasia;

-Attentiondeficitandpoorschool performanceweremoreprevalentinthe groupwithtonsilarhypertrophy

Theinvestigationof sleepapneainmouth breathersiscrucial, aswellas

determiningthe etiologyofaltered breathingpattern

Veraetal. (2006),16_Sao Bernardodo Campo,Sao Paulo,Brazil

-Surveyof77recordsofsubjectswith learningdisordersdiagnosismadebya multidisciplinaryteam;

-Appliedquestionnairebasedonthe DSM-IVcriteriaforclassificationof AttentionDeficitHyperactivityDisorder (ADHD)subtypes;

-Assessmentofbreathing:Guided interviewwithfamilymembersand clinicalevaluationofthepatient, assessingbreathingamongother aspects,suchasbodyposture, structuresanalysisandotherfunctions ofthestomatognathicsystemand -Statisticalanalysis:testforequalityof twoproportions,ANOVA,confidence intervalforproportionandmean (significance≤5%)

-77subjectsfromtheOutpatient ServiceofNeurologicalDisorders diagnosedwithattentiondeficit hyperactivitydisorderbythe multidisciplinaryteam; -Ages7to17years(mean:not mentioned),with63males (81.8%)and14females(18.2%); -Moststudentsfrompublic schools(64---83%);

-Schoolfailure(39%),school(87%) andrespiratory(51%)complaints

-TherewasprevalenceofADHDin males,children’sagesbetween7and11 yearsandthe1stgradeto6thgrade -Therewasahighincidenceoflearning disabilities(62.3%)withschooldifficulty complaints(87%).

-Therewasstatisticalsignificancefor thepresenceoflearningdisorder,school difficultiesandnoschoolfailure(61%). -Therewashighoccurrenceofaltered breathingpattern(71.4%),whichin associationwiththeattentiondisorder, affected41.6%ofthesample.

-Therewasapredominanceofattention disorderandoronasalbreathingfor gendersandtypesofADHD

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Uemaetal. (2007),17_São Paulo,São Paulo,Brazil

-Interview;

-Generalphysicalexamination; -Otorhinolaryngologicalassessment: clinicalandinstrumentalexamination (nasofibrolaryngoscopyand

polysomnography);

-Testing:learning(Rey)andcognitive (WISC-III,cancelationofsymbolsand letters(byMesulam,previously validatedinBrazil),thelatterinvolving thegraphicrecognitionofletters)and -Statisticalanalysis:Kruskal---Wallis test,adoptingasignificancelevelof5%

-81children;

-Agesbetween6and12years (themeanwasnotstated); -41malesand36females(4 subjectsnotmentioned),divided intothreegroups:onecontrol (20),withobstructivesleepapnea syndrome(24)andanotherwith primarysnoring(37)

-Learningtest(Reytest)showedworse resultsinimmediatememoryandin attentionlevelinpatientswith obstructivesleepdisorders

Mouth-breathing childrenwith obstructivesleep disordershada poorerperformance inthelearningtest thanthecontrol group

Petryetal. (2008),18 Uruguaiana, RioGrande doSul,Brazil

-Useofquestionnairesaboutthe symptomsofbreathingsleeping disorders;asthma(databaseofthe InternationalStudyofAsthmaand AllergiesinChildhood),educationaland socio-economicaspects;

-Skintestswithcommonenvironmental allergensin2004and

-Statisticalanalysis:Chi-squaretestand multivariatelogisticregression,witha significancelevelof5%

-1011schoolchildrenfrompublic schools

-Agedbetween9and14years (mean:11.2);

-507malesand504females; -Complaintofpoorschool performance:8(0.8%)

-Presenceofhabitualsnoring:27.6%; -Presenceofdaytimemouthbreathing: 15%;

-Presenceofexcessivedaytime sleepiness:7.8%;

