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crescimento facial vertical após a adenotonsilectomia em
UNIVERSIDADE FEDERAL DE MINAS GERAIS
FACULDADE DE MEDICINA
Programa de Pós-Graduação em Saúde da Criança e do Adolescente
CRESCIMENTO FACIAL VERTICAL
APÓS A ADENOTONSILECTOMIA EM
RESPIRADORES ORAIS: O QUE
ESPERAMOS É O QUE
ENCONTRAMOS?
BERNARDO QUIROGA SOUKI
BELO HORIZONTE - MG
2009
BERNARDO QUIROGA SOUKI
CRESCIMENTO FACIAL VERTICAL
APÓS A ADENOTONSILECTOMIA EM
RESPIRADORES ORAIS: O QUE
ESPERAMOS É O QUE
ENCONTRAMOS?
Tese apresentada ao Programa de Pós-Graduação em
Saúde da Criança e do Adolescente, da Faculdade de
Medicina da UFMG, como requisito parcial à obtenção do
grau de Doutor em Ciências da Saúde.
Orientador: Prof. Dr. Jorge Andrade Pinto
Co-orientadora: Profa. Dra. Helena Maria Gonçalves Becker
BELO HORIZONTE - MG
2009
S721c
Souki, Bernardo Quiroga.
Crescimento facial vertical após a adenotonsilectomia em respiradores
orais [manuscrito]; o que esperamos é o que encontramos? / Bernardo
Quiroga Souki. - - Belo Horizonte: 2009.
130f.: il.
Orientador: Jorge Andrade Pinto.
Co-orientadora: Helena Maria Gonçalves Becker.
Área de concentração: Saúde da Criança e do Adolescente.
Tese (doutorado): Universidade Federal de Minas Gerais, Faculdade de
Medicina.
1. Respiração Bucal. 2. Adenoídectomia. 3. Tonsilectomia. 4. Má
Oclusão/epidemiologia. 5. Dissertações Acadêmicas. I. Pinto, Jorge
Andrade. II. Becker, Helena Maria Gonçalves. III. Universidade Federal de
Minas Gerais, Faculdade de Medicina. IV. Título.
NLM: WS 280
2
3
Programa de Pós-Graduação em Ciências da Saúde
Área de Concentração em Saúde da Criança e do Adolescente
Reitor: Prof. Ronaldo Tadêu Pena
Vice-Reitora: Profª. Heloisa Maria Murgel Starling
Pró-Reitora de Pós-Graduação: Profª. Elizabeth Ribeiro da Silva
Pró-Reitor de Pesquisa: Prof. Carlos Alberto Pereira Tavares
Diretor da Faculdade de Medicina: Prof. Francisco José Penna
Vice-Diretor da Faculdade de Medicina: Prof. Tarcizo Afonso Nunes
Coordenador do Centro de Pós-Graduação: Prof. Carlos Faria Santos Amaral
Subcoordenador do Centro de Pós-Graduação: João Lúcio dos Santos Jr.
Chefe do Departamento de Pediatria: Profª. Maria Aparecida Martins
Coordenador do Programa de Pós-Graduação em Ciências da Saúde – Área de Concentração
em Saúde da Criança e do Adolescente: Prof. Joel Alves Lamounier
Subcoordenadora do Programa de Pós-Graduação em Medicina - Área de
Concentração em Pediatria: Profª. Ana Cristina Simões e Silva
Colegiado do Programa de Pós-Graduação em Ciências da Saúde – Área de Concentração em
Saúde da Criança e do Adolescente:
Profª. Ivani Novato Silva
Prof. Jorge Andrade Pinto
Profª. Lúcia Maria Horta Figueiredo Goulart
Profª. Maria Cândida Ferrarez Bouzada Viana
Prof. Marco Antônio Duarte
Profª. Regina Lunardi Rocha
Gustavo Sena Sousa (Representante Discente)
4
À minha amada esposa Barbra, grande incentivadora
deste ideal acadêmico. Sem o seu apoio este projeto
não chegaria ao final.
Às minhas queridas filhinhas Ana Clara e Nina, de
quem tanto tempo roubei para dedicar a este trabalho.
Ao saudoso Breno, que tanta falta me faz.
5
AGRADECIMENTOS
Ao Dr. Jorge Andrade Pinto pela oportunidade a mim confiada ao assumir a
responsabilidade desta orientação, abrindo portas para este meu projeto
pessoal. A
objetividade
liberdade e confiança por ele me oferecidas, bem como a
na
sua
competente
orientação
me
fizeram
crescer
academicamente. Reconhecerei eternamente esta oportunidade.
À minha co-orientadora Helena Maria Gonçalves Becker pela carinhosa
acolhida no Ambulatório do Respirador Oral do HC-UFMG, lidando sempre
de forma empolgada e amiga nas questões relativas aos nossos projetos
acadêmicos, incluindo esta tese. Muitíssimo obrigado por tudo!!!
À Letícia Paiva Franco, médica otorrinolaringologista que participou
ativamente de toda a coleta de dados para esta tese, operando de forma
competente as nossas crianças. O seu interesse pelo bom andamento do
meu trabalho, como se fosse a sua própria tese, nunca será esquecido.
Você foi incrível!!!
À ortodontista Giovana Batista Pimenta, companheira de projetos
acadêmicos à tanto tempo, muito obrigado pela ajuda na coleta dos dados
e elaboração dos artigos. Este trabalho também é seu!!!
Ao meu irmão Marcelo que também me acompanha na vida profissional há
tantos anos, agradeço a ajuda na coleta inicial dos dados, bem como os
constantes comentários críticos durante a redação dos artigos.
6
À Gleicilene Silva Chaves pela competente ajuda na coleta de dados,
controlando os retornos dos pacientes pós-cirúrgicos, assim como
monitorando a adesão dos núcleos familiares daquelas crianças que
estavam na fila de espera do SUS. A maneira alegre e disponível que você
sempre nos ajudou ficará aqui registrada. Boa sorte nos seus projetos
futuros.
A todos os residentes de Otorrinolaringologia do HC-UFMG, graduandos
bolsistas do AROHC-UFMG e funcionárias do Hospital São Geraldo do HCUFMG, que contribuíram com a coleta de dados, o meu muito obrigado.
Ás alergologistas Juliana e Marisa, colegas de AROHC-UFMG agradeço a
ajuda na coleta de dados, bem como a cordialidade na relação profissional
semanal.
Ao cirurgião-dentista Sidney M. Williams agradeço a disponibilidade de
revisar a redação dos artigos em língua inglesa.
Aos Drs. Paulo Camargos, Dauro Oliveira, Celso Becker e Paulo Fernando
que participaram da banca de qualificação, trazendo importantes sugestões
para esta tese.
Aos Professores Júlio Carlos Noronha, Maria de Lourdes de Andrade
Massara e José Ferreira Rocha Júnior pela amizade e oportunidades
oferecidas na minha jornada acadêmica que me permitiram crescer e
alcançar agora esta tese de doutoramento.
7
APRESENTAÇÃO
Este trabalho se refere à tese apresentada ao Programa de Pós-Graduação em
Saúde da Criança e do Adolescente da Faculdade de Medicina da
Universidade Federal de Minas Gerais (UFMG) e representa requisito parcial
para a obtenção do título de doutor.
Os questionamentos que motivaram as investigações apresentadas nesta tese,
bem como os dados para a sua elaboração, surgiram no Ambulatório do
Respirador Oral do Hospital das Clínicas da UFMG (AROHC-UFMG). Tal
projeto teve as suas atividades iniciadas em novembro de 2002, sendo
aprovado pelo Comitê de Ética e Pesquisa da UFMG (COEP-UFMG) com o
parecer ETIC 291/03 sob o título “Estudo das alterações otorrinolaringológicas,
fonoaudiológicas, alergológicas, ortodônticas e posturais do respirador oral”.
A proposta primária do AROHC-UFMG é a avaliação interdisciplinar de
crianças respiradoras orais. Após a anamnese completa, conduzida por
otorrinolaringologistas, as crianças são submetidas a exames clínico e
complementar por profissionais das áreas de Otorrinolaringologia, Alergologia,
Ortodontia e Fonoaudiologia, visando diagnosticar os fatores etiológicos da
disfunção respiratória e dar o encaminhamento e/ou orientações terapêuticas.
Até o dia 20 de agosto de 2009, após quase 7 anos de atividades, o AROHCUFMG atendeu 639 crianças com idade variando entre 2 anos e 8 meses a 12
anos e 9 meses. A média de idade é de 6 anos e 6 meses. Deste total, 364
(56,96%) eram do sexo masculino e 275 (43,04%) do sexo feminino. A
indicação de cirurgia para a desobstrução das vias aéreas superiores foi dada
para 286 crianças (44,75%).
De acordo com as opções de formato contempladas pelo regulamento do
Programa, essa tese se baseia em três artigos produzidos durante o
doutoramento, respectivamente intitulados:
8
1) “Prevalence of malocclusion among mouth breathing children: do
expectations meet reality?”
2) “Changes in vertical dentofacial morphology after adeno-/tonsillectomy during
deciduous and mixed dentitions mouth breathing children - one year follow up
study”
3) “Vertical facial growth following adeno-/tonsillectomy: changing concepts?”
O primeiro artigo (Capítulo 1.1) foi elaborado a partir dos dados coletados
durante os primeiros cinco anos de funcionamento do AROHC-UFMG. Ele traz
um levantamento epidemiológico sobre a prevalência de más oclusões em um
centro de referência para respiradores orais. A reconhecida associação entre a
respiração oral e algumas alterações dentofaciais (má oclusão de classe II,
mordida aberta anterior e mordida cruzada posterior), faz com que os clínicos
tenham a expectativa de encontrar más oclusões na maioria das crianças
respiradoras orais. Da mesma forma, é fácil imaginar que o grau de obstrução
das vias aéreas superiores tenha associação com a prevalência das referidas
más oclusões. Nos primeiros anos de funcionamento do AROHC-UFMG, os
profissionais envolvidos com o atendimento perceberam que a expectativa de
encontrar más oclusões nas crianças examinadas não era plenamente
contemplada. Surgiu, assim,
a necessidade de
estudar
de maneira
academicamente formal este assunto, especialmente em uma grande amostra
de respiradores orais. Este primeiro artigo foi publicado na revista International
Journal of Pediatric Otorrinolaryngology, no volume 73, disponível online em 12
de março de 2009. Os seus dados principais foram apresentados, na forma de
pôster, no XIX ENT World Congress, recebendo o prêmio de Melhor Trabalho
na categoria Otorrinopediatria.
O segundo artigo (Capítulo 2.2) traz respostas à dúvida, quanto a eventuais
diferenças no padrão de crescimento facial vertical, se a desobstrução cirúrgica
das vias aéreas superiores é efetuada durante a fase de dentadura decídua ou
na fase de dentadura mista. Este assunto é original na literatura, sob uma
perspectiva longitudinal, e pretende adicionar informações que possam auxiliar
na decisão sobre a época ideal para a adenotonsilectomia em crianças
respiradoras orais. Este artigo foi aceito para publicação na revista International
9
Journal of Pediatric Otorrinolaryngology, recebendo o número IJPORL-D-0900411.
No terceiro artigo (Capítulo 3.3) é feita uma reflexão sobre o conceito
consensual de que as crianças submetidas à desobstrução cirúrgica das vias
aéreas superiores adquirem um crescimento facial vertical mais próximo da
normalidade. Este artigo será enviado para a publicação na revista Angle
Orthodontist, após a publicação do Artigo 2, em função deste último servir de
referencial metodológico.
Além dos capítulos referentes aos artigos, esta tese traz um capítulo de
Considerações Iniciais onde são introduzidos os temas a serem estudados,
além da descrição do Objetivo da tese. No capítulo de Considerações Finais é
feita uma breve síntese dos achados e são apresentadas as conclusões. Nos
Anexos são trazidas 1) a aprovação desta pesquisa pelo Comitê de Ética em
Pesquisa da Universidade Federal de Minas Gerais, 2) a versão em PDF da
publicação do Artigo 1 e 3) o comprovante de aceitação do Artigo 2 pela revista
International Journal of Pediatric Otorhinolaryngology.
As citações apresentadas em cada um dos três artigos encontram-se com
numeração “entre colchetes” [ ], na seqüência que aparecem nos texto,
conforme normas das revistas para qual eles foram encaminhados. A lista de
referências bibliográficas encontra-se ao final de cada artigo.
As citações apresentadas nos Capítulos 1 e 3 foram numeradas em ordem
alfabética, a partir da lista de referências bibliográficas apresentadas ao final do
Capítulo 1.
10
RESUMO
Introdução: A associação entre a respiração oral e o crescimento dentofacial
tem sido descrita na literatura há pelo menos 150 anos. Apesar de uma série
de conceitos a respeito deste tema estar consolidado na mente dos clínicos, é
lícito questionar se a expectativa criada pelos dados apresentados previamente
corresponde à realidade. O que esperamos é o que encontramos? Assim, esta
tese teve como objetivo 1) levantar a prevalência de más oclusões associadas
com a respiração oral e estudar a sua associação com os fatores obstrutivos
nasais, 2) estudar o impacto da adenotonsilectomia (A+A), realizada em dois
estágios do desenvolvimento oclusal, no crescimento facial vertical e 3) avaliar
se a A+A realmente favorece a melhora do padrão de crescimento facial
vertical, utilizando um desenho metodológico diferente, com outro tipo de grupo
controle.
Métodos: Tese apresentada no formato de três artigos, com cada um deles
respondendo a cada objetivo, respectivamente. O primeiro deles apresenta um
levantamento epidemiológico sobre a prevalência de más oclusões (classe II,
mordida aberta anterior e mordida cruzada posterior) em uma amostra de 401
crianças respiradoras orais. Por meio de análise univariada foi estudada a
associação entre a obstrução das vias aéreas superiores e essas más
oclusões. O segundo artigo traz um estudo sobre o crescimento facial vertical,
após 1 ano da A+A, em dois estágios do desenvolvimento da oclusão
(dentaduras decídua e mista). No terceiro artigo é feita uma avaliação do
crescimento facial vertical após a A+A em 39 crianças respiradoras orais (TG).
O grupo controle (CG), composto por crianças respiradoras orais com
indicação de A+A, foi pareado com o TG em relação à faixa etária, estágio de
desenvolvimento da oclusão, gênero e padrão facial vertical.
Resultados: Artigo 1 - A idade média da amostra era de 6 anos e 6 meses
(D.P.: 2 anos e 7 meses), com variação entre 2 e 12 anos. Todos os pacientes
foram avaliados por otorrinolaringologistas para a confirmação do hábito de
respiração oral. Obstrução por adenóide e/ou amígdala foi detectada em 71,8%
da amostra, independentemente da presença de rinite. Rinite alérgica,
isoladamente, foi encontrada em 18,7% das crianças. Respiração oral não
obstrutiva foi diagnosticada em 9,5% da amostra. Mordida cruzada posterior foi
encontrada em aproximadamente 30% das crianças durante as fases de
11
dentaduras decídua e mista e 48% dos indivíduos durante a dentadura
permanente. Nas dentaduras mista e permanente a mordida aberta anterior e a
má oclusão de classe II foram muito prevalentes. Mais do que 50% das
crianças respiradoras orais apresentavam uma relação inter-arcos dentários
normal nos três planos do espaço. A análise univariada não mostrou
associação estatisticamente significativa entre o tipo de obstrução (hiperplasia
por adenóide/amígdala ou presença de rinite) e más oclusões (classe II,
mordida aberta anterior e mordida cruzada posterior). Artigo 2 - Após 1 ano de
acompanhamento,
nenhuma
diferença
estatisticamente
significativa
no
crescimento facial vertical foi observada nos grupos submetidos a A+A na
dentaduras decídua ou mista, comparativamente aos seus grupos controle
obstruídos. Exceção feita à divergência maxilo-mandibular durante a fase de
dentadura decídua. Artigo 3 - Crescimento facial significativo (p<0,000) foi
encontrado para todas as medidas lineares em TG e CG. Uma redução da
proporção do terço inferior da face em relação à altura facial total, da inclinação
do plano mandibular em relação à base craniana e da divergência maxilomandibular, bem como um aumento da proporção da altura facial posterior em
relação à altura facial anterior total, aconteceu em TG e CG. Não houve
diferença estatisticamente significativa entre a rotação mandibular do TG e CG.
Conclusões:
. A prevalência de mordida cruzada posterior foi maior na população de
respiradores orais do que na população geral, independentemente dos estágios
de desenvolvimento da oclusão.
. A prevalência de mordida aberta anterior e de má oclusão de classe II foi
maior nas crianças mais velhas (dentaduras mista e permanente) do que nas
mais novas (dentadura decídua).
. Não houve associação entre a causa da respiração oral (hiperplasia de
adenóide, hiperplasia de amígdala, rinite, funcional) e a presença de má
oclusão de classe II, mordida aberta anterior e mordida cruzada posterior.
. A maioria das crianças respiradoras orais apresentou uma relação oclusal
inter-arcos normal.
. Não houve diferença no padrão de crescimento facial vertical quando a A+A
foi realizada nas fases de dentaduras decídua ou mista inicial, exceção feita à
divergência maxilo-mandibular durante a dentadura decídua.
12
.
As
crianças
submetidas
a
A+A
tiveram
um
crescimento
facial
predominantemente horizontal, similar à normalidade descrita na literatura.
. As crianças que permaneceram obstruídas por 1 ano também tiveram um
crescimento facial predominantemente horizontal.
. Sugere-se a necessidade de uma revisão das conclusões apresentadas
previamente por outros autores a respeito do impacto da desobstrução
cirúrgica das vias aéreas superiores sobre o padrão de crescimento facial
vertical.
13
SUMMARY
Introduction: The association between nasal impairment and dentofacial
morphology has been studied for more than a century. Controversies still exist
about this subject, despite a lot of information is available on the literature.
Therefore, the purpose of this PhD thesis was to evaluate if expectations meet
reality regarding some assumptions previously established on clinicians’ minds.
Three points were investigated: 1) epidemiological report on the prevalence of
malocclusion among a group of children consecutively admitted at a referral
mouth breathing (ENT) center, studying the association of such malocclusions
and upper airway obstructive factors, 2) the impact of respiration normalization
on vertical dentofacial growth during two stages of dental development after
adeno-/tonsillectomy (T&A) and 3) the impact of respiration normalization on
vertical dentofacial growth after adeno-/tonsillectomy (T&A), controlling the
results with a matched group of untreated mouth breathing children.
Methods: The work described in this thesis consists of three papers. Each one
answering each objective listed above. The first paper reports a cross-sectional,
descriptive study, carried out at an Outpatient Clinic for Mouth-Breathers.
Dental inter-arch relationships and nasal obstructive variables of 401 children
were diagnosed and the appropriate cross tabulations were done. In the second
paper,
linear
and
angular
cephalometric
measurements,
as
well
as
superimposing tracings of serial lateral cephalograms of 39 patients in the
treatment group were compared with those of 31 untreated mouth breathing
controls. Cephalometric records in the treatment group comprised registrations
made at baseline before surgery (T0), and then at approximately 1 year postoperatively (T1). Corresponding registrations were available for the control
group, with baseline cephalometric radiographs taken approximately 1 year
before the second one (T0 and T1, respectively). Treated and untreated
individuals were divided into deciduous and mixed dentition groups to aid
identification of an optimum timing for normalizing the respiration after T&A,
under a vertical dentofacial perspective. In the third paper the impact of T&A on
the vertical dentofacial growth is revisited after an untreated group of mouth
breathing children served as controls.
Results: Paper #1 - Mean age was 6 years and 6 months (SD: 2y7m), ranging
14
from 2 to 12 years. All subjects were evaluated by otorhinolaryngologists to
confirm mouth breathing habit. Adenoid/tonsil obstruction was detected in
71.8% of this sample, regardless of the presence of rhinitis. Allergic rhinitis
alone was found in 18.7% of the children. Non obstructive mouth breathing was
diagnosed in 9.5% of this sample. Posterior crossbite was detected in almost
30% of the children during primary and mixed dentitions and 48% in permanent
dentition. During mixed and permanent dentitions, anterior open bite and class
II malocclusion were highly prevalent. More than 50% of the mouth breathing
children carried a normal inter-arch relationship in the sagital, transversal and
vertical planes. Univariate analysis showed no significant association between
the type of the obstruction (adenoids/tonsils obstructive hyperplasia or the
presence of allergic rhinitis) and malocclusions (class II, anterior open bite and
posterior crossbite).
Paper #2 - After one year of follow up, no statistically significant difference on
vertical dentofacial growth was observed in deciduous or mixed dentitions
treatment groups compared to same stage untreated control groups. The
reduction of the divergence (NL-MP) between maxilla and mandible was
statistically significant greater for adeno-/tonsillectomy group during primary
dentition.
Paper #3 - Statistically significant growth (p<0.000) was found for all linear
measurements (SBL-Go, SBL-Me, NL-Me) in both groups (TG and CG). A
reduction in LAFH/TAFH, SBL-MP and NL-MP, as well as an increase in
PFH/TAFH, were the growth mean behavior both in TG and CG. There was no
statistically significant difference between TG and CG regarding the mandibular
rotation.
Conclusions:
. The prevalence of posterior crossbite is higher in mouth-breathing children
than in the general population.
. During mixed and permanent dentitions, anterior open bite and class II
malocclusion were more likely to be present in mouth breathers.
. Although more children showed these malocclusions, most mouth breathing
children evaluated in this study did not match the expected “mouth breathing
dental stereotype.
. In this population of mouth breathing children, the obstructive size of adenoids
15
or tonsils and the presence of rhinitis were not risk factors to the development of
class II malocclusion, anterior open bite or posterior crossbite.