-Schoolchildrenwithmouthbreathing showed13×higherriskofmanifesting

symptomsofexcessivedaytime sleepinesscomparedtocontrols

-Highprevalenceof respiratorydisorders. -Childrenwith excessivedaytime sleepinessseemto haveanalmost10×

higherriskoflearning disordersthanthose without

Kajiharaand Nishimura (2012),19 Maringa, Parana, Brazil

-Otorhinolaryngologicalassessment basedontheanalysisofmedicalrecords; -Analysisofthesignsandsymptomsof mouthbreathing,throughinterviews; -Resolutionofmathematicaloperations andproblems(notvalidated)and -Statisticalanalysis:simplelogistic regressionmodelandoddsratio calculation(95%CI)

-63schoolchildren(30mouthand 33nasalbreathers);

-Mouthbreathersdiagnosedwith allergicrhinitisandpharyngeal tonsilhypertrophy;

-Agesbetween8and10years (meanwasnotmentioned); -Sampledistributionregarding genderwasnotmentioned; -Studentsbetweenthethirdand fourthgradefrompublicschools

Mathematicalmistakes:

-Amongmouthbreathers:334(65.49%); -Control:173(30.84%).

Throughsimplelogisticregression, mouthbreathersweremorelikelyto showdifficultieswhencomparedto controls,inthetasksof:

1)Mathematicaloperations(4times), mainlyinvolvingattention(4×),

algorithm(4×)andcombinederrors

(18×);

2)Resolutionofmathematicalproblems (8×),withchanceofattentionerrors

(10×)andproblemsinterpretation(9×)

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474

Ribeiro

GCA

et

al.

Fensterseifer etal. (2013),20 PortoAlegre, RioGrande doSul,Brazil

-Clinicalneuropediatric,psychological, andsocialassessment;

-Clinicalotorhinolaryngological, instrumentalandimagingassessment (oroscopy,anteriorrhinoscopy,cavum X-ray,andecho-rhinometry);

-Learningdisabilitydefinedbyhistory of,atleast,twoconsecutiveyearsof schoolfailurefortheexperimental groupand

-Statisticalanalysis:Mann---Whitneytest andStudent’st-testwithsignificance valueofp<0.5

-48schoolchildren;

-Agesbetween8and12years (mean:9.1);

-GroupI-24studentswith learningdisabilities;

-GroupII(Control)-24students withoutlearningdisabilities; -18(37.5%)werefemalesand30 males(62.5%);

-Allstudentsattendedpublic schools

Nasalobstructiontendedtobehigherin patientswithlearningdifficulties. Therewasastatisticallysignificant associationbetweenlearningdisabilities andpharyngealtonsillarandpalatine hypertrophy

Studentswith tonsillarhypertrophy, mouthbreathers, havegreater difficultyinlearning comparedtochildren withouthypertrophy

Periloetal. (2013),21 Belo Horizonte, MinasGerais, Brazil

-RespiratoryCharacteristicAssessment Questionnaire;

-Assessmentoftheusuallippositionby observingthechildfor5min(bytwo evaluators);

-ProtocolofAssessmentof

Cognitive-LinguisticSkills-collective version,Brazilianadaptation:alphabet recognitioninsequence,copyofshapes, writingunderdictation,arithmeticand short-termmemory,and

-Statisticalanalysis:Mann---Whitneyand KruskalWallistestwithp<0.01for statisticallysignificantcorrelations

-131schoolchildren(664th gradersand653rdgradersfrom elementaryschool);

-Bothgenders(distributionwas notmentioned);

-Ages9to10years(meannot mentioned);

-Allstudentsattendedpublic schools

Therewasnosignificantassociation betweentheperformanceof cognitive-linguisticskillsandthe presenceofrespiratorycharacteristics amongthesampleschoolchildren

(10)

Oral

breathing

and

learning:

literature

review

475

Kuroishietal. (2015),22 Ribeirao Preto,Sao Paulo,Brazil

-ClinicalInterview; -Puretoneaudiometry;

-Otorhinolaryngologicalassessmentby clinicalandimagingassessment (oroscopy,rhinoscopyand nasoendoscopy);