. Regarding the vertical dentofacial growth pattern, normalization of the mode of
respiration after T&A in young children (deciduous dentition) is not more
effective than in older children (mixed dentition).
. The normalization of the mode of respiration, after T&A, did not change the
pattern of mandibular vertical growth, after one year, when compared to a
matched untreated group of mouth breathers.
. Apparently, there is a greater clockwise rotation of the anterior portion of
maxilla in adeno-/tonsillectomized children than in obstructed controls during
primary dentition.
. The previously posted concept that T&A improve the vertical dentofacial
growth must be revisited.
16
LISTA DE FIGURAS
Artigo 2
Figure 1Figure 2-
Figure 3-
Figure 4-
Cephalogram illustrating the skeletal landmarks, the
angular and linear measurements…………………………..
Mandibular true rotation evaluated by angular changes
between T0 (SBL 1) and T1 (SBL 2) after the
superimposition on the fiducial skeletal landmarks
indicated by arrows……………………………………………
Mandibular apparent rotation between T0 and T1.
Superimposition
on
the
SBL
at
“point
T”……………………………………………………………..….
Net growth measured in the four groups (TG1, CG1, TG2,
CG2). Negative values mean measurement reduction
between T0 and T1 while positive values indicate
increase………………………………....................................
64
65
66
72
Artigo 3
Figure 1-
Net growth measured in the treatment group (TG) and
control group (CG). Negative values mean measurement
reduction between T0 and T1 while positive values indicate
increase………………………………………………………... 91
17
LISTA DE TABELAS
Artigo 1
Table 1-
Table 2-
Table 3-
Prevalence of dental and ENT findings according to gender
distribution. Number of children (n) and prevalence given in
percentage (n/N x 100%)………………………………………………… 41
Prevalence of dental and ENT findings in the deciduous. mixed and
permanent dentitions. Number of children (n) and prevalence given
43
in percentage (n/N x 100%)…………………………………………..
Univariate analysis between grouped malocclusion (dependent
variable) and the obstructive causes for mouth breathing
45
(independent variables)……………………………………………….
Artigo 2
Table 1-
Table 2-
Table 3-
Table 4-
Table 1- Independent samples t-test comparison of the baseline
(T0) cephalometric angular and ratio measurements between the
treatment (TG) and control (CG) groups during the two stages of
dental development (deciduous and mixed dentitions)……………..
Table 2- Paired-sample t-test comparison between changes of
cephalometric measurements in T0 and T1 for the group of children
submitted to T&A during deciduous dentition (TG1) and its untreated
matched control group (CG1)…………………..………......................
Table 3- Paired-sample t-test comparison between changes of
cephalometric measurements in T0 and T1 for the group of children
submitted to T&A during mixed dentition (TG2) and its untreated
matched control group (CG2)...…………………………………….......
Table 4– Independent samples t-test comparison of mandibular
rotation (true rotation. apparent rotation and angular remodeling)
between treatment (TG) and control (CG) groups during deciduous
and mixed dentitions…………………………………………………......
68
69
70
71
Artigo 3
Table 1Table 2-
Table 3-
Table 4-
Comparison of the baseline (T0) cephalometric angular, linear and
ratio measurements between the TG (n=39) and CG (n=31)……..
Comparison between the treatment group (TG) and control group
(CG) for changes within each pair of variable using a paired
Student’s t-test….………………………………………………………..
Comparison between the treatment group (TG) and control group
(CG) for nominal changes in vertical facial proportions (LAFH/TAFH
and PFH/TAFH) and skeletal rotation (SBL-PM and NL-PM) using χ2
test………………………………………………………………………..
Comparison between the treatment group (TG) and control group
(CG) mandibular rotation using an independent sample t-test……..
89
90
92
92
18
ÍNDICE
Capítulo 1: Considerações iniciais .........................................................
20
1.1 A associação entre a respiração oral e o crescimento dentofacial.
1.2 Normalização da respiração, após a desobstrução cirúrgica das vias aéreas
superiores, e o crescimento facial vertical.
1.3 Adeno-/tonsilectomia na desobstrução das vias aéreas superiores: existe
uma época ideal?
1.4 Objetivo da tese ……………………………………………….........
29
1.5 Referências bibliográficas ..............................................................
30
Capítulo 2: Artigos …………………………………………………………
33
2.1 - Artigo 1: “Prevalence of malocclusion among mouth breathing children: do
expectations meet reality?” ……………………………………………..
34
2.2 - Artigo 2: “Changes in vertical dentofacial morphology after adeno/tonsillectomy during deciduous and mixed dentitions mouth breathing children one year follow up study” ……………………………………………… …
57
2.3 - Artigo 3: “Vertical facial growth following adeno-/tonsillectomy: changing
concepts?” …………………………………………………………….. ....
82
Capítulo 3: Considerações finais ……………………………………. ....
100
Apêndices e Anexos
Apêndice 1 – Termo de Consentimento Livre e Esclarecido ................
108
Apêndice 2 – Dados brutos do Artigo 1 ....................................................
109
Apêndice 3 – Dados brutos dos Artigos 2 e 3 ..........................................
118
Anexo 1: Cópia da aprovação do projeto no Comitê de Ética em Pesquisa da
Universidade Federal de Minas Gerais......................................................
121
19
Anexo 2: Artigo 1 – versão impressa da Revista International Journal of Pediatric
Otorhinolryngology...................................................................................
122
Anexo 3: Aceitação do Artigo 2 pela Revista International Journal of Pediatric
Otorhinolryngology............................................................................
130
20
CAPÍTULO 1
Considerações iniciais
21
1.1 A associação entre a respiração oral e o crescimento dentofacial.
O equilíbrio das funções vitais exercidas pelo sistema estomatognático, dentre
elas a respiração nasal, é essencial para que haja o desenvolvimento
dentofacial normal, dentro dos padrões morfológico e genético de cada
indivíduo 7, 23.
Assim, a função naso-respiratória tem sido de grande interesse nas últimas
décadas, devido à sua relação biológica com a forma e a função, e também por
causa de sua enorme implicação clínica, para pediatras, otorrinolaringologistas,
alergologistas,
ortodontistas,
fonoaudiólogos,
fisioterapeutas
e
outros
profissionais da área de saúde que lidam com pacientes em fase de
crescimento 22.
Investigações sobre o impacto de fatores ambientais sobre o crescimento e o
desenvolvimento facial têm demonstrado uma associação entre a obstrução
das vias aéreas e variadas formas de más oclusões e displasias ósseas 3, 5, 9, 17,
20, 22
.
Em humanos, os estudos têm concentrado suas atenções no papel das formas
etiológicas mais incidentes de obstrução respiratória causadoras da respiração
oral: hiperplasia adenoideana, rinites alérgicas, hiperplasia amigdaliana,
hipertrofias de conchas nasais 3, 12, 18.
Por outro lado, trabalhos clássicos com primatas não humanos confirmaram
que a obstrução nasal severa à passagem de ar, artificialmente criada, pode
causar uma série de más oclusões. Apesar da resposta não ser uniforme entre
os animais, a abertura da boca para a realização da respiração oral
gradualmente resultou em um plano mandibular mais inclinado e um ângulo
goníaco mais aberto 8, 9, 10.
Tomes, em 1872, descreveu o termo “fácies adenoideana”, para indivíduos
respiradores orais. Nestes indivíduos, a boca permanece aberta, com falta de
selamento labial passivo. O lábio superior é curto, hipofuncionante e o lábio
22
inferior é evertido, hiperfuncionante. A musculatura jugal é relaxada, o nariz é
pequeno e pouco desenvolvido. A língua se posiciona inferior e anteriormente,
entre os incisivos superiores e inferiores. Os incisivos superiores são
projetados para vestibular. O olhar demonstra cansaço e a face apresenta uma
expressão atoleimada 26.
Espera-se, ainda, que os respiradores orais crônicos tenham uma atresia
maxilar, com tendência a um cruzamento no segmento posterior 3,20, um padrão
de crescimento facial vertical excessivo17, muitas vezes com uma mordida
aberta anterior e uma relação oclusal de classe II 22.
Apesar das características dentofaciais descritas acima serem aquelas que
vêm à mente da maioria dos profissionais da área de saúde, quando diante de
um paciente respirador oral, a literatura mostra que, do ponto de vista
epidemiológico, a “fácies adenoideana” típica não é o achado mais comum nos
pacientes respiradores orais. Alguns autores, inclusive, questionam a
associação entre o padrão respiratório e a morfologia facial 15.
Shapiro29 concluiu que, apesar do crescente volume de artigos científicos
demonstrando as relações entre a obstrução das vias aéreas superiores e o
crescimento facial, os clínicos deveriam ter cuidado na indicação de terapias
radicais ou na promessa de resultados ousados.
Alterações morfológicas isoladas (como o aumento da altura facial anterior
inferior e a atresia dos arcos) são bastante prevalentes em respiradores orais 3,
20
, enquanto que a relação sagital inter-arcos mais encontrada é a de classe I e
não a de classe II 11, 16.
O
crescimento
facial
verticalmente
excessivo
(dolicocefalia)
é
uma
preocupação para a Ortodontia, em virtude de suas implicações estéticas e
limitações terapêuticas mecânicas28. A hereditariedade é o fator etiológico
preponderante em relação à dolicocefalia31, todavia fatores ambientais, como a
respiração oral, podem contribuir com o agravamento deste padrão
desfavorável de crescimento 3, 5, 17.
23
Ricketts26 afirmou que a face dos respiradores orais cresce com excesso
vertical devido à rotação mandibular posterior favorecida pela manutenção da
boca aberta.
Apesar da controvérsia se a respiração oral é que causaria o excesso de
crescimento facial vertical ou se indivíduos com morfologia facial alongada
estariam mais susceptíveis à obstrução das vias aéreas superiores 30, 35, é fato
que existe uma forte associação entre os respiradores orais e uma face longa 5,
17
.
1.2 Normalização da respiração, após a desobstrução cirúrgica das vias
aéreas superiores, e o crescimento facial vertical.
Acreditando-se que a respiração oral favorece um crescimento facial excessivo
é possível teorizar que a normalização da função respiratória, após a
desobstrução cirúrgica das vias aéreas superiores, é capaz de promover uma
reversão, pelo menos parcial, deste padrão perverso de crescimento facial.
Diversas publicações descreveram o impacto positivo da adenoidectomia e do
aumento do fluxo de ar pelo nariz no crescimento facial vertical. Entretanto, a
maioria delas14,18,19,21,36 foi produto de um mesmo estudo longitudinal,
conduzido na Suécia na década de 1960, onde 38 crianças foram
acompanhadas por cinco anos e o crescimento comparado com o de indivíduos
sem obstrução respiratória.
Linder-Aronson18 relatou uma redução da divergência entre a maxila e a
mandíbula, decorridos 1 e 5 anos pós-adenoidectomia, enquanto que em
publicação subseqüente, o mesmo autor principal com co-participação de
outros
dois
pesquisadores19
descreveram um crescimento
mandibular
significativamente mais horizontal nas meninas e apenas uma tendência a este
padrão de rotação mandibular nos meninos, após a normalização do padrão
respiratório.
24
Kerr, McWilliam e Linder-Aronson14 estudaram a mudança de forma e
posicionamento espacial da mandíbula após a adenoidectomia, concluindo que
decorridos 5 anos da normalização da respiração oral o padrão esquelético das
crianças se tornou menos dolicocefálico. Eles concluíram que a mudança do
padrão respiratório influenciou a rotação mandibular, bem como a sua
morfologia.
Behlfelt2 estudou o efeito do aumento das amígdalas e da sua remoção
cirúrgica no crescimento facial. A amostra era composta por 73 crianças com
idade média de 10,1 anos. O pesquisador encontrou que crianças com
hiperplasia amigdaliana têm maior prevalência de retro-inclinação de incisivos
inferiores, protrusão de incisivos superiores, redução do comprimento da
arcada
inferior,
tendência
à
mordida
aberta
anterior,
aumento
da
sobressaliência e tendência ao cruzamento na região posterior. Na análise
esquelética, estas crianças mostraram ter maior prevalência de retrognatismo
mandibular e de rotação horária da mandíbula, aumento na altura facial anterior
inferior e mordida aberta. Após a remoção cirúrgica das amígdalas, houve um
reposicionamento dorsal da base da língua, favorecendo uma redução da
atresia mandibular e da prevalência de mordida cruzada posterior. Identificouse, também, um aumento da altura facial posterior inferior.
Woodside, Linder-Aronson e Lundstrom36 verificaram não haver diferenças na
direção do crescimento maxilar no grupo de crianças adenoidectomizadas, em
relação às crianças sem problemas respiratórios. O crescimento da sínfise
mandibular, expresso no queixo, foi maior no grupo de crianças operadas do
que no grupo controle normal.
Arun, Isik e Sayinsu1 investigaram retrospectivamente 66 teleradiografias em
norma lateral da face de crianças com história de adenoidectomia precoce (até
4 anos de idade) ou tardia (após 4 anos de idade). Nenhuma diferença
estatisticamente
significativa
foi
encontrada
nas
variáveis
esqueletais
estudadas, exceção feita à altura facial anterior. Eles concluíram que esta
investigação deveria ser considerada como um estudo piloto, sugerindo o
25
monitoramento longitudinal de crianças que forem precocemente submetidas à
adenoidectomia.
Mahoni, Karsten e Linder-Aronson21 tiveram como objetivo determinar se as
alturas
dentoalveolar
e
facial,
inicialmente
aumentadas
nas
crianças
respiradoras orais, são mantidas após a adenoidectomia. As comparações
feitas com um grupo de crianças respiradoras nasais, cinco anos após a
cirurgia, mostraram que a redução da altura dentoalveolar dos molares
superiores e da altura facial anterior inferior estão associadas à mudança do
padrão respiratório de oral para nasal.
Recentemente, Zettergren-Wijk, Forsberg e Linder Aronson37 publicaram os
seus achados em relação ao crescimento facial de 17 crianças submetidas à
adenoidectomia para o tratamento de Síndrome da Apnéia Obstrutiva do Sono
(SAOS). O padrão morfológico facial vertical das crianças portadoras de SAOS,
que antes da adenoidectomia era diferente daquele encontrado nas 17
crianças-controle, sem problemas respiratórios, adquiriu características de
semelhança 5 anos após sanado o problema obstrutivo.
Chama a atenção, consideração feita por Linder-Aronson, Woodside e
Lündstrom19 que, sob o ponto de vista puramente científico, seria preferível ter
uma amostra controle obstruída, ao invés de composta por crianças sem
obstrução naso-respiratória. Entretanto tal desenho metodológico, segundo
estes autores, teria limitações éticas.
Exceção feita ao estudo de Arun, Isik e Sayinsu1, em todos os artigos citados
anteriormente, pelas crianças estarem na mesma faixa etária (dentadura
mista), nenhuma inferência foi feita a respeito do momento ideal para a
adenoidectomia.
26
1.3 Adeno-/tonsilectomia na desobstrução das vias aéreas superiores:
existe uma época ideal?
A tonsilectomia tem sido utilizada como procedimento cirúrgico há muito tempo.
Em 50 a.c., Celsus já havia descrito uma técnica para tal operação. Já a
adenoidectomia, por outro lado, provavelmente não havia sido executada até o
final do século XIX, quando Wilhelm Meyer sugeriu que as vegetações
adenoideanas eram responsáveis não somente pelos sintomas nasais, mas
também pela perda de audição 6.
As duas cirurgias conjuntamente começaram a ser empregadas de maneira
cada vez maior no início do século XX, quando a então popular teoria da
infecção focal indicava que vários distúrbios sistêmicos, com destaque para o
“reumatismo” eram causados pela doença das amígdalas e adenóide 24.
De forma exagerada, entusiastas inclusive indicavam A+A como tratamento
para condições diversas como anorexia, retardo mental, enurese ou
simplesmente como medida de promoção de saúde 24.
Talvez o apogeu do entusiasmo com a A+A tenha acontecido, em algumas
comunidades, onde cirurgias por atacado nas populações infantis aconteciam
nas próprias escolas públicas 6.
Após essa fase de indicações excessivas, iniciou-se a fase de contestação com
a quase proibição da realização desta cirurgia. O ceticismo na indicação de
A+A em larga escala começou a ser progressivamente maior na década de
1930, recebendo reforço positivo a medida que 1) os estudos epidemiológicos
indicavam uma redução natural na incidência de infecções do trato respiratório
superior, após os primeiros anos de vida escolar, 2) o reconhecimento, no
período que antecedeu o surgimento de uma vacina eficaz contra a
poliomielite, que crianças submetidas a A+A tinham maior risco de desenvolver
esta doença, 3) surgiram novas drogas antimicrobianas eficazes contra as
bactérias envolvidas com as infecções respiratórias e 4) um número
27
considerável de estudos eram publicados confirmando que a A+A era
ineficaz24.
O preconceito em relação a A+A, particularmente no meio pediátrico, surgiu e
até mesmo ficou exagerado pelas freqüentes indicações inadequadas 24.
Durante os anos de 1950, um importante programa de saúde norte americano
(United Mine Workers of America Health and Retirement Funds), na esperança
de melhorar a qualidade de atenção e também reduzir custos, instituiu a norma
de exigir uma avaliação e consentimento prévio de peritos credenciados, em
relação a A+A 24.
Ao final dos anos 1960, uma considerável parcela dos livros-texto de pediatria
questionava as indicações de amigdalectomia, enquanto uma revisão cética de
um conceituado periódico denominou esta intervenção de “ritual cirúrgico” 24.
Em 1976, uma sugestão foi feita propondo que A+A fosse completamente
suspenso, até que sua eficácia pudesse ser estabelecida em ensaios clínicos
controlados 24.
Não bastasse este ambiente, que variava entre o ceticismo e condenação, o
apoio a A+A continuou a existir em vários segmentos da área médica. Estudos
que indicaram a associação entre a obstrução das vias aéreas superiores e as
alterações no crescimento dentofacial contribuíram com o incentivo à
continuidade desta técnica cirúrgica18.
Atualmente, vivemos a fase de análise de resultados e indicações mais
criteriosas, baseadas em estudos científicos, porém o estigma da cirurgia ainda
permanece entre alguns profissionais, especialmente da área de Pediatria.
Sob o olhar da Ortodontia, o adiamento da normalização do padrão
respiratório, no caso de crianças respiradoras orais, não parece ser uma
conduta desejável, por pelo menos duas razões: 1) a respiração oral pode ser
um fator etiológico de más oclusões e a persistência de tal interação
28
fisiopatológica tende a agravar as seqüelas dentofaciais
26,27
, 2) a maior parte
4
do crescimento facial acontece nos primeiros anos de vida .
Entretanto quem geralmente define a época de uma intervenção cirúrgica para
a normalização da respiração oral é o médico pediatra. Como, por questões
históricas, alguns destes profissionais tendem a recomendar o adiamento da
A+A, tal situação é preocupante, uma vez que, até a presente data, não há um
relato de estudo clínico controlado para definir a idade limítrofe para a
normalização do padrão respiratório, nos casos de obstrução das vias aéreas
superiores, sob uma perspectiva ortodôntica, especialmente em relação ao
padrão de crescimento facial vertical.
Ao mesmo tempo, acredita-se, empiricamente, que a opinião destes
profissionais é, muitas vezes, discordante dos otorrinolaringologistas apesar de
haver estudos que demonstrem o contrário 25.
29
1.4 Objetivo da tese
Diante dos fatos expostos anteriormente, o objetivo desta tese foi avaliar se as
expectativas apresentadas a seguir, relacionadas à associação entre a
respiração oral e o complexo dentofacial, correspondem à realidade. Ou seja, o
que esperamos é o que encontramos?
Expectativa 1: A maioria das crianças respiradoras orais é portadora de má
oclusão de classe II, mordida aberta anterior e mordida cruzada posterior,
sendo que a gravidade da obstrução das vias aéreas superiores tem
associação com estas más oclusões.
Expectativa 2: A desobstrução cirúrgica das vias aéreas superiores de
respiradores orais, durante a fase de dentadura decídua, propicia um
crescimento facial vertical mais favorável do que quando realizada durante a
fase de dentadura mista.
Expectativa 3: A desobstrução cirúrgica das vias aéreas superiores em
respiradores orais propicia um crescimento facial vertical mais favorável do que
em crianças obstruídas.
30
1.5 Referências Bibliográficas
1
Arun T, Isik F, Sayinsu K. Vertical growth changes after adenoidectomy.
Angle Orthod. 2003; 73:146-150.
2
Behlfelt K. Enlarged tonsils and the effect of tonsillectomy: characteristics
of the dentition and facial skeleton posture of the head, hyoid hone and
tongue; mode of breathing. Swed Dent J 1990; suppl 72:5-35.
3
Bresolin D, Shapiro PA, Shapiro GG, Chapko MK, Dassel S. Mouth
breathing in allergic children: Its relationship to dentofacial development.
Am J Orthod. 1983; 83:334-40.
4
Casselbrant ML. What is wrong in chronic adenoiditis/tonsillitis anatomical
considerations. Int J Ped Otorhinol. 1999;49:S133-S135.
5
Cheng MC, Enlow DH, Papsidero M, Broadbent Jr BH, Oyen O, Sabat M.
Developmental effects of impaired breathing in the face of the growing
child. Angle Orthod. 1988; 58:309-320.
6
Deutsch ES. Tonsillectomy and adenoidectomy. Changing indications.
Pediatr Clin North Am. 1996; 43:1319-38.
7
Enlow DH. Crescimento facial. 3 ed. São Paulo: Artes Médicas. 553p.
1993.
8
Harvold EP, Chierici G, Vargervik K. Experiments on the development of
dental malocclusions. Am J Orthod. 1972; 61:38-44.
9
Harvold EP, Tomer BS, Vargervik K, Chierici G. Primate experiments on
oral respiration. Am J Orthod. 1981; 79:359-372.
10 Harvold EP, Vargervik K, Chierici G. Primate experiments on oral sensation
and dental malocclusions. Am J Orthod. 1973; 63:494-508.
11 Howard CC. Inherent growth and its influence on malocclusion. J Am Dent
Assoc. 1932; 19:642-648.
12 Hulcrantz E, Larson M, Hellquist T, Ahqvist-rastad J, Jakobsson OP. Int J
Ped Otorhinolaryngol. 1991; 22:125-34.
13 Karlsen AT. Craniofacial growth differences between low and hogh MP-SN
angle males: a longitudinal study. Angle Orthod. 1995; 65:341-350.
14 Kerr JS, McWilliam JS, Linder Aronson S. Mandibular form and position
related to changed mode of breathing – a five-year longitudinal study.
Angle Orthod. 1989; 59:91-96.
31
15 Kluemper GT, Vig PS, Vig KW. Nasorespiratory characteristics and
craniofacial morphology. Eur J Orthod. 1995; 17:491-495.
16 Leech HL. A clinical analysis of orofacial morphology and behavior of 500
patients attending an upper respiratory research clinic. Dent Pract. 1958; 9:
57-68.
17 Lessa FCR, Enoki C, Feres MFN, Valera FCP, Lima WTA, Matsumoto
MAN. Breathing mode influence in craniofacial development. Braz J
Otorhinol. 2005; 71:156-60.
18 Linder-Aronson S. Effects of adenoidectomy on dentition and facial
skeleton over a period of five years. In: Cook JT (ed) Transactions of the
Third International Orthodontic Congress. St Louis: The CV Mosby
Company, 1975; 85-100.
19 Linder-Aronson S, Woodside DG, Lundström A. Mandibular growth
direction following adenoidectomy. Am J Orthod Dentof Orthop. 1986;
89:73-284.
20 Lofstrand-Tideström B, Thilander B, Ahlqvist-Rastad J, Jakobsson O,
Hultcrantz E. Breathing obstruction in relation to craniofacial and dental
arch morphology in 4-year-old children. Eur J Orthod. 1999; 21:323-332.
21 Mahony D, Karsten A, Linder Aronson S. Effects of adenoidectomy and
changed mode of breathing on incisor and molar dentoalveolar heights and
anterior face heights. Aust Orthod J. 2004; 20:93-98.
22 McNamara JA. Influence of respiratory pattern on craniofacial growth.
Angle Orthod. 1981; 81:269-300.
23 Moss-Salentijn L. Melvin L. Moss and the functional matrix. J Dent Res.
1997; 76:1814-1817.
24 Paradise JL. Tonsillectomy and adenoidectomy. In: Bluestone CD, Alper
CM, Stool SE, Arjmand EM. Pediatric otolaryngology. Chapter 61. Vol 2.
4th ed. Philadelphia: Saunders; 2003:1210-1222.
25 Pirara S, Bento RF, Camas J. Consensos e controvérsias nas indicações
de adenoamigdalectomia entre pediatras e otorrinolaringologistas. Braz J
Otorhinol. 1999; 65:308-315
26 Ricketts RM. Respiratory obstruction syndrome. Am J Orthod. 1968;
54:495-514.
27 Ricketts RM. Respiratory obstructions and their relation to tongue posture.
32
Cleft Palate Bulletin. 1958;8:4-5 (abstract) cited by Linder Aronson S.
Effects of adenoidectomy on dentition and facial skeleton over a period of
five years. In: Cook JT (ed) Transactions of the Third International
Orthodontic Congress. St Louis: The CV Mosby Company, 1975; 85-100.
28 Schudy FF. The rotation of the mandible resulting from growth: its
implications in orthodontic treatment. Angle Orthod. 1965; 35:36-50.
29 Shapiro PA. Effects of nasal obstruction on facial development. J Allergy
Clin Immunol. 1988; 81: 967-71.
30 Smith RM, Gonzales C. The relationship between nasal obstruction and
craniofacial growth. Ped Clin of North America. 1989; 36:1423-34.
31 Soares JF, Siqueira AL. Introdução à estatística médica. Belo Horizonte:
Coopmed Editora Médica, 2 ed., 2002. 300p.
32 Sparks CS, Jantz RL. A reassessment of human cranial plasticity: Boas
revisited. Proc Nat Acad Sciences. 2002; 99:14636-14639.
33 Tollaro I, Baccetti T, Franchi L. Mandibular skeletal changes induced by
early functional treatment of class III malocclusion: a superimposition study.
Am J Orthod Dentof Orthop.1995; 108:525-532.
34 Wang MK, Buschang PH, Behrents R. Mandibular rotation and remodeling
changes during early childhood. Angle Orthod. 2009; 79:271-275.
35 Warren DW. Effect of airway obstruction upon facial growth. Otolaryngol
Clin North America. 1990; 23:699-712.
36 Woodside DG, Linder Aronson S, Lundström, A. Mandibular and maxillary
growth after changed mode of breathing. Am J Orthod Dentof Orthop.
1991; 100:1-18.
37 Zettergren-Wijk L, Forsberg CM, Linder Aronson S. Changes in dentofacial
morphology after adeno-/tonsillectomy in young children with obstructive
sleep apnoea – a 5-year follow-up study. Eur J Orthod. 2006; 28:319-326.
33
CAPÍTULO 2
Artigos
34
Artigo 1
Título: Prevalence of malocclusion among mouth breathing children: do
expectations meet reality?
Autores: Bernardo Q. Souki, Giovana B. Pimenta, Marcelo Q. Souki, Leticia P.
Franco, Helena M. G. Becker and Jorge A. Pinto.
Revista: International Journal Pediatric Otorhinolaryngology
35
Artigo 1
Prevalence of malocclusion among mouth breathing children: do
expectations meet reality?
a,b
Bernardo Q. Souki , Giovana B. Pimentaa, Marcelo Q. Soukia, Leticia P.
Francoa, Helena M. G. Beckera and Jorge A. Pintoa
a
Federal University of Minas Gerais, Outpatient Clinic for Mouth-Breathers, Belo
Horizonte, Brazil
b
Catholic University of Minas Gerais, School of Dentistry, Orthodontics, Belo
Horizonte, Brazil
Keywords: Mouth breathing, malocclusion, adenoids, tonsils, rhinitis
Abstract
Objective: The aim of this study was to report epidemiological data on the
prevalence of malocclusion among a group of children, consecutively admitted
at a referral mouth breathing otorhinolaryngological (ENT) center. We assessed
the association between the severity of the obstruction by adenoids/tonsils
hyperplasia or the presence of allergic rhinitis and the prevalence of class II
malocclusion, anterior open bite and posterior crossbite.
Methods: Cross-sectional, descriptive study, carried out at an Outpatient Clinic
for Mouth-Breathers. Dental inter-arch relationship and nasal obstructive
variables were diagnosed and the appropriate cross tabulations were done.
Results: Four hundred and one patients were included. Mean age was 6 years
and 6 months (SD: 2y7m), ranging from 2 to 12 years. All subjects were
evaluated by otorhinolaryngologists to confirm mouth breathing. Adenoid/tonsil
obstruction was detected in 71.8% of this sample, regardless of the presence of
rhinitis. Allergic rhinitis alone was found in 18.7% of the children. Non
obstructive mouth breathing was diagnosed in 9.5% of this sample. Posterior
crossbite was detected in almost 30% of the children during primary and mixed
dentitions and 48% in permanent dentition. During mixed and permanent
dentitions, anterior open bite and class II malocclusion were highly prevalent.
More than 50% of the mouth breathing children carried a normal inter-arch
relationship in the sagital, transversal and vertical planes. Univariate analysis
showed no significant association between the type of the obstruction
36
(adenoids/tonsils obstructive hyperplasia or the presence of allergic rhinitis) and
malocclusions (class II, anterior open bite and posterior crossbite).
Conclusions: The prevalence of posterior crossbite is higher in mouth-breathing
children than in the general population. During mixed and permanent dentitions,
anterior open bite and class II malocclusion were more likely to be present in
mouth breathers. Although more children showed these malocclusions, most
mouth breathing children evaluated in this study did not match the expected
“mouth breathing dental stereotype”. In this population of mouth breathing
children, the obstructive size of adenoids or tonsils and the presence of rhinitis
were not risk factors to the development of class II malocclusion, anterior open
bite or posterior crossbite.
1 Introduction
The association between nasal respiratory impairment and dento-facial
morphology has been studied for more than a century
[1-3]
and for decades it
has been strongly accepted that inter-arch growth pattern can be influenced by
an unbalanced muscular function on mouth breathers [4].
The knowledge that obstruction of nasal breathing most likely will perversely
impact the facial growth even led some authors to propose classic terms to
describe such patients as “adenoid faces”
“respiratory obstruction syndrome”
[7]
[5]
, “long face syndrome”
[6]
and
.
A stereotype of these patients, therefore, can be drawn, where an anterior open
bite
[8]
, a reduced transversal dimension
[9,10]
, associated or not with posterior
crossbite [11], and a class II malocclusion [12, 13,14] are expected.
However, as individual facial genotypes have different sensitivity on developing
malocclusion, following the exposure to mouth breathing, a wide variety of interarch relationships can be found.
The emphasis on this mouth breathing stereotype has been unfortunate
because it implies that all patients with those clinical findings are mouth
37
breathers and that nasal impaired respiration will ultimately result in this
malocclusion. Besides that, one question arises: can we predict the outcome of
these malocclusions based on the presence and on the type of airway
obstructive cause which led to this deleterious habit?
Routinely, Ear, Nose and throat (ENT) specialists and general clinicians use the
diagnosis of the airflow blockage by adenoids and tonsils hyperplasia as a
parameter to the establishment of the treatment planning
[15]
. Although this
axiom has been used routinely by clinicians, it has not been sufficiently tested
regarding the development of malocclusion.
The aim of this study was to report epidemiological data on the prevalence of
malocclusion among a group of children, consecutively admitted at a referral
mouth breathing ENT center. We assessed the association between severity of
the obstruction by adenoids/tonsillar hyperplasia or the presence of allergic
rhinitis and the prevalence of class II malocclusion, anterior open bite and
posterior crossbite.
2 Patients and methods
2.1 Population
Four hundred and forty four children consecutively referred by pediatricians and
primary care physicians to the Outpatient Clinic for Mouth-Breathers, at the
Hospital das Clínicas at Federal University of Minas Gerais (UFMG), Brazil,
between November of 2002 and November of 2007, with the chief complaint of
mouth breathing were systematically evaluated by a multidisciplinary team
comprised by ENT doctors, allergologists and orthodontists, in a single day visit.
Children whose mouth breathing could not be confirmed, those who have had
previous orthodontic treatment or were younger than 2 years of age were
excluded from the analysis. Therefore, the sample of this cross-sectional study
totaled 401 patients.
38
All subjects were evaluated by otorhinolaryngologists to confirm mouth
breathing resulting from at least one of the following airway pathologies:
obstructive tonsillar hyperplasia, obstructive adenoidal hyperplasia and allergic
rhinitis. The children whose obstruction by one of these conditions could not be
diagnosed were classified as functional mouth breathers [16].
The participant’s rights were protected, and informed consent and assent were
obtained according to the Ethics Committee of the Federal University of Minas
Gerais.
2.2 ENT data collection
An interview with children’s parents, or guardians, asking about the quality of
the children’s sleep, snoring, oral breathing and throat infections, confirmed the
“chief complaint” of mouth breathing. Parents were also asked if the child had
been undergone an adenoidectomy or tonsillectomy earlier. Clinical ENT
examination was performed by two of the authors (L.F. and H.B.), according to
the following guidelines:
Palatine tonsil hypertrophy was classified by mouth examination according to
the criteria of Brodsky and Koch
[17]
as follows: grade 0 – tonsils limited to the
tonsillar fossa; grade 1 – tonsils occupying up to 25% of the space between the
anterior pillars in the oropharynx; grade 2 – tonsils occupying 25-50% of the
space between the anterior pillars; grade 3 – tonsils occupying 50-75% of the
space between the anterior pillars; and grade 4 – tonsils occupying 75-100% of
the space between the anterior pillars.
Tonsils grade 0, 1 and 2 were considered as non-obstructive and those
classified as grade 3 and 4 were named as obstructive. [18]
Adenoids were assessed by flexible nasoendoscopy and were grouped into two
categories based on nasopharyngeal obstruction (<75% and ≥75%). A cut-point
of 75% was chosen to classify the blockage of the nasopharynx as obstructive
or non-obstructive. [19]
39
2.3 Allergological data collection
The allergological assessment, to diagnose allergic rhinitis, included a
structured medical interview, physical examination, following the standard volar
forearm skin prick method, as described elsewhere[20]. These exams were
performed in 326 children under the supervision of one of the authors (J.P).
2.4 Dental data collection
The dental clinical examination was performed by a team of orthodontists, who
worked together for at least ten years, and were previously calibrated. The
subjects were grouped by stage of dental development, according to the
variation in primary and permanent teeth eruption, into deciduous, mixed and
permanent periods.
The inter-arch occlusion dental classification was based on Barnett [21]:
Vertical: relationship was classified as 1) normal, 2) anterior open bite or 3)
deep bite. An open bite was registered in cases that lacked any overbite,
regardless of the amount. A deep bite was registered when more than half of
the lower incisors were overlapped by the incisal edges of the upper incisors.
Transversal: relationship was classified as 1) normal, 2) posterior crossbite,
without mandibular functional shift, and 3) posterior bite, with mandibular
functional shift.
Sagital: relationship was classified as a) normal occlusion, b) class I
malocclusion, c) class II malocclusion and c) class III malocclusion. During the
deciduous and mixed dentitions, it was considered a class I dental relationship
when the upper deciduous cuspid intercuspation was set between the lower
deciduous cuspid and first deciduous molar. When in permanent dentition the
Angle classification was followed.
2.5 Dental data comparison
A large number of studies on the prevalence of malocclusion in different
40
populations have been published. These data served as a reference of what
should be the distribution on inter-arch anomalies among a general population,
where mouth and nasal breathers were sampled together [28-32, 35-41].
2.6 Statistics
Epi-data was used to enter data. SPSS version 12.0 was used for the analysis.
Descriptive statistics and univariate analysis in cross tables are showed. The
significance level of p<0.05 was chosen. Normality of age distribution was
tested using Kolmogorov-Smirnov test.
For each dental and ENT variable, the number of children with the diagnosed
status (n) and its prevalence (%) are given.
For the purpose of statistical analysis, dental variables were binarily grouped
according to the expected inter-arch relationships in mouth breathing subjects.
Therefore the dependent variables examined were class II malocclusion,
anterior open bite and posterior crossbite.
The independent ENT variables were the obstructive grade of tonsil and
adenoids and the presence of rhinitis.
3 Results
The mean age of this sample was 6 years and 6 months and the standard
deviation was 2 years and 7 months. The age of the children ranged between 2
and 12 years. With the exception of 38 children (9.5%), whose mouth breathing
was due to functional habit, 363 subjects had an objective airway obstructive
factor. Of these children, 288 (71.8%) were judged to have tonsil and/or
adenoid obstruction, combined or not with rhinitis. Allergic rhinitis, as the only
obstructive cause, was found in 75 children (18.7%).
Table 1 shows the prevalence of the studied variables, by gender. As there was
no gender statistically difference (p > 0.05), the analysis was done considering
41
boys and girls as a single group.
Table 1 – Prevalence of dental and ENT findings according to gender
distribution. Number of children (n) and prevalence given in percentage (n/N x
100%).
Variables
Boys
n
%
Stage of development
N=401
Deciduous dentition
106
Mixed dentition
110
Permanent dentition
12
χ2 = 6.050 (2 df) p value = 0.05
Sagital relationship
N=384
Normal occlusion
26
Class I malocclusion
97
Class II malocclusion
64
Class III malocclusion
30
χ2 = 2.230 (3 df) p value = 0.526
Vertical relationship
N=385
Normal
115
Deep bite
38
Open bite
67
χ2 = 2.349 (2 df) p value = 0.309
Transversal relationship
N=392
Normal
158
Posterior crossbite w/o
31
shift
Posterior crossbite w shift
32
χ2 = 1.631 (2 df) p value = 0.443
Tonsils status
N=399
Grades 0, I, II
141
Grades III, IV
86
χ2 = 1.918 (1 df) p value = 0.166
Adenoid obstruction status
N=390
<75%
95
≥ 75%
124
χ2 = 0.235 (1 df) p value = 0.628
Rhinitis
N=326
Yes
133
No
51
χ2 = 0.008 (1 df) p value = 0.928
Girls
Total
n
%
n
%
26.4
27.4
3.0
60
99
14
15.0
24.7
3.5
166
209
26
41.4
52.1
6.5
6.8
25.3
16.7
7.8
17
83
51
16
4.4
21.6
13.3
4.2
43
180
115
46
11.2
46.9
29.9
12.0
29.9
9.9
17.4
98
21
46
25.5
5.5
11.9
213
59
113
55.3
15.3
29.4
40.3
7.9
116
22
29.6
5.6
274
53
69.9
13.5
8.2
33
8.4
65
16.6
35.3
21.6
95
77
23.8
19.3
236
163
59.1
40.9
24.4
31.8
70
101
17.9
25.9
165
225
42.3
57.7
40.8
15.6
102
40
31.3
12.3
235
91
72.1
27.9
As seen in Table 1, the majority of the children was within the deciduous
(41.4%) or mixed (52.1%) dentitions. In this growth period of their lives, they
42
were susceptible to the unbalanced muscular adaptation to mouth breathing.
Only few children (6.5%) were in permanent dentition.
Based on Table 1, 58.1% of the sample had a normal sagital relationship (class
I dental relationship). Class I malocclusion was found in 46.9% of these
children, the other 11.2% represents the normal occlusion children. Regarding
the three stages of occlusal development (Table 2), Class I dental relationship
was found in 64.2% during deciduous dentition, 53.8% and 54.2% during mixed
and permanent dentitions, respectively.
About 42% of this sample presented with a sagital disharmony, represented by
class II or III (Table 1). The prevalence of class III gets higher as kids get older
(Table 2).
Considering the 384 children whose sagital classification was done, dental
Class II was the sagital relationship of 27% during primary dentition, 32.8% on
mixed dentition and 25% on permanent dentition (Table 2).
The vertical inter-arch relationship must be studied in the dental stage of
development because of its known physiologic difference along the growing
period. Nevertheless, Table 2 brings the information that a normal vertical
relationship was found in, at least, 52.7% of the sample, regardless of the
dental stage of development. Open bite prevalence was around 30% during the
deciduous and mixed dentitions and 20% in permanent dentition.
In the transversal analysis, posterior crossbite was detected in close to 30% of
the kids during deciduous and mixed dentitions and 48% in permanent dentition
(Table 2).
All comparisons in Table 2 demonstrate that there is no difference in the
malocclusion occurrence when comparing the three stages of dental
development (p values >0.05).
43
Table 2- Prevalence of dental and ENT findings in the deciduous. mixed and
permanent dentitions. Number of children (n) and prevalence given in
percentage (n/N x 100%).
Variable
Deciduous
Dental
Sagital relationship
N=384
Normal occlusion
Class I malocclusion
Class II malocclusion
Class III malocclusion
χ2 p value = 0.196
Vertical relationship
N=385
Normal
Deep bite
Open bite
χ2 p value = 0.731
Transversal relationship
N=392
Normal
Posterior crossbite
w/o shift
Posterior crossbite w
shift
χ2 p value = 0.314
ENT
Tonsils status
N=399
Grades 0, I, II
Grades III, IV
χ2 p value = 0.005
Adenoid obstruction status
N=390
< 75%
≥ 75%
χ2 p value = 0.000
Rhinitis
N=326
Yes
n
159
%
24
78
43
14
15.1
49.1
27.0
8.8
165
87
27
51
Mixed
n
201
Permanent
%
19
89
66
27
n
24
9.5
44.3
32.8
13.4
195
52.7
16.4
30.9
164
%
1
12
6
5
4.2
50.0
25.0
20.8
15
5
5
60.0
20.0
20.0
25
111
27
57
56.9
13.8
29.2
203
25
118
19
72.0
11.6
143
29
70.4
14.3
13
5
52.0
20.0
27
16.5
31
15.3
7
28.0
20
6
76.9
23.1
20
4
83.3
16.7
20
1
95.2
4.8
165
83
82
208
50.3
49.7
161
43
118
63.9
36.1
205
26.7
73.3
137
79
58
133
75
26
102
103
24
49.8
50.2
168
57.7
42.3
136
32
21
81
19
No
χ2 p value = 0.000
Note: χ2 based on n x 3 tables. n = variable
Regarding the tonsils (Table 1), the more obstructing grades (3 and 4) were
found in about 40.9% of the kids, but considering the stratified groups by age
(Table 2), kids during early stages (deciduous dentition) had a higher
prevalence (49.7%) than latter stages (36.1% and 23.1% during mixed and
permanent dentitions, respectively). Table 2 also illustrates that the distribution
44
of tonsillar obstruction shifted according to aging. Children during the deciduous
dentition stage of development have more obstructive tonsils than older ones
(p<0.05).
The adenoid’s obstruction of the nasopharynx showed similar epidemiological
behavior. Although the average prevalence of the obstructive group (≥75%
occupation of nasopharynx space) was 57.7%, (Table 1), when analyzing this
variable under the perspective of dental stage of development, it is clear that
prevalence declines steeply from 73.3% to 16.7% along the aging (Table 2),
with statistically significant difference (p<0,05).
The overall prevalence of allergic rhinitis was 72.1% (n=235/326), as
demonstrated on Table 1. During mixed and permanent dentitions the
proportion of subjects with rhinitis was bigger (81% and 95.2%, respectively)
than in deciduous dentition 57.7% (Table 2), a statistically significant difference
(p<0.05).