-Sentencereadingcompetencetestto evaluatereadingcomprehension;School achievementtest(Arithmeticsubtest); Illinoistestofpsycholinguisticabilities withBrazilianadaptation(auditory sequentialmemorysubtest-number repetition)andrepetitionof pseudowordsand

-Statisticalanalysis:Mann---Whitney test,withsignificancelevelof5%

-55schoolchildren(42mouthand 11nasalbreathers);

-Gender:29femalesand26 males;

-Samplesizecalculationwas performed(aminimumof13 participantswasdeterminedper group);

-Agesbetween7and10years (meanage:8.7yearsforthe mouthbreathergroupand8.4for thecontrol);

-Mouthbreatherswithoneor moreofthefollowing

characteristics:nasalobstruction orirritation(>3months), hypertrophy(tonsillarorinferior turbinate)anddeviatedseptum; -Educationallevel:2ndand3rd gradersofelementaryschool attendingpublicschools

Studentswithmouthbreathingshowed significantlyworseperformancewhen comparedtonasalbreathingonesin readingcomprehension,arithmeticand operationalmemoryforpseudowords, butnotfornumbers

(11)

476 RibeiroGCAetal.

As for the nosological diagnosis confirming the eti-ology of mouth breathing, half of the researchers we studied15,17,19,20,22_submitted_their_sample_groups_to

otorhi-nolaryngological assessment, demonstrating obstructive mouth breathing, although with different etiologies. It shouldalsobenotedthatAbreuetal.13_stated_that_the_study

groupunderwentmedicalassessment,butdidnotmention whichspecialtyperformedsuchassessmentorwhat proce-dureswereperformed.

Perilo et al.21 _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 otorhinolaryngologicalevaluationtoconfirmtheetiologyof thealteredbreathingpattern,didnotmentionthenumber ofaffirmative questionsthat shouldhave been marked in orderto consider the subject a possible mouth breather. Such bias was minimized by observing labial sealing for 5min,observedbytwoevaluatorsduringadistractortask. Thus,theydidnotdividethesampleintomouthandnasal breathers,analyzing therespiratory characteristics ofthe sample and comparing them with the cognitive-linguistic skills.

The assessed studies that comprised the sample used non-probabilisticsamples,chosen intentionallyor by con-venience, that can result in bias in data interpretation as it depends on the researcher’s appraisal. Despite the abovementionedfact,Kuroishietal.22_carried_out_a_sample

calculationstudytodeterminethesample sizethatwould providea morerepresentativepopulation andmore accu-rateresults.25

Although school failure is a complex analysis variable since other aspects can influence its occurrence, it is inferredthatstudentswithlearningdisordershaveagreater chance for failure.Therefore,it wouldbe worthwhilefor studiestoshowwhetherthe sampleconsisted ofstudents thatdidordidnotfailschool.TheresearchbyFensterseifer etal.20_established_a_minimum_of_two_years,_and_the_study

byVeraetal.16_reported_complaints_(by_most_of_the_family

membersofmouthbreathers)oflearningdifficulties,while 39%hadfailed(fromonetothreetimes),moreoftenin ele-mentaryschool.Otherstudies14,15,17---19,21,22_did_not_mention

schoolfailure,andinthestudybyAbreu etal.,13 _the

stu-dentswererequiredtobeattheappropriateschoolyearfor age,i.e.,thosestudentswhofailedwerenotincludedinthe study,whichmaybeconsideredaweakness.

Anotherimportantfactorforanalysisistheplacewhere theselectedstudioes occurredandthetimeperiodduring which the studies were performed, since climate change must be taken into account.26 _Most _studies _in _our

sam-plewerecarriedoutbyBrazilianresearchers,13,15---22_which

justifies our interest in the subject. Only four studies (40%)13,15,17,20_indicated_the_period_(in_months_or_years)

dur-ingwhichthesampleselectionwasobtained.