Table 3 shows the univariate analysis between grouped malocclusion
(dependent variable) and the ENT independent variables. No association was
found between the expected type of malocclusion for mouth breathers and the
presence of variables that obstruct the nasal airflow (p>0.05).
The comparison between our findings and the literature inter-arch prevalence
data is done in the discussion section.
45
Table 3 – Univariate analysis between grouped malocclusion (dependent
variable) and the obstructive causes for mouth breathing (independent
variables).
Variables
Tonsil/adenoid
obstruction
Rhinitis only
No obstructive
cause diagnosed
p value
78
196
24
49
13
24
0.589
79
198
24
48
10
26
0.710
85
197
26
48
7
29
0.242
Class II
malocclusion
Yes
No
Anterior open
bite
Yes
No
Posterior
crossbite
Yes
No
4 Discussion
Several reports have associated mouth breathing with dental malocclusion. The
first papers were limited to clinical impressions of dentistry pioneers who related
the disturbance on facial and occlusal harmony to the impairment of nasal
breathing in their patients. Later, many papers published reports based on the
findings of scientific data collection, mostly considering the skeletal outcome
evaluated by cephalometry. However, data on occlusal clinical parameters of
mouth breathing children are scarce.
Dental inter-arch relationship, in the three planes of space, is the basic clinical
parameter in understanding the patient’s occlusion and its behavior when
exposed to unbalanced muscular activity. Therefore, it is important to assess
the occurrence of occlusal disorders among mouth breathing children.
Despite the large sample size of this study, the limitations of a cross-sectional
design needs to be considered. As our sample is comprised only of mouth
breathers, the prevalence of dental inter-arch status had to be compared with
other epidemiological reports on a general population
[28-32,
35-41]
. This
methodology brings at least two biases: 1) it is fact that in a general population
46
a significant number of children are mouth breathers
[22-24]
. Thus, the difference
between the prevalence of malocclusion in this mouth breathing population and
a “normal breathing” population would be greater. 2) The reported prevalence
varies considerably between the different studies, even among the same
population. This divergence in prevalence figures may depend not only on
differences for specific ethnic groups [25], but also on wide ranges in number and
age among the examined subjects. However, differences in registration
methods, i.e. the criteria for the recorded items, are probably the most important
factor explaining these differences. Despite these methodological limitations,
this study brings results that deserve further discussion.
Our study compared the prevalence of only one malocclusion in each plane of
space: class II (sagital), anterior open bite (vertical) and posterior crossbite
(transversal), since an occlusal pattern for mouth breathers is well described.
Anomaly studies usually report findings by chronological age. Malocclusion,
however, is a manifestation that is related to development of the dentition.
Given the great individual variations in dental maturation, it seems logical to
determine the prevalence of malocclusion for groups at different stages of
dental development, rather than for different age groups. It is interesting to point
out that the pattern of distribution of the prevalence of malocclusions does not
show any statistical difference among the three stages of dental development
(Table 2), as it occurs in the general population
[26]
. It is expected that the
prevalence of each malocclusion changes among the growth period. This fact
suggests that in a mouth breathing population, the increase in the prevalence of
some malocclusions alter the common pattern.
Regarding the sagital relationship, it is known that race impacts significantly the
prevalence of classes I, II and III malocclusions
[27]
. Therefore, a good
comparison is made only with Brazilian data. This was possible in the first two
stages of dental development. During primary dentition, the prevalence of class
II in our mouth breathing group was 27%. The prevalence found in previous
publications in Brazil varies between 6.8% and 30%
[28-30].
Our findings are quite
similar to a large sample study (n=2139) conducted by Tomita et al.
[28]
.
47
However our prevalence is higher than found in other studies
al.
[29]
[29, 30]
. Kataoka et
concluded that the prevalence of class II in their sample was low (6.8%)
because their population was comprised only by Japanese-Brazilian ethnic
children. This fact, explains the difference between our findings. However, the
difference in relation to the results found by Sadakyio et al.
[30]
(15.6%) can be
justified by data collection methodology discrepancies or differences due to
mouth breathing.
In mixed dentition, our study's class II prevalence (32.8%) is much higher than
the 12.5% reported by Zanetti
[31]
. This significant discrepancy suggests that in
older children, the perverse impact of mouth breathing, on sagital inter-arch
development, is greater than on the deciduous dentition. Cheng et al.
[11]
noted
that the younger a subject is, at the time of evaluation, the less the “adenoid”
type of facial characteristics is expressed. This opinion corroborates our
findings. We can hypothesize that the longer the exposure to the unbalanced
muscular function, due to mouth breathing, the greater the risk of developing
class II malocclusion. More epidemiological reports on sagital relationship
during the mixed dentition stage would be helpful in testing this hypothesis, but
only one was found. Longitudinal cohort studies are necessary to test if this
hypothesis is correct.
During permanent dentition, the prevalence of class II in this sample was 25%.
A comparison with Brazilian data was not possible because no epidemiological
study involving general population at this stage was found, regarding this type
of malocclusion. Comparing to Horowitz
[32]
, who evaluated American subjects,
the prevalence numbers (22.5%) are quite similar to our results. This
observation corroborates the conclusions of Howard
McNamara
[3]
[33]
, Leech
[34]
and
. Nevertheless, comparing our permanent dentition class II
findings with the classic study of Emrich, Brodie, Blayney [35], also in the United
States, who found 14%, our prevalence was higher. As the size of permanent
dentition sample, in our study, was small (n=24), we suggest that other studies,
with larger samples, should test this association.
Regarding the vertical inter-arch relationship, the same type of association
48
described to class II was found. Compared to the literature data, the prevalence
of open bite during deciduous dentition, in the investigated mouth breathers,
was quite similar. While our children’s anterior open bite prevalence during
deciduous dentition was 30.9%, the revised literature on general population
varied between 20.6% and 46.3%
[28, 44-46]
. But, when analyzing the older
children (mixed dentition), an important difference was noted. The prevalence of
open bite reported in the reference articles
[31, 36-39]
varies between 12.00% and
20.1%, while our sample had a prevalence of 29.2%.
In the transverse dimension we found the most significant discrepancy in the
prevalence of malocclusion. Dental literature data shows that the prevalence of
posterior crossbite ranges from 8% to 22%
(40)
. Prevalence studies on posterior
crossbite during permanent dentition are rare, but Thilander et al.
[41]
found a
prevalence of 3.9% during this stage. Therefore we considered 22% as the top
value. We found a prevalence of 30.1% of posterior crossbite in whole group.
This prevalence of close to 30% in the primary and mixed dentitions and almost
50% in the permanent one is higher than in the general population and
deserves additional consideration.
As the etiology of malocclusion has singular characteristics when considering
the three different planes of space, this heterogeneity can help with the
comprehension of our findings.
Sagital dental inter-arch relationship is mostly determined by heredity
[27]
and
therefore mouth breathing is only a secondary etiological factor to class II
development. Most likely, the power of the unbalanced muscular activities, due
to mouth breathing, is not enough to shift a solid class I or III patterns into a
class II. Maybe those children with a tendency toward a class II, who could
growth into class I, depending on environmental factors, are the population
candidates who develop class II, when exposed to mouth breathing. Therefore,
in an epidemiological analysis, as we did, the prevalence of class II is higher
than in the general population, especially in older children.
Vertical dental relationship also has heredity as the major determinant, but
49
environmental factors such as non-nutritious sucking habits and mouth
breathing work as secondary causes of anterior open bite [42]. During deciduous
dentition, when sucking habits are highly prevalent in Brazil
[43]
, the prevalence
of anterior open bite found in our sample of nasal impaired children was within
the range cited in previous Brazilian studies
[40-42]
. However, during mixed and
permanent dentitions, as these sucking habits decline in the general population,
the difference with our data gets bigger.
The transversal dental relationship, although governed by individual facial
genotype [47], suffers greatly from environmental perverse factors
al.
[48]
[40]
. Mocellin et
, found 63.3% of palatal constriction in mouth breathers and 5% in nasal
breathers. This fact explains why the discrepancy in the prevalence of posterior
crossbite was so significant between the mouth breathers and the general
population. As ethnic difference does not influence posterior crossbite
[25]
, the
comparison with data from other studies is feasible.
The triad of class II malocclusion, anterior open bite and posterior crossbite,
despite showing a higher prevalence in a mouth breather sample than in the
general population, is not the most prevalent inter-arch relationship among the
studied nasal impaired children. In fact, a significant number of children showed
a normal occlusion, even growing with this perverse habit.
It is clear that mouth breathing is capable of adding an environmental weight to
the etiology of such malocclusions. However, since heredity plays a more
important rule on facial growth and development, we should not expect to find,
on an individual basis, many of these dental anomalies. It is not possible,
therefore, to predict with any certainty whether or not a mouth breathing child
will develop malocclusion, despite the fact that on an epidemiological level,
mouth breathers have a higher risk of developing class II, anterior open bite and
posterior crossbite than a general population, as shown in other studies [10].
The results of this study suggest that older mouth breathing children (mixed and
permanent dentitions) have a tendency toward increasing the prevalence of
class II malocclusion and open bite. If this assumption is true, normalizing nasal
50
airflow passage in younger children, instead of postponing ENT treatments,
would be beneficial from an orthodontic point of view. This hypothesis needs to
be tested in a longitudinal design study.
Our data did not show any association between the prevalence of malocclusion
and an obstructive pattern of the tonsils and/or adenoid, nor with the presence
of allergic rhinitis. This is a controversial field in which previous studies have
shown discordant findings [2, 7, 49-54].
An explanation of this finding is based on morphogenetic sensitivity in the
development of malocclusion. If the child facial type is prone to the development
of one or more of the studied inter-arch abnormalities, mouth breathing will only
add an additional etiological “push”, regardless of the severity or the type of the
obstruction. Similarly, when a child has a low susceptibility to the development
of malocclusion, even in the presence of a greater airflow obstruction, no
dentofacial sequela will occur.
If this explanation represents the truth, the risk of developing malocclusion may
be proportional to its morphogenetic susceptibility, but not with the severity of
the obstruction. In this research, no evaluation of the skeletal pattern was done,
which would allow the identification and stratification of the susceptibility.
Therefore, it is only possible to speculate that a full spectrum of malocclusion
was present. This balanced distribution contributed to the interesting results of
no association between malocclusion and the grade of airflow blockage.
Secondly, another point which must be considered is the time lapse between
the initiation of mouth breathing and the malocclusion outcome. If we theorize
that, over time, children with greater obstruction could develop more
malocclusion than children with less severity, using a young sample may
explain the lack of association between the tested variables.
One more explanation to our results could be the chosen cut point which
classified the tonsils and adenoids hyperplasia as being obstructive or not. As
no validation of these clinical criteria was done yet, anyone can argue that a
51
bias on the obstruction classification interfered with the results.
As it was expected, the younger children had more tonsils and adenoids
obstruction than older ones
[55]
. The prevalence of rhinitis, however, was much
higher in older children. The reason is linked to Waldeyer’s ring involution with
aging, consequently reducing the number of older subjects with adenoid or
tonsil hyperplasia referred to the hospital. Thus the respiratory ENT complaint of
older children tends to be rhinitis.
The findings of this study suggest that, based on the orthodontic point of view,
ENT doctors should consider treating all mouth breathing children, regardless of
the etiological factor, since it is not possible to identify the risk of developing
malocclusion based solely on routinely used criteria.
Further research, with a longitudinal design and using methods that can help in
the identification of morphogenetic sensitivity such as lateral cephalometric
radiograph, and better evaluation of the severity of airway obstruction could add
important information to this topic.
In conclusion, our study showed that the investigated nasal impaired children
had a higher prevalence of posterior crossbite than general population at the
same stage of development. During mixed and permanent dentitions, anterior
open bite and class II malocclusion were more likely to be present in mouth
breathers. However, the majority of the children did not match the expected
“mouth breathing dental stereotype”. We have also showed that, in this sample
of mouth breathers, adenoids/tonsils hyperplasia or the presence of rhinitis,
have no association with the prevalence of class II malocclusion, anterior open
bite and posterior crossbite.
Acknowledgments
We thank Sidney M. Williams, DDS, for his kind contribution reviewing the
English language manuscript and Ms. Gleicilene Fatima Silva Chaves for her
contribution on data collection.
52
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57
Artigo 2
Título: Changes in vertical dentofacial morphology after adeno-/tonsillectomy
during deciduous and mixed dentitions mouth breathing children - one year
follow up study.
Autores: Bernardo Q. Souki, Giovana B. Pimenta, Leticia P. Franco, Helena M.
G. Becker and Jorge A. Pinto.
Revista: International Journal Pediatric Otorhinolaryngology
58
Changes in vertical dentofacial morphology after adeno-/tonsillectomy
during deciduous and mixed dentitions mouth breathing children - one
year follow up study.
Bernardo Q. Soukia,b, Giovana B. Pimentaa, Leticia P. Francoa, Helena M. G.
Beckera and Jorge A. Pintoa
a
Federal University of Minas Gerais, Outpatient Clinic for Mouth-Breathers, Belo
Horizonte, Brazil
b
Catholic University of Minas Gerais, School of Dentistry, Orthodontics, Belo
Horizonte, Brazil
Keywords: Mouth breathing, adenoidectomy, tonsillectomy, dentofacial growth
Abstract
Objective: The aim of this one year follow up study was to investigate, in
mouth breathing children, the impact of respiration normalization on vertical
dentofacial growth during two stages of dental development after adeno/tonsillectomy.
Method: Linear and angular cephalometric measurements, as well as
tracing superimposition of serial lateral cephalograms of 39 patients in the
treatment group were compared with those of 31 untreated mouth breathing
controls. Cephalometric records in the treatment group comprised registrations
made at baseline before surgery (T0), and then at approximately 1 year
postoperatively (T1). Corresponding registrations were available for the control
group, with a baseline cephalometric radiograph taken approximately 1 year
before the second one (T0 and T1, respectively). Treatment and untreated
groups were divided into deciduous and mixed dentition groups to aid the
identification of an optimum timing for normalizing the respiration after T&A,
under a vertical dentofacial perspective.
Results: After one year of follow up, no statistically significant difference
on vertical dentofacial growth was observed in deciduous or mixed dentitions
treatment groups compared to the same occlusal developmental stage of
untreated control groups.
59
Conclusion: The results indicate that regarding the vertical dentofacial
growth pattern normalization of the mode of respiration after T&A in young
children (deciduous dentition) is not more effective than in older children (mixed
dentition).
1. Introduction
The hyperplasia of adenoids, whether or not combined with tonsil’s hyperplasia,
may affect the children in many ways, resulting in Eustachian tube
dysfunction/otitis media
to thrive
[4]
halitosis
[1,2]
[1,2]
, rhinosinusitis
, swallowing problems
, speech problems
[1,2]
[1,2]
[1,2]
, obstructive sleep apnea [3], failure
, reduced ability to smell and taste
and abnormal dentofacial growth
[5-8]
[1,2]
,
. Some
of these consequences are due to the blockage of nasal airflow when oversized
tonsils/adenoids lead to mouth breathing.
Mouth breathing is a leading reason for otorhinolaryngological (ENT)
consultation
[9]
. Consequently, tonsillectomy and/or adenoidectomy (T&A) are
among the most common surgical procedures in children [10].
In the early years of the 20th century, surgical removal of tonsils was the rule
and was overused in many times
[2,12]
[11]
. Therefore, in the last decades there was
a tendency towards a more conservative management of the upper airway
obstructive tissues
[12, 13]
. Such an approach has a strong philosophical appeal,
but sometimes favors postponing the normalization of respiration. Choosing
between a conservative approach or a more aggressive therapy in young
children should be based on scientific evidence, rather than on emotion [1].
Among the dentofacial growth abnormalities associated with nasal airflow
obstruction, excessive vertical growth has a special concern for orthodontists
[14]
. The association between mouth breathing and a long facial form can be
attributed to the posterior rotation of the mandible that occurs in mouth
breathers
[15]
. Knowing that the vertical growth of the face is closely related to
mandibular growth rotation
[16]
, it seems logical that the acquisition of a normal
breathing in growing individuals should be a priority.
60
Previous longitudinal studies have showed that surgical treatment of nasal
obstruction in growing individuals results in a vertical facial development closer
to a normal pattern
[17-23]
, but have not tested differences on timing of adeno-
/tonsillectomy.
Therefore, the aim of this study was to evaluate one year prospectively the
cephalometric vertical dentofacial changes of mouth breathing children who had
early and late normalization of the mode of respiration, after ENT surgical
procedures.
2. Patients and Methods
2.1. Sample
The sample consisted of 70 children, ranging from 3 to 10 years of age referred
by pediatricians and primary care physicians to the Outpatient Clinic for MouthBreathers, at the Hospital das Clínicas of the Federal University of Minas Gerais
(UFMG), Brazil, with a diagnosis of mouth breathing. An interview with
children’s parents, or guardians, asking about the quality of the children’s sleep,
snoring, oral breathing and throat infections, confirmed the ‘‘chief complaint’’ of
mouth breathing. None of the children had been undergone an adenoidectomy
or tonsillectomy earlier. Clinical ENT examination was performed by two of the
authors (L.F. and H.B.), according to the following guidelines.
Palatine tonsil hypertrophy was classified by mouth examination according to
the criteria of Brodsky and Koch
[24]
as follows: grade 0, tonsils limited to the
tonsillar fossa; grade 1, tonsils occupying up to 25% of the space between the
anterior pillars in the oropharynx; grade 2, tonsils occupying 25–50% of the
space between the anterior pillars; grade 3, tonsils occupying 50–75% of the
space between the anterior pillars; and grade 4, tonsils occupying 75–100% of
the space between the anterior pillars. Tonsils grade 0, 1 and 2 were
61
considered as non-obstructive and those classified as grade 3 and 4 were
named as obstructive [25].
Adenoids were assessed by flexible nasoendoscopy and were grouped into two
categories based on nasopharyngeal obstruction (<75% and ≥75%). A cut-point
of 75% was chosen to classify the blockage of the nasopharynx as nonobstructive or obstructive
[26]
. All subjects presented obstructive tonsils and/or
adenoids, and were to undergo T&A.
At the beginning of this study, 26 children were within deciduous dentition (19
male and 7 female) and 44 presented in mixed dentition (27 male and 17
female). Angle class I malocclusion was the sagital classification of 25 children
(35.7%). Class II was found in 27 subjects (38.6%) and normal occlusion was
detected in 18 children (25.7%). Anterior open bite was diagnosed of 22
subjects (31.4%), while a normal vertical inter-arch relationship was present in
29 cases (41.4%). Posterior crossbite was accessed in 14.3% of the children.
The treatment group (TG) was comprised of those 39 children whose surgical
procedure was immediately authorized by municipality public healthy service.
Obstructive adenoids were detected in 35 children and obstructive tonsils in 23
children of this group. The control group (CG) consisted of 31 patients who had
to wait more than one year for the surgical authorization. From this total, 26 had
obstructive adenoids and 12 presented obstructive tonsils. The control samples
matched the treatment samples as to the mean age at baseline, gender
distribution, Angle inter-arch relationship and mean duration of observational
periods.
The children were further separated into younger subjects (deciduous dentition
at the beginning of the study) and older subjects (mixed dentition at the
beginning of the study). Using this stratification, we evaluated age-related
differences and trends in four groups: treatment group within deciduous
dentition (TG1), treatment group within mixed dentition (TG2), control group
within deciduous dentition (CG1) and control group within mixed dentition
(CG2).
62
Among the treatment group children, one had been a thumb sucker. In this
patient however, the habit had ceased before the start of the study. Fifteen
children in this group had been dummy suckers, but the sucking habit had
ceased at least two years before they entered the investigation. Among the
controls, none were finger sucker when entering the study and 10 had ceased
dummy sucking for over a 1 year period.
Surgical effects on mouth breathing habits were determined with the same ENT
criteria used pre-surgically. These findings were confirmed by parents report
during bimonthly visits along with the 1 year post-surgical consultations. All
control group patients kept their mouth breathing habit during the 1 year period,
as reported by their parents quarterly.
The participant’s rights were protected, and informed consent and assent was
obtained according to the Ethics Committee of the Federal University of Minas
Gerais.
2.2. Cephalometric analysis
Standard lateral cephalometric radiographs were obtained to evaluate the
skeletal characteristics of the two groups. All radiographs were taken using the
same equipment. Cephalometric records in the treatment group comprised
registrations made at baseline before surgery (T0), and then at approximately 1
year post-operatively (T1). Corresponding registrations were available for the
control group, with a baseline cephalometric radiograph taken at baseline and
another approximately 1 year after (T0 and T1, respectively).
Cephalometric analysis was performed by the same orthodontist (B.S), in
random order. Measurements (SNGoGn, NSGn and ArGoGn) routinely used
for orthodontic treatment planning were performed to characterize the baseline
vertical facial type of subjects
[27, 28]
. All measurements showed higher angles
than on average for the general population. Therefore, the baseline sample was
characterized as excessive vertical growing faces.
63
The assessment of treatment results was based on a previously described
reference system traced through craniofacial stable structures
[34]
. First, the
stable basicranial line (SBL) was traced through the most superior point of the
anterior wall of sella turcica at the junction with tuberculum sellae (point T)
drawn tangent to lamina cribrosa of the ethmoid bone. The next step was the
identification of the following five skeletal landmarks
[35]
: Menton (Me), Gonion
(Go), Articulare (Ar), Anterior Nasal Spine (ANS), Posterior Nasal Spine (PNS).
Then, the following angular (.), linear (-) and ratio (/) measurements were
obtained and are described below (Fig 1):
1) SBL.MP: determined by the intersection between the SBL and the
mandibular plane (Go-Me). This angle measures the inclination of the
mandibular plane.
2) NL.MP: determined by the intersection between the nasal line (ANS-PNS)
and the mandibular plane. This angle measures the divergence between the
maxilla and the mandible.
3) SBL-Me: linear measurement determined by the orthogonal union of the
mental point and the SBL, corresponding to the total anterior facial height
(TAFH).
4) NL-Me: linear measurement determined by the union of the mental point and
the nasal line, measured over the SBL-Me line, corresponding to lower anterior
face height (LAFH).
5) SBL-Go: linear measurement determined by the orthogonal union of the
gonial point and the SBL, corresponding to the posterior facial height (PFH).
6) Lower/Total anterior facial height ratio (LAFH/TAFH): determined by the ratio
between NL-Me and SBL-Me.
64
7) Posterior/Total anterior facial height ratio (PFH/TAFH): determined by the
ratio between SBL-Go and SBL-Me.
MP
Figure 1 - Cephalogram illustrating the skeletal landmarks, the angular and
linear measurements.
Individuals with a vertical growing facial type have an opened mandibular plane
angle (SBL.MP), as well as a hyperdivergence of nasal line and mandibular
plane (NL.MP). Due to the backward rotation of the mandible, such individuals
present a small ratio between the posterior face height and the total anterior
face height (PFH/TAFH). A large ratio between the lower anterior face height
and the total anterior face height (LAFH/TAFH) is also expected.
Superimposing tracings of serial lateral cephalograms allowed the classification
of the mandibular rotation as true rotation, apparent rotation and angular
remodeling [30, 36].
True rotation was defined as the angular change between the SBL, at the first
and at the second observation, on the superimposed tracings, using fiduciary
mandible landmarks (Fig. 2) [34].
65
Figure 2 - Mandibular true rotation evaluated by angular changes between T0
(SBL 1) and T1 (SBL 2) after the superimposition on the fiducial skeletal
landmarks indicated by arrows.
The T1-T0 difference between SBL.MP measurements was used to describe
apparent rotation. Mandibular apparent rotation can be visualized by
superimposing tracings on SBL at point T (Fig. 3). Angular remodeling was
defined as the difference between apparent rotation and true rotation.
The cephalometric data were concentrated in tables and subject to statistical
analysis for the determination of morphologic differences.
66
Figure 3 - Mandibular apparent rotation between T0 and T1. Superimposition on
the SBL at “point T”.
2.3. Error analysis
To determine errors in landmark identification and measurements, 25 cases
randomly selected head films were retraced and remeasured by the same
orthodontist, after an interval of at least two months. To test inter-examiners
reliability, 15 cases were retraced by a second orthodontist (G.P.). Random
error was calculated using Dahlberg's equation
[37]
. Systematic error (bias) was
assessed using the paired t-test, for p<0.05.
2.4. Data Analysis
The results of Kolmogorov-Smirnov and Levene tests demonstrated the
accomplishment of the suppositions of normality and homoscedasticity which
allowed the comparison between the means of the two groups and the growth
changes with parametric test (independent samples t-test and paired sample ttest respectively). Exception to “angular remodeling”, because the normal
67
distribution and equal variance assumption were rejected, a non-parametric test
(Mann-Whitney U test) was used.
To assess significant differences between craniofacial starting forms at the time
of the first observation, we compared treatment and control groups at T0 (TG1
vs. CG1; TG2 vs. CG2).
To overcome discrepancies between treatment and control groups with regard
to observation period, all differences were annualized. Craniofacial growth
changes (T1-T0) in the early-treatment group (TG1) were contrasted with those
in the early-control group (CG1). Similarly, the changes in the late-treatment
group (TG2) were compared with those in late-untreated group (CG2).
All computations were performed with the Statistical Package for the Social
Sciences (SPSS), version 12.0.
3. Results
The systematic error in measurement did not exceed 0.74° or 0.5 mm and thus
considered to be of no further importance. The random error ranged between
0.3 and 0.5 mm for the linear measurements and between 0.02° and 0.88° for
the angular measurements. There were no statistically significant differences
between the two measurements.
The age distribution of the subjects in the experimental and control groups did
not showed statistical difference at a probability level of 5% at baseline (T0).
The mean ages in the deciduous dentition (CG1 and TG1) were 5.1 (SD: 0.83)
and 4.7 years (SD: 0.93), respectively. During mixed dentition the mean ages
were 7.9 (SD: 1.51) during CG2 and 7.5 years (SD: 1.56) during TG2.
68
Table 1- Independent samples t-test comparison
of the baseline (T0)
cephalometric angular and ratio measurements between the treatment (TG) and
control (CG) groups during the two stages of dental development (deciduous
and mixed dentitions).
Variable
SBL.PM
NL.PM
Deciduous
dentition
PFH/TAFH
LAFH/TAFH
SBL.PM
NL.PM
Mixed
dentition
PFH/TAFH
LAFH/TAFH
Groups
TG1
CG1
TG1
CG1
TG1
CG1
TG1
CG1
n
13
13
13
13
13
13
13
13
Mean
41.54
41.54
34.65
35.15
62.00
60.99
57.41
58.04
SD
4.180
2.809
3.782
3.502
2.844
1.794
1.746
2.413
SE
1.159
0.779
1.049
0.971
0.789
0.497
0.484
0.669
p value
1.000
TG2
CG2
TG2
CG2
TG2
CG2
TG2
CG2
26
18
26
18
26
18
26
18
42.37
41.81
34.11
33.03
60.43
60.21
56.73
56.85
5.684
5.255
4.021
3.821
3.629
3.834
2.536
2.118
1.160
1.238
0.789
0.900
0.729
0.903
0.495
0.499
0.742
0.730
0.285
0.454
0.373
0.848
0.870
The gender distribution within treatment and controls groups in both stages of
dental development were statistically the same (Χ2 p value >0.05).
No significant differences between craniofacial starting forms for any of the
angular and ratio cephalometric variables at T0 were observed (Table 1). The
homogeneity between treatment and control groups with regard to mean age,
sex distribution, and craniofacial pattern at T0 permitted comparison of these
paired groups with regard to the growth differences between T1 and T0 for all
the cephalometric variables.
Tables 2 and 3 display the comparison of the annualized vertical growth result
(T1-T0) in deciduous and mixed dentition groups. The linear measurements
(SBL-Go, SBL-Me and NL-Me) had statistically significant changes between T0
and T1 in the treatment groups, as well as in control groups, regardless the
stage of dental development. The ratio measurements (PFH/TAFH and
LAFH/TAFH) did not have statistically significant changes either during
deciduous dentition or mixed dentition surgical intervention, as well as in the
69
untreated control groups. The angular measurements (SBL.MP and NL.MP)
showed different pattern of growth comparing deciduous and mixed dentition
groups. During deciduous dentition (Table 2) the reduction of SBL.MP angle
from T0 to T1 did not show statistically significant differences either in the
treatment and control groups. However, during mixed dentition (Table 3), the
SBL.MP reduction was statistically different for the treatment and control
groups. The NL.PM changes in the mixed dentition groups were similar. Both
treatment and control groups had a reduction of the divergence between maxilla
and mandible (p>0.05) (Table 3). Nevertheless, the deciduous dentition
treatment group showed a statistically significant reduction of the divergence
between maxilla and mandible, whereas the untreated control group had an
increase in the divergence (Table 2).
Table 2- Paired-sample t-test comparison between changes of cephalometric
measurements in T0 and T1 for the group of children submitted to T&A during
deciduous dentition (TG1) and its untreated matched control group (CG1).
Groups
Mean
TG1
(n=13)
CG1
(n=13)
1
T0
Variables
1
T
SD
0
T vs. T
Mean
SD
difference
4.461
-0.31
2.146
0.615
SD
p value
SBL.PM
41.54
4.180
Mean
41.23
NL.PM
34.65
3.782
33.92
3.499
-0.73
1.091
0.033
SBL-Go
58.77
3.244
61.65
3.478
2.88
1.861
0.000
SBL-Me
94.88
5.443
99.34
4.780
4.46
1.919
0.000
NL-Me
54.42
2.596
56.96
2.193
2.54
1.265
0.000
PFH/TAFH
62.01
2.844
62.10
2.953
0.09
1.041
0.748
LAFH/TAFH
57.41
1.746
57.38
1.790
-0.03
0.650
0.896
SBL.PM
41.54
2.809
41.04
2.940
-0.50
1.732
0.318
NL.PM
35.15
3.502
35.42
2.978
0.27
1.549
0.543
SBL-Go
60.07
4.334
63.12
4.496
3.05
1.450
0.000
SBL-Me
98.50
6.416
102.39
7.056
3.89
1.401
0.000
70
NL-Me
57.08
2.921
59.19
3.159
2.11
1.157
0.000
PFH/TAFH
60.99
1.794
61.66
1.800
0.67
1.155
0.057
LAFH/TAFH
58.04
2.413
57.91
2.211
-0.13
0.610
0.449
Paired samples correlation were all higher than 0.849 (p value 0.000)
Table 3- Paired-sample t-test comparison between changes of cephalometric
measurements in T0 and T1 for the group of children submitted to T&A during
mixed dentition (TG2) and its untreated matched control group (CG2).
Groups
T
SBL.PM
42.36
5.687
41.69
NL.PM
34.11
4.023
33.75
4.271
-0.36
1,730
0.288
SBL-Go
64.17
5.001
66.20
5.780
2,03
1,712
0.000
SBL-Me
106.25
6.172
109.06
6.451
2,81
1,479
0.000
NL-Me
60.27
4.341
61.81
4.835
1,54
1,394
0.000
PFH/TAFH
60.42
3.629
60.86
4.179
0.44
1,537
0.765
LAFH/TAFH
56.73
2.526
56.65
2.328
-0.08
1,228
0.159
SBL.PM
41.81
5.255
41.25
5.303
-0.57
1.055
0.039
NL.PM
33.03
3.821
32.31
2.855
-0.72
1.750
0.098
SBL-Go
64.00
5.104
66.28
5.319
2.28
1.691
0.000
CG2
(n=18)
SBL-Me
106.31
5.311
109.11
5.579
2.80
1.373
0.000
NL-Me
60.44
3.988
61.39
4.496
0.95
1.282
0.006
PFH/TAFH
60.20
3.834
60.75
3.949
0.55
1.297
0.091
LAFH/TAFH
56.75
2.118
56.64
2.376
-0.11
0.788
0.089
SD
Mean
T1 vs. T0
Mean
difference
5.591
-0.67
Mean
TG2
(n=26)
T1
0
Variables
SD
Paired samples correlation were all higher than 0.844 (p value 0.000)
SD
p value
1,306
0.026
71
Table 4 gives information on mandibular rotation in the four groups. No
statistically significant difference on mandibular rotation was found between
treatment and control groups, despite the stage of dental development.
Table 4– Independent samples t-test comparison of mandibular rotation (true
rotation. apparent rotation and angular remodeling) between treatment (TG) and
control (CG) groups during deciduous and mixed dentitions.
Groups
Deciduous
dentition
Mixed
dentition
Variables
CG
TG
TG vs. CG
SE
difference
0.993
Mean
SD
Mean
SD
True rotation
-0.70
2.131
-0.84
2.877
Mean
difference
0.14
p
value
0.886
Apparent
rotation
-0.51
2.488
-0.62
2.139
0.11
0.910
0.905
Angular
remodeling *
0.19
1.662
0.22
2.106
0.03
0.744
0.964
True rotation
-1.52
2.831
-1.06
1.620
0.46
0.718
0.543
Apparent
rotation
-0.69
1.759
-0.58
1.118
0.11
0.430
0.809
Angular
remodeling*
0.82
1.945
0.48
1.348
0.34
0.540
0.525
* Mann Whitney U Test
Figure 4 illustrates the net growth observed between T0 and T1 during
deciduous and mixed dentitions, comparing the mean values found in treatment
and control groups. Negative values indicate that a measurement reduction,
while positive values indicate an increase. An independent t-test comparison of
the means indicates that the divergence between maxilla and mandible during
deciduous dentition is the only variable that had inter-group statistically
significant difference.
72
LAFH/TAFH
-0,03
=
SBL-MP
-0,31
=
-0,50
PFH/TAFH
NL-MP
-0,73*
TG1
-0,13
CG1
+0,09
+0,67
=
+0,25
=
LAFH/TAFH
-0,08
=
SBL-MP
-0,67*
-0,57*
=
PFH/TAFH
NL-MP
-0,36
TG2
CG2
-0,11
-0,72
+0,44
+0,55
=
=
Figure 4 – Net growth measured in the four groups (TG1, CG1, TG2, CG2). Negative
values mean measurement reduction between T0 and T1 while positive values indicate
increase.
* indicates statistically significant intra-group difference
= indicates no statistically significant inter-group difference
73
4. Discussion
Although absolute and relative evidence-based indications for T&A are well
described in the ENT literature, the pendulum of public and professional opinion
concerning these surgical procedures continues to swing between enthusiasm
and condemnation [2].
Postponing T&A in young mouth breathing children is sometimes the
physician’s choice due to surgical complications concerns [2], as well as because
adenoids and tonsils airflow obstruction gradually undergo a reduction after 5
years of age
[26]
. However, if the mode of respiration does not shift to nasal,
such a conservative approach can contribute to unfavorable excessive vertical
dentofacial growth, since clockwise mandible rotation is most likely to occur [15].
Considering that a significant facial growth happens early in life [32], it is possible
to theorize that allowing a child to breath with difficulty years ahead, can
contribute to a more mature dentofacial abnormality.
Arun, Isik and Sayinsu
[33]
investigated retrospectively 66 lateral cephalometric
radiographs of subjects with early (up to 4 years of age) and late (after 4 years
of age) adenoidectomy history. No statistically significant difference was found
among the studied skeletal vertical parameters, with exception to the lower
anterior facial height. They concluded that their investigation should be
considered as a pilot study, suggesting a longitudinal monitoring of children who
had early adenoidectomies. This knowledge can contribute to the understanding
of the benefits of early breathing normalization, by surgical management of
adenoids and tonsils hyperplasia, from the orthodontist’s point of view.
Therefore, the primary question of the present investigation was: do children
who have an early change in the mode of respiration, after T&A, grow differently
than late treatment children?
We established that the children within the deciduous dentition group, at
baseline, were in the “early” group, while children in mixed dentition were
74
grouped as “late”. Using the dental stage of development as a cut point has the
advantage of been an easy clinical criteria. We conscientiously chose this
criteria, even knowing that such a parameter has one disadvantage that can
bias our conclusions.
Because dental development is independent of pubertal growth
[38]
, children
within the same stage of dental development, even matched in chronological
ages, can be in different maturational stages. Therefore, a comparison using
skeletal maturational parameters would be more sensitive. However using
hand-wrist radiographs would not be practical in a daily clinical perspective, and
cervical vertebral maturation method using the lateral cephalogram is not
indicated for very young children [42]. Future studies should include maturational
stage of development as indication of early and late intervention.
True mandibular rotation provides important information for an understanding of
dentofacial growth changes
[30, 40]
. The literature has shown that the mandible
typically rotates in a forward direction
[30, 39]
during childhood than during adolescence
with greater rates of true rotation
[30]
. This behavior is independent of
gender or sagital dental malocclusion classification
[30]
. As our sample was
comprised only by childhood individuals, it was expected that the true
mandibular
rotation
would
follow
this
forward
pattern.
However,
as
environmental variables, such as mouth breathing, were present in all children,
maybe a backward rotation tendency could happen, lessening or reversing the
forward rotation.
The rates of true rotation, apparent rotation and angular remodeling, either
during deciduous or mixed dentitions, were not affected by T&A. No statistically
significant difference was found between treatment and control groups, as
showed in Table 4.
The annual changes (degree/year) in true rotation observed in this study for
mixed dentition children were –1.52 and -1.06 for treatment group and control
group, respectively. Such rates are similar to those previously reported for
general population during the transition from primary to early mixed dentition [30]
75
and for 5- to 10-year-olds
[16]
. The similarity between our findings and in the
general population’s suggests that the presence of mouth breathing, or the
normalization of respiration after T&A, does not alter the mandible rotation
during mixed dentition.
During the deciduous dentition, the annual changes (degree/year) in true
rotation was smaller (-0.69 and -0.84 for TG1 and CG1, respectively), but the
forward counterclockwise prevailed. It is possible to speculate that the relatively
low rates of true rotation in our sample could be due to age differences.
However, such finding is contradictory to Wang, Buschang and Behrents
[30]
.
The fact is that both treatment and control groups showed a similar pattern of
mandible true rotation, thus T&A seamed to have no influence on such variable
after 1 year.
The apparent rotation was very similar in all four groups. We found that a
counterclockwise rotation of about 0.5 degrees was the mean annual change.
Therefore, the mandible rotated forward regardless the stage of dental
development. The rates of apparent rotation are similar to those previously
reported [16,30].
As commented by Wang, Buschang and Behrents
[30]
, subjects undergoing
greater true mandibular rotation will also undergo greater remodeling. The lower
border of the mandible is compensating to maintain its orientation in response
to faster rates of true rotation. We had a higher rate of angular remodeling in
mixed dentition groups, whose true rotation was also higher.
Our cephalometric analysis showed that mouth breathing children submitted to
T&A have the same vertical dentofacial growth behavior as their matched
controls, regardless of the stage of dental development, suggesting that
normalizing the breathing pattern during late deciduous dentition or during
mixed dentition did not make difference. Such results are in agreement with
those reported in the transversal study of Arun, Isik and Sayinsu
timing of T&A did not influenced the vertical dentofacial growth.
[33]
, where
76
The only measurement that showed a different pattern of change between T0
and T1 was the angular divergence between maxilla and mandible in the group
of children adenotonsillectomized during deciduous dentition. This group (TG1)
had a significant reduction of the NL.MP angle, while its control group (CG1)
had a not significant increase. However, we considered that the vertical
improvement of such measurement alone is not sufficient to consider the
deciduous dentition as a better moment to T&A.
Analyzing our sample mean age, during deciduous dentition, it is clear that late
primary dentition prevails, thus this group is older than the 4 years old
suggested by Arun, Isik and Sayinsu
[33]
as an age limit to consider as early for
T&A. This fact may have influenced the results. Maybe if the children in the
deciduous dentition were younger other results could be found. Additional
research, including younger children, as well as, the identification of other
independent variables, can bring supporting data as to the timing of T&A.
Previous longitudinal studies
[17-23]
, which evaluated changes in dentofacial
growth of mouth breathers following T&A, used nasal breathing subjects as
controls. We opted to use an untreated mouth breathing sample as the control
group, understanding that this methodology better represents what should be
the expected growth if no intervention was performed, as previously mentioned
by Linder-Aronson et al. [19]. Therefore, normative data available in the literature
for general population can not be used for comparisons. The data collection for
this type of control group, without ethical concerns, was possible because in this
population, the time span between the surgery indication and the government
authorization to it, in several cases, was long due to high demand. Fortunately,
our findings showed that waiting such a long time for the opportunity to be
operated on did not worsen the vertical dentofacial pattern of such children.
Such information suggests the necessity of additional studies, using untreated
mouth breathing children as controls, to investigate the behavior of dentofacial
growth after T&A.
The five year follow up, reported in previous studies, would be less sensitive to
measurements errors, as commented by Linder-Aronson et al.
[19]
. However,
77
with our research design, the observational period is limited. As the reported
changes in the first year post-operativelly are apparently enough to indicate
modifications on the mode of growth [29], we believe that 1 year follow up brings
us important data to discuss.
The reported data allow us to believe that postponing mouth breathing
treatment from late deciduous dentition to mixed dentition will not, on average,
favor an undesirable dentofacial vertical growth. Our study, however, does not
indicate in all cases that postponing the normalization of mouth breathing is not
harmful to vertical dentofacial growth. Despite not being the subject of our
study, we believe that depending on the facial morphogenetic susceptibility,
vertical growth behavior of some mouth breathing children may be deleterious
and should be avoided. Clinicians must be aware of such cases and establish
individually the appropriate timing to surgical intervention.
In conclusion, our results indicate that, regarding the dentofacial vertical growth
pattern, normalization of the mode of respiration in young children (deciduous
dentition) is not more effective than in older children (mixed dentition).
Acknowledgments
We thank Sidney M. Williams, DDS, for his kind contribution reviewing the
English language manuscript, as well as to Ms. Gleicilene Silva Chaves for her
help with data collection.
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82
Artigo 3
Título: Vertical facial changes following adeno/-tonsillectomy: changing
concepts?
Autores: Bernardo Q. Souki, Giovana B. Pimenta, Leticia P. Franco, Helena M.
G. Becker and Jorge A. Pinto.
Revista: Angle Orthodontist (a ser enviado)
83
Artigo 3
Vertical facial changes following adeno/-tonsillectomy: changing
concepts?
Bernardo Q. Soukia,b, Giovana B. Pimentaa, Leticia P. Francoa, Helena M. G.
Beckera and Jorge A. Pintoa
a
Federal University of Minas Gerais, Outpatient Clinic for Mouth-Breathers, Belo
Horizonte, Brazil
b
Catholic University of Minas Gerais, School of Dentistry, Orthodontics, Belo
Horizonte, Brazil
Keywords: Mouth breathing, adenoidectomy, tonsillectomy, dentofacial growth
Abstract
Objective: The aim of this one year follow up study was to investigate, in
mouth breathers, the impact of respiration normalization on vertical dentofacial
growth after adeno-/tonsillectomy (T&A) controlling the results with a matched
group of untreated mouth breathing children.
Method: Linear and angular cephalometric measurements, as well as
superimposing tracings of serial lateral cephalograms of 39 patients in the
treatment group (TG) were compared with those of 31 untreated mouth
breathing controls (CG). Cephalometric records in the treatment group
comprised registrations made at baseline before surgery (T0), and then at
approximately 1 year post-operatively (T1). Corresponding registrations were
available for the control group, with a baseline cephalometric radiograph taken
approximately 1 year before the second one (T0 and T1, respectively).