Researchers27 _have _emphasized _the _impact _of _climate

changeonupperairway(UA)disordersinchildrenyounger than 13 years in the metropolitan region of São Paulo, in the months that correspond to the start of winter. Theyaddedthatthepeakofrespiratorydiseasemorbidity occursin May,possiblydue tothermoregulation problems insubjectsadaptedtothemilderclimate/weatherofApril, explainingthatpeoplewiththermoregulationproblemsare

more sensitive torespiratory andcardiovasculardiseases, especiallythepediatricpopulation.

There is an increase in hospital consultations27

dur-ing this period and,consequently, a higher probability of school absenteeism, which can impair academic perfor-mance,dependingonthechronicityofthecondition.

In Brazil, respiratory diseases accounted for 5% of the years of life lost due to premature death,28 _emphasizing

the importance of public health measures to reduce this percentage.

Anotheranalysisvariableconcernstheimpactof urban-izationontheliving conditionsandhealthof theBrazilian population. It can be observed that of the ten selected studies,halfwereperformedincapitalcities13,15,17,20,21_and

the other half14,16,18,19,22 _in _{well-developed} _cities. _In_large

Brazilian cities, according to Maricato,29 _there _has _been

an increase in ecological social inequality, a situation in whichthereisanuncontrolledgrowthofcities,with popula-tionincreaseintheoutskirtregions.Usually,theindividuals livingintheoutskirtsofBraziliancitieshavealow socioeco-nomicstatus(asdemonstratedbyresearch)30_and,_thus,_are

morevulnerabletofactorsthatcancompromisequalityof lifeandhealth.

In addition to the aforementioned facts, it can be observedthatschoolfailureishigherinboysthaningirls, predominantly among African-descendants and/or those fromlow-incomefamilies.30 _This_study _sample_was_mostly

comprised of boys,confirming whatliterature has shown, bothwithrespecttoschoolfailureandthepossibilityofthe presenceofacomorbidityfactor,suchasADHD.16

Thus,itispossibletoconcludethattheunderstandingof thedeterminantsoflearninganditsfailureare multifacto-rialandcomplex;moreover,therearefewvalidated tools toinvestigatelearningdisorders,andthatcreatesdifficulty when comparing the procedures. Only two studies22 _used

validated tools, another21 _used _a _published _protocol _that

was adapted to Brazilian students, and another19 _applied

anevaluationtestthatwasusedinadifferentnon-validated study;theremainingstudies13---16,18,20_did_not_use_assessment

protocols withthe students, butinstead usedschool fail-urerecordsorquestionnairesappliedtofamilymembersor teachers,increasingtheanalysisbiasinsuchstudies.

The School Achievement Test (Teste de Desempenho Escolar --- TDE), developed by Lilian Stein,31 _was_partially

usedinonestudy(10%).22 _The _study_compared_the

exper-imentalgroupwithacontrolgroup andthesubjectswere matched for age and educational level, with part of the sampleshowingmouthbreathing.Itwasverifiedthatsuch students had lower school performance than the control group in reading comprehension, arithmetic, and working memorytasks(exceptfornumbers).

Regardingtheassessmentofmathematicalskills,two19,22

ofthestudiesthatappliedtestsfoundresultsindicating dif-ficultiesinmouthbreathers,whiletheotheronedidnot.21

Reading comprehension was considered worse in mouth breathers,22 _as_well_as_writing_skills_in_subjects_with

respi-ratorydisordercharacteristics,whencomparedwiththose withoutsuchdisorders.21

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for analysis was small and showed diverse evaluation procedures.Controlled, interdisciplinarystudies, withthe inclusionofstandardizedassessments,usingvalidatedtools and uniform sample groups must be performed sothat a systematic meta-analysisreview study canbe carried out and,thus,morescientificevidencewillbecomeavailable, both for clinical practice and for the implementation of publichealthandeducationpolicies.

Conclusions

Thereisevidencethatthebreathingpatterncaninfluence the learning process.This systematic review showed that mouthbreathersaremorelikelytohavelearningdifficulties thannasalbreathers.Furtherstudiesareneededinorderto increasethescientificevidenceforclinicalpractice,andfor theimplementationofpublichealthandeducationpolicies.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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