Results: Statistically significant growth (p<0.000) was found for all linear
measurements (SBL-Go, SBL-Me, NL-Me) in both groups (TG and CG). A
reduction in LAFH/TAFH, SBL-MP and NL-MP, as well as an increase in
PFH/TAFH, were the growth mean behavior both in TG and CG. There was no
statistically significant difference between TG and CG regarding the mandibular
rotation.
84
Conclusion: The results indicate that the normalization of the mode of
respiration, after T&A, did not change the pattern of mandibular vertical growth,
after one year, when compared to a matched untreated group of mouth
breathers.
1. Introduction
Previous studies reported that the mandible typically rotates in a forward
direction during childhood and adolescence[1]. However Lavergne and Gasson[2]
using metal implants demonstrated that only occasionally the mandible exhibit a
simple pattern of rotation. In most cases the rotational phenomenon appears to
be complex with variations in direction and intensity.
Individuals with backward rotation of the mandible and an increased lower
anterior facial height are of concern to Orthodontists due to aesthetics,
functional and mechanical reasons[3]. Excessive vertical dentofacial growth is
associated with heredity[4], but environmental factors such as mouth breathing
can play an important rule in the growth direction[5-9].
The association between mouth breathing and a long facial form can be
attributed to the posterior rotation of the mandible that occurs in nasal impaired
children[10]. This backward rotation most likely occurs due to a greater vertical
growth in the molar region than at the condyles, which happens when the mouth
is maintained open.
A series of publications signed by Swedish
[5,6,11-13]
researchers have set the
concept that normalization of mouth breathing after adenoidectomy, leads
children to a vertical dentofacial growth closer to a normal pattern. The control
groups of those reports were composed by healthy subjects who had no history
of nasal obstruction or nasorespiratory allergy.
Despite the conclusion that adenoidectomy has a positive impact on vertical
dentofacial growth, Linder-Aronson, Woodside and Lündstrom[6], in the
discussion of one of those articles, recognized that it would have been
85
preferable, from a purely scientific point of view, to have unoperated but
obstructed control samples. However, this would have been unethical.
Considering that using healthy subjects as controls could bias the previously
reported results, a question arises whether the reported data are robust enough
to sustain the prevailing concept that normalizing the mode of breathing after
surgical otorhinolaryngological (ENT) procedures will improve the dentofacial
vertical growth. Therefore, an ethical research design with untreated mouth
breathing children, would contribute to the comprehension of this growth
behavior.
The high demand for medical assistance in the Brazilian public health service
determined a long waiting line, what implies that many severely obstructed
children have to wait over a year for the authorization to surgical procedures.
Thus, such patients, growing under the influence of mouth breathing can
contribute to a better understanding of the natural development of the disease
and its consequences.
The purpose of this study was to compare the dentofacial vertical growth and
the
mandibular
rotation
of
a
group
of
children
who
underwent
adenotonsillectomy to normalize the mode of breathing with an untreated mouth
breathing control group.
2. Patients and Methods
2.1. Sample
The sample consisted of 70 children of both sexes, ranging from 3 to 10 years
referred by pediatricians and primary care physicians to the Outpatient Clinic for
Mouth-Breathers, at the Hospital das Clínicas at Federal University of Minas
Gerais (UFMG), Belo Horizonte, Brazil, with a diagnose of mouth breathing.
Otorhinolaryngological examination (ENT) confirmed the obstructed nasal
airflow. All subjects had enlarged tonsils and/or adenoids, and were to undergo
86
T&A.
The treatment group (TG) was comprised of those 39 children (14 female and
25 male) whose surgical procedure was immediately authorized by municipality
public health service. The control group (CG) consisted of 31 patients (10
female and 21 male) who had to wait more than one year for the surgical
authorization. The control group matched the treatment group as to the mean
age at baseline, gender distribution, and mean duration of observational
periods.
Among the treatment group children, one had been a thumb sucker. In this
patient however, the habit had ceased before the start of the study. Fifteen
children in this group had been dummy suckers, but the sucking habit had
ceased at least 2 years before they entered the investigation. Among the
controls, none were finger suckers when entering the study, and 10 ceased
dummy sucking for more than 1 year.
The surgery was successful in all treated patients and resolved mouth
breathing, a fact which was verified by parents report during bimonthly visits
along with 1 year post-operative consultations. All control group patients kept
their mouth breathing habit during the 1 year period, as reported by their
parents quarterly.
The participant’s rights were protected, and informed consent and assent was
obtained according to the Ethics Committee of the Federal University of Minas
Gerais.
2.2. Cephalometric analysis
Standard lateral cephalometric radiographs were obtained to evaluate the
skeletal characteristics of the two groups. All radiographs were taken using the
same equipment. Cephalometric records in the treatment group comprised
registrations made at baseline before surgery (T0), and then at approximately 1
year post-operatively (T1). Corresponding registrations were available for the
87
control group, with a baseline cephalometric radiograph taken at baseline and
another approximately 1 year after (T0 and T1, respectively).
Cephalometric measurements (SNGoGn, NSGn and ArGoGn) routinely used
for orthodontic treatment planning were performed to characterize the baseline
vertical facial type of subjects
[14, 15]
. However, to assess the treatment results, a
previously described reference system traced through craniofacial stable
structures
[16]
was choisen. The cephalometric landmarks and measurements
used in this study have been published elsewhere [23].
The cephalometric data were concentrated in tables and subject to statistical
analysis for the determination of morphologic differences between treatment
and control groups.
2.3. Error analysis
To determine errors in landmark identification and measurements, 25 cases
randomly selected head films were retraced and remeasured by the same
investigator (B.S), after an interval of at least two months. In order to test interexaminers reliability, 15 cases were retraced by a second orthodontist (G.P.).
Random error was calculated using Dahlberg's equation
[17]
. Systematic error
(bias) was assessed using the paired t-test, for p<0.05.
2.4. Data Analysis
The results of Kolmogov-Smirnov and Levene tests demonstrated the
accomplishment of the suppositions of normality and homoscedasticity which
allowed the comparison between the means of the two groups and the growth
changes with parametric test (independent samples t-test and paired sample ttest respectively). Exception to “angular remodeling”, because the normal
distribution and equal variance assumption were rejected, a non-parametric test
(Mann-Whitney U test) was used.
To assess significant differences between craniofacial starting forms at the time
of the first observation, we compared treatment and control groups at T0 (TG vs.
CG).
88
To overcome discrepancies between treated and control groups with regard to
observation period, all differences were annualized. Craniofacial significance of
the changes (T1-T0) in the TG was contrasted with those in the CG using a
paired sample t-test.
Mandibular rotation in TG was compared with CG using an independent sample
t-test or Mann-Whitney U test. All computations were performed with the
Statistical Package for the Social Sciences (SPSS), version 12.0.
3. Results
The systematic error in measurement did not exceed 0.74° or 0.5 mm and thus
considered to be of no further importance. The random error ranged between
0.3 and 0.5 mm for the linear measurements and between 0.02° and 0.88° for
the angular measurements. There were no statistically significant differences
between the two measurements.
The age distribution of the subjects in the treatment and control groups did not
showed statistical difference at a probability level of 5% at baseline (T0). The
mean age in the TG was 6.5 (S.D.:1.92) and 6.7 (S.D.:1.85) for CG. The gender
distribution within treatment and controls groups were statistically the same (Χ2
p value = 0.750).
No significant differences between TG and CG, regarding the craniofacial
starting forms, for any of the cephalometric variables at T0 were observed
(Table 1). The homogeneity between treated and control groups with regard to
mean age, sex distribution, and craniofacial pattern at T0 permitted comparison
of the groups with regard to the differences between the values at T1 and at T0
for all the cephalometric variables.
89
Table 1- Comparison of the baseline (T0) cephalometric angular, linear and ratio
measurements between the TG (n=39) and CG (n=31).
Variable
SNGoGn
NSGn
ArGo.GoMe
SBL.PM
NL.PM
SBL-Go
SBL-Me
NL-Me
PFH/TAFH
LAFH/TAFH
Groups
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
TG
CG
Mean
38.8
38.7
70.4
70.4
134.6
133.7
42.2
41.6
34.2
33.9
63.2
62.3
101.2
103.0
58.1
59.0
0.6362
0.6052
0.5784
0.5735
SD
4.52
4.10
3.44
2.98
4.17
4.59
5.26
4.33
4.00
3.78
8.56
5.11
10.43
6.91
4.80
3.90
0.1736
0.0312
0.6225
0.0228
SE
0.73
0.74
0.55
0.54
0.67
0.83
0.86
0.77
0.65
0.67
1.40
0.91
1.71
1.24
0.78
0.70
0.0285
0.0056
0.0102
0.0041
t-test p
value
0.874
0.946
0.375
0.652
0.703
0.598
0.425
0.429
0.331
0.675
Table 2 gives the comparison of the annualized vertical growth result (T1-T0) in
the treatment and control groups. Statistically significant growth (p<0.000) was
found for all linear measurements (SBL-Go, SBL-Me, NL-Me) in both groups
(TG and CG).
Both TG and CG showed the same pattern of vertical facial growth with a
reduction in LAFH/TAFH, SBL-MP and NL-MP, and an increase in PFH/TAFH
(Table 2). However analyzing statistically such changes, the reduction of
divergence between maxilla and mandible (NL-PM) was significant only for
treatment group. For LAFH/TAFH, SBL-MP and PFH/TAFH the statistically
significant difference was detected only for the control group.
90
Table 2- Comparison between the treatment group (TG) and control group (CG)
for changes within each pair of variable using a paired Student’s t-test.
Groups
TG
CG
T1
0
Variables
T
T1 vs. T0
Mean diff
SD
-0.4
1.61
SBL.PM
Mean
42.2
SD
5.26
Mean
41.8
SD
5.17
p value
0.124
NL.PM
34.2
4.00
33.7
4.08
-0.5
1.55
0.041
SBL-Go
63.2
8.56
65.6
9.07
2.4
1.83
0.000
SBL-Me
101.2
10.43
104.6
10.07
3.4
1.75
0.000
NL-Me
58.1
4.80
60.1
4.84
2.0
1.38
0.000
PFH/TAFH
63.62
17.36
63.83
17.28
0.21
1.38
0.349
LAFH/TAFH
57.86
6.22
57.84
6.05
-0.02
1.06
0.923
SBL.PM
41.6
4.33
41.1
4.40
-0.5
1.35
0.036
NL.PM
33.9
3.78
33.6
3.25
-0.3
1.71
0.328
SBL-Go
62.3
5.11
64.9
5.16
2.6
1.61
0.000
SBL-Me
103.0
6.91
106.2
6.99
3.2
1.46
0.000
NL-Me
59.0
3.90
60.4
4.08
1.4
1.34
0.000
PFH/TAFH
60.52
3.12
61.13
3.21
0.60
1.21
0.009
LAFH/TAFH
57.35
2.28
56.93
2.37
-0.41
0.74
0.004
Paired samples correlation were all higher than 0.892 (p value 0.000)
The categorized vertical dentofacial changes (T1-T0) is brought in Table 3. The
comparison between TG and CG resulted in no statistically significant difference
for PFH/TAFH, SBL-PM and NL-PM (p> 0.05). However, statistically significant
more control group children had a reduction in LAFH/TAFH than treated ones.
91
LAFH/TAFH
-0,02
=
SBL-MP
-0,4
=
-0,5*
PFH/TAFH
NL-MP
-0,5*
TG
-0,41*
CG
+0,3
+0,21 +0,60*
=
=
Figure 1 – Net growth measured in the treatment group (TG) and control group
(CG). Negative values mean measurement reduction between T0 and T1 while
positive values indicate increase.
* indicates statistically significant intra-group difference
= indicates no statistically significant inter-group difference
Figure 1 illustrates the net growth observed between T0 and T1 comparing the
mean values found in treatment and control groups. Negative values indicate
that a measurement reduction, while positive values indicate an increase. In all
variables, there was a coincidence in the direction of growth. The reduction of
SBL.MP and NL.MP angles and LAFH/TAFH ratio, as well as the increase in
the PFH/TAFH ratio are indicative of an improvement in the vertical dentofacial
growth in both TG and CG. The independent t-test comparison of the means
indicates no inter-group statistically significant difference, despite some
variables had a statistically significant different intra-group mean difference
between T0 and T1.
92
Table 3- Comparison between the treatment group (TG) and control group (CG)
for nominal changes in vertical facial proportions (LAFH/TAFH and PFH/TAFH)
and skeletal rotation (SBL-PM and NL-PM) using χ2 test.
T1-T0
Variable
LAFH/TAFH
PFH/TAFH
SBL-PM
NL-PM
Groups
Increase
Decrease
TG
22
17
CG
6
25
p value
Increase
Decrease
23
16
21
10
0.451
Increase
Decrease
19
20
11
20
0.266
Increase
Decrease
20
19
15
16
0.810
0.002
Table 4- Comparison between the treatment group (TG) and control group (CG)
mandibular rotation using an independent sample t-test.
Variables
True rotation
p value
Groups
TG
CG
Mean
-1.24
-0.97
SD
2.62
2.19
SE
0.42
0.39
TG
CG
-0.63
-0.60
2.00
1.59
0.32
0.28
0.935
TG
CG
* Mann Whitney U test
0.61
0.37
1.85
1.68
0.30
0.30
0.581
Apparent rotation
Angular remodeling*
0.643
No statistically significant differences were observed between TG and CG
regarding the mandibular rotation (true or apparent), nor the angular
remodeling. A forward (counterclockwise) mandible growth direction was the
mean behavior of both groups (Table 4).
4. Discussion
As the linear measurements of vertical facial length increased significantly (p
value < 0.000) from T0 to T1 in both groups (Table 2), the authors suppose that
93
the amount of growth in the investigated children allowed the present study.
The morphological pattern of the investigated subjects at baseline is in
agreement with previous published data
[14, 15]
, confirming that mouth breathers
present, in average, an excessive vertical growth. It was found an SNGoGn
angle close to 39º, an NSGn angle of 70º and an ArGo-GoGn angle around
134º (Table 1). Those numbers are representative of a hyperdivergent patient.
Comparing the present investigation findings with those reported previously
[5,6,11-13]
, based only on the treatment group of children, the results are similar.
Mouth breathers who had surgically removed their upper airway obstruction
tend to grow horizontally, with a reduction of their facial hyperdivergence.
However, due to differences in the control groups our conclusions are different.
In the present invstigation both treated and untreated mouth breathers showed
similar vertical facial growth one year prospectively, therefore we can not
conclude that surgical upper airway desobstruction changes the vertical pattern
of growth.
In our study, the control group was composed of severely obstructed children,
with the same respiratory limitations of the treatment group. In the former
publications
[5,6,11-13]
the control group was composed by nasal breathers who
had no histories of upper airway obstruction, nasorespiratory allergy, or
recurrent otitis media. Those children had never undergone adenoidectomies or
orthodontic treatment.
Besides that, the previous researchers used the information that treatment
children had significantly greater lower face heights and steeper mandibular
planes than the control children[6,13], to propose that mandibular growth direction
in the treatment group would keep growing more vertically than an unobstructed
control group.
Such a statement was taken from one of these papers
[6]
: “From the literature
one would expect that a sample of children with severely obstructed
94
nasopharyngeal airways would show a more vertical mandibular growth
direction than would unobstructed matched controls. Following adenoidectomy
and the establishment of nose breathing, growth directions that approach those
of the controls might be expected.”
Considering that mouth breathers will grow always increasing the vertical facial
morphology, the methodology employed previously was adequate. But such an
assumption presented to us an intriguing question: does mouth breathers` face
consistent grow vertically?
The unexpected answer that this group of researchers found was no. In fact, in
a one year follow up, our sample of obstructed control group of children had a
forward growth of the mandible, a reduction in the inclination of mandibular
plane (SBL.MP), a reduction in the divergence of maxilla and mandible
(NL.MP), a reduction in the lower anterior face height ratio to total anterior face
height (LAFH/TAFH), and an increase in the posterior face height ratio to total
anterior face height (PFH/TAFH). All of these characteristics, certified one year
prospectively, change the previous assumption that severely obstructed
children will grow vertically, and thus hint at the necessity of revising the
concept that the improvement in the vertical growth of the face, following T&A,
is merely due to the change of the mode of respiration.
The authors of this study recognize that one year follow up may be an
insufficient length of time to affirm that obstructed mouth breathers will keep
growing within the same pattern. In fact, Lavergne and Gasson [2] have showed
that constancy in face growth direction is not the rule. But, if Waldeyer´s ring
tissues spontaneously decrease with age
[19]
, we can expect that if we could re-
examine those children 5 years later, most of them would have a broader upper
airway, therefore growing with less influence of obstructive tissues.
We studied the vertical growth of the dentofacial complex measuring the
mandibular rotation, the divergence of mandible to the maxilla and the
proportions of the posterior face height and lower anterior face height to anterior
total face height. The choice of these measurements is in agreement with
95
current concepts of cephalometry for this type of investigation.
The rates of true mandibular rotation observed in this study (Table 5) were
similar to those reported previously by papers on the general population
[1,20-22]
.
We found a true forward rotation of -1.24 degree/year for the treatment group
and -0.97 degree/year for the untreated control group. Such rates confirm that
both obstructed and adenotonsillectomized children have a pattern of mandible
growth within normality. The mandible apparent rotation also had a forward
pattern with similar rates (0.6 degree/y) in treatment and control groups, as well
as for those previously reported for the general population in the same age
group [1]. On the basis of this data, the current sample had a forward mandibular
rotation, even in children presenting upper airway obstruction.
The reduction in the mandible to maxilla divergence was the cephalometric
parameter used by Linder-Aronson[5] to affirm that following adenoidectomy and
a switch from mouth to nose breathing, the mandible anterior rotation in the
operated children was greater than in the unobstructed control group. He found,
after a five-year observational period, that the reduction of such divergence in
the treatment group (4.0º) was statistically significantly greater than in the
unobstructed control group (2.3º). However, after the first year of follow up, the
difference in the reduction (0.9º and 0.5º for adenoidectomy and the control,
respectively), was not statistically significant.
In the present investigation it was found a reduction in the divergence between
maxilla and mandible of 0.5º (SD 1.55º) for the treatment group and 0.3º (SD
1.71º) for the untreated control. Such a difference is also not statistically
significant when compared the inter-groups net changes (independent t-test p
value>0.05). However, analyzing the differences within each group, the
reduction of NL-MP from 34.2 to 33.7 in the treatment group is statistically
significant (paired t-test p value <0.05), while the reduction from 33.9 to 33.6 in
the control group is not statistically significant (p value 0.328). Calls attention
the high standard deviation, what indicates that the data are spread out over a
large range of value, therefore needing to be interpreted with caution.
96
Thus, regardless if we consider the five-year observational period inter-group
difference information provided by Linder-Aronson[5] or the one-year follow up
intra-group difference information brought by the present investigation, it seems
that there is a significant reduction in the divergence of the maxilla and the
mandible following adenoidectomy and a switch from mouth to nose breathing.
However, such change must be associated with a clockwise rotation of the
nasomaxillary complex, rather than a counterclockwise rotation of the mandible.
Such
rotation
in
the
adenoidectomy
group
was
illustrated
in
the
superimpositions previously brought by Figures 6 and 7 in the Kerr, McWilliam
and Linder-Aronson[13] paper, as well as in the Zettergren-Wijk, Forsberg,
Linder-Aronson [12] results.
The connection between normalization of nasal breathing and a greater
clockwise rotation of the maxillary anterior portion can be attributed in part to an
improvement in the functionality of the nasal cavity and therefore the stimulus
that such function exerts over the nasal cavity floor downward growth[24].
Facial height, particularly the LAFH and posterior face height PFH, is well
known to be a result of the interplay between condylar growth and sutural and
alveolar development
[25]
. The use of LAFH/TAFH and PFH/TAFH ratios rather
than absolute values is more appropriate in determining facial height patterns
[26]
.
We found that the PFH/TAFH ratio increased both in the treatment group as
well as in the untreated control, but such changes in the proportion of the face
after one-year follow up was significant only for those children who kept mouth
breathing. The same fact was observed regarding LAFH/TAFH. Both groups
had a decrease in the proportion, but the difference was significant only in the
control group (Table 3). In fact, the proportion of the control group children who
had a decrease of LAFH/TAFH was larger than the treated subjects (Table 4).
Therefore, the control group had a facial growth different from what was
supposed previously [6].
Such a finding was unexpected but supports the point of view that using an
97
untreated control group changes the conclusion of previous statements.
As a 5-year follow up with untreated mouth breathing control would be
unpractical, from an ethical and physiological perspective, we suggest that an
increase in the number of children in the control group could add a more robust
confirmation of our findings. Also useful would be a self controlled study design,
where the growth of mouth breathers, one year pre-adenotonsillectomy, could
be compared with the one year post-surgical changes for each patient.
Conclusions
• In the group of adeno-/tonsillectomized children, the mandible showed a
forward rotation, the divergence between maxilla and mandible decreased, the
PFH/TAFH ratio increased and the LAFH/TAFH decreased.
• The untreated control group presented the same pattern of hyperdivergence
reduction.
• The previous concept that normalization of mouth breathing leads to a better
vertical dentofacial growth shoul be revisited.
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100
CAPÍTULO 3
Considerações finais
101
A elaboração de uma tese geralmente parte de um planejamento ideal, mas
durante a sua execução limitações metodológicas muitas vezes se apresentam
aos pesquisadores. Com o intuito de contribuir na execução de pesquisas
futuras, o objetivo deste capítulo foi trazer uma reflexão acerca de algumas
limitações metodológicas, bem como uma síntese desta tese .
Foram apresentados, por meio de artigos, os resultados de três investigações
sobre algumas expectativas que tínhamos a respeito da associação entre a
respiração oral e o crescimento dentofacial. Algumas delas surgiram por
conceitos já estabelecidos na literatura, outras baseadas em algumas
hipóteses plausíveis de serem formuladas sobre este tema.
Optamos pela denominação “expectativa” ao invés de “hipótese” para
diferenciarmos do modelo clássico de uma tese onde o teste de hipóteses
segue um padrão ortodoxo, diferente do aqui adotado.
A revisão da literatura sinalizou que há consenso no conceito de que a
normalização da respiração oral, após a adenoidectomia, favorece um
crescimento facial, no aspecto vertical, mais próximo daquele presente em
crianças sem obstrução nasal. Entretanto, como nestas publicações não é feita
nenhuma menção à época da desobstrução cirúrgica, é razoável criarmos uma
expectativa de que quanto mais cedo for normalizada a respiração, melhor será
o crescimento facial vertical doravante. Considerando a importância desta
informação, para a eleição de um momento mais favorável para uma eventual
intervenção cirúrgica otorrinolaringológica, faz-se necessária a avaliação se
esta expectativa corresponde à realidade. Exatamente isto é que foi abordado
no Artigo 2.
Exceção feita à divergência entre a maxila e a mandíbula, que sofreu maior
redução na dentadura decídua, as outras variáveis cefalométricas examinadas
não apresentaram diferenças significantes estatisticamente. Portanto, os
resultados encontrados neste estudo mostraram que, sob o parâmetro do
102
crescimento facial vertical, não há diferença em operar as crianças durante a
fase de dentadura decídua completa ou na fase de dentadura mista final.
Este achado nos faz refletir se nas áreas médica e odontológica, na ânsia de
atuar terapeuticamente o mais cedo possível, intervenções desnecessárias
(over-treatment) podem estar sendo indicadas. Assim, os clínicos devem ter
cuidado na indicação de terapias cujos resultados não sejam comprovados.
Em função das crianças respiradoras orais desta amostra, tanto dos grupos
tratamento como dos grupos controle, apresentarem ao exame radiográfico
inicial um padrão dolicocefálico (excesso de crescimento vertical), imagina-se
que em algum momento prévio uma disfunção naso-respiratória possa ter
contribuído com tal morfologia facial. Portanto, a época crítica para a
desobstrução cirúrgica poderia ser anterior a aquela investigada. Talvez
durante a fase de irrupção da dentição decídua. Tal suposição é compatível
com a opinião expressa em artigo prévio1 que avaliou este assunto em um
estudo transversal. Entretanto, não é possível descartar a hipótese de que
crianças com padrão morfogenético dolicocefálico sejam mais susceptíveis à
respiração oral e, portanto, a associação entre a obstrução nasal e o aspecto
facial teria uma relação causal inversa, conforme proposto por Warren35 e,
também, Smith e Gonzáles30. Isto se confirmando, a época da desobstrução
das vias aéreas superiores pouco interferiria com o padrão facial vertical.
Estudos complementares são necessários para elucidar tal dúvida.
A consideração feita por Linder-Aronson, Woodside e Lundstrom19 que, sob o
ponto de vista científico, seria melhor que o grupo controle fosse composto por
indivíduos doentes, sem tratamento, coloca em questionamento o conceito
previamente estabelecido, pelo grupo liderado pelo próprio autor principal, que
a adenoidectomia propicia um crescimento facial vertical mais próximo da
normalidade.
Um novo desenho metodológico, onde no grupo controle a doença expressaria
a sua história natural, elucidaria esta questão. Esta investigação foi
apresentada nos Artigos 2 e 3. Tal metodologia somente foi possível, sob o
103
ponto de vista ético, uma vez que a autorização para a cirurgia
otorrinolaringológica, de responsabilidade das autoridades públicas de saúde
na região metropolitana de Belo Horizonte, rotineiramente leva um prazo
aproximado de um ano para ser obtida.
Os resultados mostraram que, no grupo submetido à adenotonsilectomia, o
padrão de crescimento facial tendeu a ser horizontal, reduzindo a
hiperdivergência facial. Portanto, coincidindo com os achados prévios descritos
na literatura14,18,19,37.
Entretanto, nas crianças respiradoras orais não tratadas do grupo controle, o
comportamento do crescimento facial vertical foi semelhante ao grupo
tratamento. Desta maneira, as conclusões por nós estabelecidas são
antagônicas aquelas apresentadas anteriormente. Os nossos achados
sugerem que o crescimento facial vertical, após a adenotonsilectomia, não
corresponde à expectativa prévia.
A grande variabilidade do padrão morfológico facial vertical nas crianças
analisadas nos Artigos 2 e 3, bem como a falta de um cálculo amostral prévio,
contribuíram para que algumas das variáveis estudadas apresentassem um
baixo poder ao testes estatísticos (1-β). Assim, os nossos achados ficaram
expostos a erros do Tipo II (β), isto é termos resultados falso-negativo onde a
hipótese nula é aceita quando a hipótese alternativa é que é a verdadeira.
Em virtude das limitações temporais impostas pela necessidade de defesa da
tese de doutoramento, o tamanho da amostra foi balizado pelos artigos que
estudaram este assunto anteriormente14,18,19,21,36,37. Como o número de
crianças investigadas naqueles artigos foi menor ou igual a 38, estabelecemos
tal n como uma meta mínima para o nosso estudo. Assim, na presente
investigação trabalhou-se com as 39 crianças disponíveis para o grupo
tratamento na data limite para o fechamento dos dados que seriam analisados.
A nossa meta seria alcançar para o grupo controle, no mínimo, o mesmo
número de crianças, mas manter as crianças que não haviam sido operadas,
sob um controle longitudinal, não foi tarefa fácil. Fatores como a) perda de
104
contato com a família, b) desistência pela longa espera pela cirurgia, c) ter sido
operado ao longo do período observacional, fizeram com que o número de
crianças no grupo controle fosse menor do que o idealizado (n=31).
Entretanto, em virtude da relevância dos achados aqui apresentados, é
essencial a continuidade da coleta de dados no AROHC-UFMG, aumentando o
tamanho da amostra o que poderia contribuir com o aumento do poder dos
testes estatísticos e, consequentemente, maior robustez às inferências aqui
introduzidas.
De qualquer maneira, com a grande variabilidade apresentada nas medidas
cefalométricas utilizadas, mesmo com amostras enormes, estaríamos sujeitos
a erros do Tipo II. Se esta variabilidade for uma característica do crescimento
facial vertical, pouco poderia ser feito. Entretanto, uma opção seria buscar
medidas cefalométricas onde o desvio-padrão fosse menor.
Nós optamos pelas medidas cefalométricas aqui apresentadas por aceitarmos
as considerações de Tollaro, Baccetti & Franchi33 que a linha cefalométrica
mais estável para estudos com crianças muito jovens é a SBL. Entretanto,
avaliações do padrão facial vertical podem ser feitas com inúmeras outras
medidas cefalométricas, que talvez apresentem menor variabilidade em torno
da média. Isto é, perderíamos em função da menor confiabilidade da referência
anatômica, porém ganharíamos em função da maior confiabilidade do poder
dos testes estatísticos.
Como exercício para solucionar esta limitação de nosso estudo, procuramos
avaliar o poder do teste (1-β) de artigos que estudaram previamente este
assunto utilizando, porém, outras medidas cefalométricas13,14,21,34,37. De forma
unânime, em todas aquelas publicações encontramos também medidas
cefalométricas com um baixo poder estatístico.
Todavia, segundo Soares e Siqueira31, em estudo onde o tamanho da amostra
é fixo, que é o nosso caso pela imposição temporal da coleta de dados, não há
como controlar simultaneamente ambos os erros (Tipos I e II). Assim,
105
convencionou-se que o erro mais sério seria do Tipo I. Em um segundo
momento, calcula-se o tamanho da amostra que reduza a probabilidade do erro
do Tipo II a níveis aceitáveis.
Outra consideração importante de ser postada é que a presença de rinite
alérgica não foi considerada. Dois motivos nos levaram a esta decisão: a) o
tratamento desta patologia é de baixa previsibilidade de resultados, dificultando
o controle desta variável e b) os estudos prévios também não consideraram
este fator etiológico. Somos da opinião que a solução do problema respiratório
após a adeno-/tonsilectomia, com o consistente relato que a criança não mais
apresenta roncos noturnos, permanecendo com a boca fechada, é um dado
soberano que indica que independentemente da presença de rinite alérgica
houve uma mudança do padrão respiratório de bucal para nasal.
As informações previamente apresentadas na literatura sinalizam que as
crianças respiradoras orais têm maior prevalência de algumas más oclusões,
como a classe II, a mordida aberta anterior e a mordida cruzada posterior. Tal
conceito gera uma expectativa que, diante de um respirador oral, as referidas
anomalias sejam frequentemente encontradas. Além do mais, imagina-se que
quanto maior a obstrução das vias aéreas superiores, maior será a prevalência
de tais más oclusões. Assim, no Artigo 1 é apresentado o estudo da
associação entre a prevalência destas más oclusões e a respiração oral. Os
resultados confirmaram que a prevalência de mordida cruzada posterior é
maior nos respiradores orais, do que na população em geral. Da mesma forma,
crianças nas fases de dentaduras mista e permanente têm maior prevalência
de mordida aberta anterior e classe II. Entretanto, contrariando as nossas
expectativas, a severidade da obstrução nasal não mostrou associação com as
más oclusões estudadas, além de que a maioria das crianças respiradoras
orais não é portadora de anormalidade na relação dentária inter-arcos.
Como os dados para a elaboração do Artigo 1 foram oriundos dos prontuários
das crianças do AROHC-UFMG, importantes informações epidemiológicas que
poderiam ser levantadas sobre a relação dentária intra-arco e inter-arcos não
106
puderam ser coletadas, uma vez que quando da idealização dos prontuários
estes dados não foram considerados relevantes.
Por exemplo, sentimos que a quantificação dos trespasses dentários vertical
(overbite) e horizontal (overjet), bem como a mensuração da proporção entre
largura e profundidade maxilar, poderiam contribuir significativamente com o
entendimento sobre a relação entre respiração oral e más oclusões.
Ainda no Artigo 1, a ausência de um grupo composto por crianças com padrão
respiratório
normal
que
serviria
de
controle
para
as
comparações
epidemiológicas foi outra limitação metodológica. Assim, foi necessário
comparar nossas crianças com dados prévios da literatura.
Considerou-se a possibilidade de um levantamento epidemiológico que
buscasse conhecer a prevalência das más oclusões estudadas na população
geral de Belo Horizonte. Entretanto, respeitamos uma recomendação anterior
do COEP-UFMG, onde diagnosticar lesões de cárie e más oclusões e não dar
algum encaminhamento para a solução do problema poderia gerar um
desconforto emocional aos pacientes e, portanto, seria desaconselhável
eticamente.
Conclusões:
. A prevalência de mordida cruzada posterior foi maior na população de
respiradores orais do que na população geral, independentemente dos estágios
de desenvolvimento da oclusão.
. A prevalência de mordida aberta anterior e de má oclusão de classe II foi
maior nas crianças mais velhas (dentaduras mista e permanente) do que nas
mais novas (dentadura decídua).
. Não houve associação entre a causa da respiração oral (hiperplasia de
adenóide, hiperplasia de amígdala, rinite e respiração oral funcional) e a
presença de má oclusão de classe II, mordida aberta anterior e mordida
cruzada posterior.
107
. A maioria das crianças respiradoras orais apresentou uma relação oclusal
inter-arcos normal.
. Não houve diferença no padrão de crescimento facial vertical quando a A+A
foi realizada na fase de dentadura decídua ou na fase de dentadura mista
inicial.
.
As
crianças
submetidas
a
A+A
tiveram
um
crescimento
facial
predominantemente horizontal, semelhante ao comportamento dos pacientes
operados descritos na literatura.
. As crianças que permaneceram obstruídas por 1 ano também tiveram um
crescimento facial predominantemente horizontal.
. É necessária uma revisão das conclusões previamente apresentadas na
literatura sobre o impacto da desobstrução cirúrgica das vias aéreas superiores
sobre o padrão de crescimento facial vertical.
108
APÊNDICES E ANEXOS
Apêndice 1 – Termo de Consentimento Livre e Esclarecido
Título do projeto: O impacto da desobstrução cirúrgica das vias aéreas superiores no crescimento e desenvolvimento dento-facial,
em dois estágios da maturação biológica das crianças.
Objetivo do estudo: O objetivo do estudo é avaliar o impacto da desobstrução cirúrgica das vias aéreas superiores no crescimento e
desenvolvimento dento-facial de crianças do projeto do Respirador Oral do HC-UFMG, em dois estágios de maturação.
Procedimentos: Se você concordar em participar deste estudo, os dados coletados nos exames feitos no Projeto do Respirador Oral
do HC-UFMG, do menor sob sua responsabilidade, serão utilizados para efeito deste estudo. Os exames são: anamnese,
fibronasoscopia, medição da resistência nasal inspiratória nasal e bucal, modelos ortodônticos de gesso, radiografia de mão e punho,
radiografia panorâmica, telerradiografia em norma lateral da face, fotografias intra e extra bucais, questionário sobre os sinais e
sintomas pós-cirúrgicos.
Riscos e desconfortos: Você ou o menor sob a sua responsabilidade não serão expostos a riscos. A criança deverá seguir a rotina de
consultas e exames indicados pelo médico e/ou dentista assistente.
Benefícios: A realização deste estudo vai ajudar na compreensão da correlação entre o momento da desobstrução cirúrgica das vias
aéreas superiores e o impacto sobre o crescimento e desenvolvimento dento-facial. Assim, poderemos indicar qual é o melhor
momento de indicar as cirurgias desobstrutivas, do ponto de vista ortodôntico. Você não receberá nenhum pagamento e não terá
custos para que o menor, sob a sua responsabilidade, participe deste estudo.
Possíveis dúvidas sobre o estudo: Este consentimento explica o estudo. Por favor, leia-o cuidadosamente. Pergunte sobre qualquer
ponto que não tenha entendido. Se não tiver dúvidas agora, pode perguntar mais tarde. Durante o estudo, você será informado sobre
qualquer fato novo que possa influenciar seu desejo de continuar participando. Se você desejar falar com alguém sobre este estudo
por julgar que não recebeu um tratamento adequado ou que foi prejudicado ao participar, ou se tiver qualquer outra questão relativa
ao estudo, você deve telefonar para os pesquisadores: Dr. Bernardo Quiroga Souki (xx-31) 3286-5108, Dra. Helena Becker (xx31)3248-9583 ou Dr. Jorge Andrade Pinto (xx-31) 32489822, ou para o Comitê de Ética da UFMG (xx-31) 3248-9364.
A UFMG não tem nenhum programa para reembolsá-lo na ocorrência de danos ou acidentes que não são de responsabilidade dos
médicos e pesquisadores.
Confidencialidade das informações: As informações obtidas serão mantidas nos limites de confidencialidade garantidos pela lei.
Entretanto, a legislação obriga a notificação de doenças infecciosas e maus tratos infantis. Em certas situações, pessoas responsáveis
por assegurar que o estudo foi conduzido apropriadamente poderão rever os seus dados. Estas pessoas manterão seus dados
confidenciais. Pessoas não envolvidas no estudo não terão acesso a nenhuma de suas informações pessoais a não ser que você dê
permissão.
Participação voluntária no estudo: Você (o menor sob a sua responsabilidade) não é obrigado a participar deste estudo e pode
desistir a qualquer momento. Se decidir não participar, sua relação com os médicos e dentistas não será modificada de nenhuma
forma.
O que significa a sua assinatura: Ao assinar este documento, você demonstra ter entendido as informações sobre o estudo e estar
disposto a participar do projeto descrito na página anterior.
VOCÊ RECEBERÁ UMA CÓPIA DESTE CONSENTIMENTO
________________________________________
Assinatura da criança (se aplicável)
__/___/___
Data
________________________________________
Assinatura do pai/mãe ou responsável legal
__/___/___
Data
________________________________________
Assinatura do pesquisador
__/___/___
Data
________________________________________
Assinatura da testemunha
__/___/___
Data
Observação: Cópias assinadas deste consentimento deverão ser a) arquivadas pelo pesquisador principal, b) anexadas ao prontuário
do paciente e c) fornecidas ao paciente.
109
Apêndice 2 – Dados brutos do Artigo 1
Genero
1
1
1
2
2
2
1
2
2
2
1
1
1
2
2
2
1
1
1
2
1
1
1
2
2
1
1
2
2
1
2
1
2
2
2
2
1
2
1
2
2
1
1
1
2
1
1
2
Idade
3,7
10,5
2,9
4,2
7,8
8,0
8,5
5,6
9,2
5,3
4,8
4,7
3,8
5,8
11,9
4,0
7,3
8,2
6,1
9,2
8,7
10,2
5,2
8,9
3,4
9,0
7,9
6,7
9,2
8,1
3,4
4,2
7,3
9,4
12,7
11,5
5,3
5,0
11,6
7,6
11,3
5,6
5,6
2,9
7,6
3,6
7,0
3,4
MAA
Class II
9
1
9
1
9
9
9
3
1
2
3
3
1
1
1
1
1
2
1
3
1
2
1
1
3
2
1
1
1
1
1
3
3
1
1
1
9
3
3
1
3
3
2
2
1
1
1
2
9
2
9
1
9
9
9
4
2
1
2
2
3
3
2
2
1
2
2
2
2
2
3
4
4
3
2
1
2
3
2
2
3
2
2
2
9
3
2
3
3
3
2
2
2
2
3
3
MCP
Dent
9
1
9
1
9
9
9
3
1
1
3
2
1
1
2
1
1
1
1
3
1
1
1
2
2
1
1
1
1
3
3
1
1
1
1
2
9
1
1
3
1
2
1
1
3
9
1
1
Amigd
9
2
9
1
9
9
9
1
2
1
1
1
1
2
3
1
2
2
2
2
2
2
1
2
1
2
2
2
2
2
2
1
2
2
3
2
9
2
2
2
3
2
1
1
1
1
2
1
4
1
3
2
2
1
1
1
1
4
2
2
2
3
2
4
3
2
4
2
2
1
4
2
3
1
1
3
1
2
3
2
2
1
3
1
3
1
2
4
1
2
2
1
1
4
4
4
Adenoid
4
2
4
1
2
1
2
2
4
4
1
4
4
4
2
3
2
2
3
4
1
1
3
2
3
2
1
2
3
3
3
3
3
3
1
3
3
3
2
3
2
2
3
1
3
1
1
2
Rinite
1
1
2
2
1
2
1
1
1
2
1
1
2
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
2
1
2
1
1
1
2
1
2
1
1
110
1
1
1
2
1
1
2
2
1
2
2
2
1
2
2
2
1
2
1
1
1
1
1
1
2
2
1
2
2
1
1
1
1
2
1
2
1
1
2
1
1
2
1
1
1
1
2
2
1
2
2
1
2
9,1
3,9
5,8
10,8
3,7
2,7
7,3
1,4
11,4
5,3
4,4
4,5
4,0
6,5
6,6
12,9
3,4
3,9
7,4
3,8
3,1
6,6
10,4
6,6
11,2
3,9
10,3
9,5
8,1
3,1
3,6
8,0
11,1
6,7
6,0
3,7
5,0
8,2
4,8
6,1
6,9
5,6
7,6
8,8
5,4
2,3
6,8
3,7
7,2
4,4
2,8
3,3
10,0
1
3
3
1
9
1
1
9
2
1
1
1
3
2
9
1
1
3
1
9
3
2
3
2
3
1
1
1
9
2
2
9
3
9
2
3
3
3
3
3
1
3
9
1
1
1
3
1
1
2
2
1
1
2
2
2
1
9
1
4
4
3
2
2
2
2
3
1
2
2
2
2
9
2
3
1
3
3
4
2
9
1
2
9
2
1
3
3
2
2
3
2
2
2
9
1
4
3
2
3
2
2
2
1
1
3
1
1
1
9
1
1
3
1
1
1
1
1
1
1
1
1
1
1
9
2
1
3
1
3
1
2
1
9
1
1
9
1
1
1
3
1
1
1
2
1
3
9
1
2
1
3
1
1
1
1
1
1
2
1
1
2
9
1
2
1
3
1
1
1
1
2
2
3
1
1
2
1
1
2
3
2
2
1
2
2
9
1
1
9
3
2
2
1
1
2
2
2
2
1
9
2
2
1
2
1
2
1
1
1
2
1
4
1
1
1
3
2
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3
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2
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11,7
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7,0
2,7
6,8
5,8
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6,5
4,2
5,7
4,3
8,8
11,2
2,9
3,8
4,5
6,2
9,8
3,0
8,2
5,1
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5,1
5,3
3,4
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9,8
8,8
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4,9
10,8
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3,5
7,7
5,5
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6,8
7,2
3,5
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12,2
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11,6
3
3
3
9
1
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1
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11,4
6,9
5,2
4,5
6,0
4,9
11,6
6,0
6,6
7,9
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4,8
11,3
5,3
10,6
7,6
4,9
7,0
5,8
6,3
5,2
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3,9
6,1
5,8
3,8
2,3
11,5
4,4
8,9
10,9
9,4
8,8
8,0
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3,3
7,5
11,4
3,8
5,6
2,7
6,3
6,6
3,7
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4,5
10,9
8,4
12,7
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2,7
2
2
3
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9
1
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3
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113
1
1
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1
1
2
2
1
1
1
2
2
1
1
1
2
1
2
1
1
7,9
5,8
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2,7
4,0
11,6
5,6
8,5
9,3
4,5
7,1
3,9
2,3
5,2
6,1
4,4
3,2
5,7
10,1
10,1
3,6
4,9
4,4
5,8
3,1
4,1
3,0
4,5
5,5
5,4
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4,7
3,5
2,0
11,9
6,1
3,2
2,7
8,0
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6,9
2,8
2,1
4,4
4,4
3,5
2,0
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3
1
1
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2
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1
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8,2
6,4
6,2
6,6
6,1
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6,5
5,4
4,9
9,9
3,0
10,6
10,4
9,4
3,5
13,9
5,4
8,1
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11,3
5,9
2,5
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6,3
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10,1
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7,7
4,8
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6,7
3,8
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2,5
8,3
4,4
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12,6
12,5
11,3
6,7
11,7
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5,0
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3,4
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3
1
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1
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2,3
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10,7
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3,4
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3,4
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9,6
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4,6
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3
2
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2
1
2
1
1
2
2
2
2
1
1
1
1
1
1
1
2
2
2
1
1
2
2
2
2
2
2
1
1
1
1
1
2
1
2
2
2
1
1
1
1
1
2
1
1
2
1
2
2
7,3
4,4
5,0
6,6
4,3
10,4
5,3
4,0
1,7
6,4
5,3
10,4
7,5
9,7
2,5
4,4
3,7
7,5
15,3
9,3
6,3
10,6
5,8
2,9
6,7
4,5
10,5
5,4
8,7
4,2
10,2
4,1
4,8
6,6
7,8
2,3
11,1
8,9
5,7
9,5
5,4
5,1
5,6
4,7
7,2
7,4
4,0
6,2
2,4
7,2
9,1
8,6
9,8
1
3
1
9
1
1
1
1
9
1
9
1
9
3
9
3
2
1
1
2
1
1
1
1
1
1
1
9
1
3
1
3
1
1
2
2
2
3
2
3
1
1
2
1
3
3
9
2
9
1
1
1
1
3
3
2
3
2
3
4
2
9
9
9
2
2
4
9
2
3
3
2
2
2
2
3
2
1
1
4
9
2
2
2
3
2
1
2
3
2
3
2
2
2
3
3
2
4
9
9
3
9
3
4
3
2
2
1
1
3
1
2
3
1
9
3
9
1
1
9
9
1
1
1
1
1
1
1
1
1
1
1
1
9
1
3
1
1
1
1
1
1
1
1
1
1
1
1
1
1
3
1
9
1
9
1
1
1
2
2
1
1
2
1
2
1
1
9
1
9
2
2
2
9
1
1
2
2
2
2
2
2
2
2
1
3
9
2
1
2
1
1
2
2
1
3
2
2
2
1
1
2
1
2
2
1
1
1
2
2
2
2
2
3
3
3
3
1
4
3
2
2
3
4
4
1
2
3
4
3
3
2
1
1
1
2
2
2
1
1
1
2
1
1
3
2
1
2
1
1
2
2
3
4
1
3
3
1
3
4
3
3
2
1
4
4
4
3
4
3
1
3
3
3
3
4
1
1
1
3
4
4
1
3
3
1
3
2
4
4
3
2
2
3
3
2
2
3
1
1
3
1
1
4
2
4
1
1
4
3
3
1
2
4
3
4
1
2
1
2
1
1
2
1
2
1
1
1
9
9
9
9
9
9
9
9
9
9
1
9
9
9
9
9
9
1
9
9
9
1
1
9
2
2
1
9
1
1
1
2
1
2
1
1
9
1
2
9
1
1
2
117
1
2
1
1
2
2
2
2
2
1
1
2
1
1
1
2
2
1
1
2
1
2
1
2
2
5,7
9,3
5,0
10,1
6,8
10,3
4,2
5,9
8,4
6,2
7,9
7,4
2,1
6,3
5,2
8,1
11,0
3,5
9,2
4,3
5,3
7,1
8,8
4,5
9,8
1
3
1
1
3
2
1
1
3
3
2
1
1
3
1
2
2
9
1
3
1
9
1
1
1
2
2
2
3
4
3
1
3
1
3
2
2
1
2
3
2
2
9
2
2
2
9
1
1
2
1
1
3
1
2
3
1
2
1
3
9
1
1
2
1
1
1
9
1
1
3
9
1
1
1
2
2
1
2
2
2
1
1
2
2
2
2
1
2
1
2
2
1
2
1
1
9
2
1
2
3
1
1
2
1
2
3
4
1
1
2
4
2
5
3
4
1
2
2
2
2
2
2
2
1
Legenda:
Gênero: 1 (masculino), 2(feminino)
Vert (relação vertical): 1 (normal), 2 (mordida profunda), 3 (mordida aberta anterior)
Sag (relação sagital): 1 (normal), 2 (classe I), 3 (classe II), 4 (classe III)
Trans (relação transversal: 1 (normal), 2 (mordida cruzada posterior, 3 (mordida cruzada
posterior com desvio
Dent (dentadura): 1 (decídua), 2 (mista), 3 (permanente)
Amigd (amigdala): 1 (grau 1), 2 (grau 2, 3 (grau 3), 4 (grau 4), 5 (não avaliada)
Adenoid (adenóide): 1 (<60%), 2 (60%-75%), 3 (75%-90%), 4 (>90%, 5 (não avaliada)
Rinite: 1 (presente), 2 (ausente), 9 (não avaliada)
5
3
3
1
3
4
4
4
1
4
1
2
3
1
2
3
1
3
1
1
4
4
4
3
1
1
1
1
9
9
9
2
2
1
9
2
2
1
1
1
1
9
1
1
2
9
1
1
9
1
118
Apêndice 3 – Dados brutos dos Artigos 2 e 3
Gener
o
2
1
2
2
2
1
1
1
1
1
1
1
1
2
2
1
1
2
2
1
1
1
2
1
1
2
Den
t
2
2
2
2
2
1
2
2
2
2
1
2
1
1
1
2
1
2
2
2
1
1
1
2
2
2
Idad
e
9,8
7,4
6,8
9,0
7,7
4,3
6,3
7,8
5,9
10,9
5,3
9,2
4,7
3,6
5,6
10,5
6,6
8,1
8,1
5,9
4,9
5,4
4,1
6,3
6,0
6,8
Cirurgi
a
2
2
1
1
1
1
2
1
1
2
2
2
2
1
2
1
2
2
1
1
1
1
1
1
1
1
SBLPM
1
37,0
37,5
44,0
45,0
44,0
40,0
47,0
38,0
49,0
40,0
44,0
37,5
40,0
41,5
41,0
52,5
41,0
46,0
38,5
37,0
39,5
47,0
34,5
40,5
42,0
40,5
NLPM
1
39,0
28,0
35,0
32,0
40,0
37,0
37,0
33,0
39,0
33,0
32,0
30,0
37,5
33,0
33,0
33,5
33,0
35,0
31,0
36,0
40,0
32,0
30,0
33,0
37,5
33,5
SBLGo
1
69,0
65,0
59,0
61,0
65,5
53,0
61,5
73,5
54,0
68,5
64,0
65,5
59,0
57,0
59,5
63,5
64,5
62,5
65,0
65,0
59,5
58,0
62,0
64,5
63,0
61,0
SBLMe
1
113,5
104,0
100,0
104,0
111,0
87,0
106,5
113,0
100,0
113,0
102,0
102,0
93,0
87,0
100,0
117,5
107,5
107,0
107,0
102,0
95,0
97,0
93,5
99,0
103,0
105,0
NLMe
1
67,0
59,0
58,0
56,5
66,0
51,0
57,5
63,0
62,0
62,0
57,0
57,0
57,5
51,0
57,5
71,0
61,5
60,0
61,0
58,0
58,0
55,0
54,0
55,0
57,5
58,0
SBLPM
2
36,5
37,0
44,0
45,0
44,0
41,0
48,5
40,0
48,0
40,0
43,0
37,0
39,5
42,0
42,0
54,0
43,5
45,0
39,0
35,0
39,5
48,0
34,0
40,0
42,5
41,0
NLPM
2
36,0
27,0
33,0
30,0
39,0
35,0
35,0
31,5
39,0
33,0
33,5
31,0
40,0
34,0
33,5
38,5
34,0
33,0
30,0
36,0
40,0
32,0
31,0
33,5
39,0
34,0
SBLGo
2
71,0
64,0
60,0
62,0
67,0
56,5
62,0
74,0
54,0
70,0
67,0
66,0
59,5
59,5
61,0
63,0
67,0
64,0
65,0
65,0
59,0
58,0
66,0
66,0
62,0
62,5
SBLMe
2
117,0
106,0
104,0
107,0
114,0
94,0
109,5
115,0
102,0
117,0
107,0
105,0
95,0
92,0
103,0
120,0
113,0
110,0
109,0
105,0
95,5
100,0
100,0
102,0
103,5
108,0
NLMe
2
69,0
58,0
59,0
58,0
67,0
55,0
59,0
63,0
62,5
64,0
59,0
58,0
58,0
53,0
58,5
72,0
64,5
63,0
63,0
60,0
58,5
57,0
59,0
57,0
58,5
60,0
RotRea
l
0,0
-3,3
0,5
-1,7
1,1
-0,7
0,0
4,5
-4,0
-0,8
-2,1
-1,0
-0,1
1,1
0,0
0,0
0,5
-1,0
-1,1
-2,6
-0,8
1,1
0,8
-3,4
-2,5
0,0
RotAp
a
-0,6
-0,5
0,0
0,0
0,0
1,5
1,7
3,0
-1,3
0,0
-1,1
-0,5
-0,1
0,5
1,1
2,2
2,3
-1,0
0,5
-1,8
0,0
1,1
-0,8
-0,6
0,4
0,7
119
1
1
1
1
1
1
1
2
1
2
2
1
1
1
1
1
1
1
2
1
1
1
2
2
1
2
1
1
1
2
2
2
1
1
1
2
2
1
2
2
1
2
1
1
1
2
2
2
1
2
2
2
1
2
2
1
2
2
2
2
1
1
2
2
5,7
5,1
4,9
7,6
5,0
3,6
6,4
6,3
5,5
6,2
4,6
4,3
3,7
9,6
8,7
5,9
5,3
7,6
8,3
6,0
4,0
7,2
9,2
5,9
8,6
6,3
7,3
6,0
6,2
3,5
9,4
8,8
1
1
1
1
1
1
2
2
2
1
2
1
2
2
2
2
2
2
2
1
2
2
1
2
2
2
1
1
2
1
2
1
47,0
39,0
44,5
39,0
54,0
44,0
40,0
40,5
43,5
36,5
41,5
46,5
41,0
53,0
32,0
49,0
47,0
41,0
47,5
42,0
39,0
41,0
39,0
39,0
38,0
37,0
48,0
37,0
44,0
36,5
44,0
40,0
37,0
35,0
36,0
29,0
46,0
37,0
34,0
27,5
39,5
34,0
42,0
40,0
38,0
37,0
29,0
37,0
37,0
32,0
32,0
34,0
33,0
29,0
30,0
29,0
29,0
31,0
36,0
35,0
35,0
27,5
38,0
37,0
60,0
61,5
56,0
65,0
56,0
58,0
68,0
61,5
61,0
60,0
53,0
64,0
50,0
61,0
72,0
54,0
59,0
62,5
57,5
65,5
61,0
70,0
65,0
65,0
69,0
59,5
61,0
66,0
63,0
56,5
68,0
66,0
104,0
95,5
96,0
103,5
101,0
94,0
107,0
102,0
100,0
96,0
88,0
99,0
85,0
114,5
104,0
102,0
102,0
102,5
101,0
103,0
100,0
114,0
109,0
103,0
110,0
100,0
105,0
105,5
104,0
88,0
112,0
107,0
56,0
56,5
55,0
55,0
59,0
53,0
61,0
59,5
56,0
53,0
56,0
56,0
50,0
70,0
56,0
62,0
60,5
58,5
56,0
62,0
57,0
62,0
63,0
60,0
64,0
55,5
62,0
60,0
57,5
50,0
64,0
55,5
47,0
35,0
42,0
36,5
51,0
42,0
38,0
39,0
42,0
36,0
41,0
46,0
40,0
52,5
32,5
50,0
48,0
39,0
45,0
38,0
37,0
40,0
38,0
39,0
38,0
37,5
46,5
35,0
39,5
35,0
43,0
39,0
37,0
33,0
35,0
27,5
43,5
36,0
33,0
27,0
37,5
33,0
41,0
38,0
37,0
33,5
28,0
36,0
36,0
32,0
32,0
35,0
35,0
30,0
30,5
30,0
31,0
34,0
34,0
35,0
33,0
27,0
35,0
35,0
61,5
66,0
61,5
69,5
59,5
62,5
73,5
65,0
63,0
62,5
57,5
66,0
53,0
63,5
74,0
56,5
61,0
67,5
61,0
70,0
66,0
70,5
68,0
67,0
72,0
61,0
64,0
69,0
68,0
61,5
72,5
68,5
106,5
100,5
102,0
106,0
106,0
100,0
113,0
104,0
103,0
97,0
92,5
102,0
87,0
117,5
106,0
106,0
105,0
107,0
104,0
108,0
105,5
114,0
113,0
106,0
112,0
101,0
110,0
105,5
109,0
94,0
115,0
109,5
57,5
59,0
57,5
55,5
60,0
56,0
63,0
59,0
57,5
52,0
58,5
57,0
51,0
71,0
56,0
64,0
62,0
61,0
56,5
61,5
60,0
61,0
64,0
61,0
64,0
54,5
65,0
60,0
61,5
54,0
66,0
57,5
-0,3
-5,6
-1,6
-7,6
-1,6
-1,4
-2,7
-1,8
0,0
0,0
3,8
1,2
1,0
-2,9
3,0
1,1
0,6
-2,0
-2,7
-6,3
-7,0
-1,5
0,2
-2,5
1,0
-2,1
-2,6
-6,8
-5,7
-3,8
-1,6
1,0
0,0
-4,4
-3,9
-3,5
-3,2
-2,7
-2,7
-1,8
-0,7
-0,6
-0,6
-0,6
-0,5
-0,5
0,5
0,6
0,6
-2,6
-1,7
-5,0
-2,8
-0,5
-0,3
0,0
0,0
0,5
-1,9
-2,3
-6,4
-1,9
-1,1
-1,0
120
2
2
1
1
1
1
2
1
1
1
2
1
1
2
2
1
2
1
2
2
2
2
2
1
5,3
6,1
7,8
6,7
6,5
5,1
9,5
6,9
7,2
10,6
10,2
4,8
1
2
1
1
1
2
1
1
1
1
1
2
43,0
44,5
40,0
37,0
50,0
43,0
35,0
37,0
35,0
45,0
53,0
36,0
35,0
37,0
30,0
31,0
36,0
34,0
27,0
30,0
30,0
32,5
37,0
34,0
55,5
57,0
70,5
63,0
56,5
61,0
72,0
61,0
72,5
70,0
66,5
61,0
94,0
98,5
114,0
103,5
106,0
100,0
114,5
96,0
108,5
115,0
117,0
96,0
54,0
57,0
61,0
58,0
64,0
57,5
63,5
54,0
58,0
64,0
67,0
54,0
42,5
44,0
40,0
42,0
47,0
42,0
35,0
37,0
36,0
43,5
53,0
37,0
33,0
35,0
26,0
30,0
36,0
34,0
27,0
30,0
30,0
33,0
38,5
36,0
57,5
59,0
74,0
66,0
59,0
65,5
77,5
63,0
75,0
75,0
70,0
65,0
97,0
100,0
114,0
108,0
107,0
103,0
117,0
99,0
112,0
120,0
122,0
102,0
56,0
58,0
66,0
61,0
65,0
60,0
65,0
56,0
60,0
67,5
72,0
58,0
-1,1
-1,1
-2,7
2,1
-0,8
0,0
-2,1
-2,1
3,9
-2,7
0,0
0,5
-0,5
-0,3
0,0
5,2
-2,5
-0,9
0,0
0,0
1,3
-2,0
0,0
1,1
121
Anexo 1: Cópia da aprovação do projeto no Comitê de Ética em Pesquisa
da Universidade Federal de Minas Gerais.
122
Anexo 2: Artigo 1 – versão impressa da Revista International Journal of
Pediatric Otorhinolryngology.
Author's personal copy
International Journal of Pediatric Otorhinolaryngology 73 (2009) 767–773
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology
journal homepage: www.elsevier.com/locate/ijporl
Prevalence of malocclusion among mouth breathing children: Do expectations
meet reality?
Bernardo Q. Souki a,b,*, Giovana B. Pimenta a, Marcelo Q. Souki a, Leticia P. Franco a, Helena M.G. Becker a,
Jorge A. Pinto a
a
b
Federal University of Minas Gerais, Outpatient Clinic for Mouth-Breathers, Belo Horizonte, Brazil
Catholic University of Minas Gerais, School of Dentistry, Orthodontics, Belo Horizonte, Brazil
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 25 November 2008
Received in revised form 9 February 2009
Accepted 11 February 2009
Available online 12 March 2009
Objective: The aim of this study was to report epidemiological data on the prevalence of malocclusion
among a group of children, consecutively admitted at a referral mouth breathing otorhinolaryngological
(ENT) center. We assessed the association between the severity of the obstruction by adenoids/tonsils
hyperplasia or the presence of allergic rhinitis and the prevalence of class II malocclusion, anterior open
bite and posterior crossbite.
Methods: Cross-sectional, descriptive study, carried out at an Outpatient Clinic for Mouth-Breathers.
Dental inter-arch relationship and nasal obstructive variables were diagnosed and the appropriate crosstabulations were done.
Results: Four hundred and one patients were included. Mean age was 6 years and 6 months (S.D.: 2 years
and 7 months), ranging from 2 to 12 years. All subjects were evaluated by otorhinolaryngologists to
confirm mouth breathing. Adenoid/tonsil obstruction was detected in 71.8% of this sample, regardless of
the presence of rhinitis. Allergic rhinitis alone was found in 18.7% of the children. Non-obstructive mouth
breathing was diagnosed in 9.5% of this sample. Posterior crossbite was detected in almost 30% of the
children during primary and mixed dentitions and 48% in permanent dentition. During mixed and
permanent dentitions, anterior open bite and class II malocclusion were highly prevalent. More than 50%
of the mouth breathing children carried a normal inter-arch relationship in the sagital, transversal and
vertical planes. Univariate analysis showed no significant association between the type of the
obstruction (adenoids/tonsils obstructive hyperplasia or the presence of allergic rhinitis) and
malocclusions (class II, anterior open bite and posterior crossbite).
Conclusions: The prevalence of posterior crossbite is higher in mouth breathing children than in the
general population. During mixed and permanent dentitions, anterior open bite and class II malocclusion
were more likely to be present in mouth breathers. Although more children showed these malocclusions,
most mouth breathing children evaluated in this study did not match the expected ‘‘mouth breathing
dental stereotype’’. In this population of mouth breathing children, the obstructive size of adenoids or
tonsils and the presence of rhinitis were not risk factors to the development of class II malocclusion,
anterior open bite or posterior crossbite.
ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords:
Mouth breathing
Malocclusion
Adenoids
Tonsils
Rhinitis
1. Introduction
The association between nasal respiratory impairment and
dento-facial morphology has been studied for more than a century
[1–3] and for decades it has been strongly accepted that inter-arch
growth pattern can be influenced by an unbalanced muscular
function on mouth breathers [4].
* Corresponding author at: Catholic University of Minas Gerais, School of
Dentistry, Orthodontics, Av. Dom Jose Gaspar, 500 CEP 30353-901, Belo Horizonte,
Brazil. Tel.: +55 3132455108 fax: +55 3132455115.
E-mail address: [email protected] (B.Q. Souki).
0165-5876/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ijporl.2009.02.006
The knowledge that obstruction of nasal breathing most likely
will perversely impact the facial growth even led some authors to
propose classic terms to describe such patients as ‘‘adenoid faces’’
[5], ‘‘long face syndrome’’ [6] and ‘‘respiratory obstruction
syndrome’’ [7].
A stereotype of these patients, therefore, can be drawn, where
an anterior open bite [8], a reduced transversal dimension [9,10],
associated or not with posterior crossbite [11], and a class II
malocclusion [12–14] are expected.
However, as individual facial genotypes have different sensitivity
on developing malocclusion, following the exposure to mouth
breathing, a wide variety of inter-arch relationships can be found.
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The emphasis on this mouth breathing stereotype has been
unfortunate because it implies that all patients with those clinical
findings are mouth breathers and that nasal impaired respiration
will ultimately result in this malocclusion. Besides that, one
question arises: can we predict the outcome of these malocclusions based on the presence and on the type of airway obstructive
cause which led to this deleterious habit?
Routinely, Ear, Nose and Throat (ENT) specialists and general
clinicians use the diagnosis of the airflow blockage by adenoids and
tonsils hyperplasia as a parameter to the establishment of the
treatment planning [15]. Although this axiom has been used
routinely by clinicians, it has not been sufficiently tested regarding
the development of malocclusion.
The aim of this study was to report epidemiological data on the
prevalence of malocclusion among a group of children, consecutively admitted at a referral mouth breathing ENT center. We
assessed the association between severity of the obstruction by
adenoids/tonsillar hyperplasia or the presence of allergic rhinitis
and the prevalence of class II malocclusion, anterior open bite and
posterior crossbite.
2. Patients and methods
2.1. Population
Four hundred and forty four children consecutively referred by
pediatricians and primary care physicians to the Outpatient Clinic
for Mouth-Breathers, at the Hospital das Clı́nicas at Federal
University of Minas Gerais (UFMG), Brazil, between November of
2002 and November of 2007, with the chief complaint of mouth
breathing were systematically evaluated by a multidisciplinary
team comprised by ENT doctors, allergologists and orthodontists,
in a single day visit.
Children whose mouth breathing could not be confirmed, those
who have had previous orthodontic treatment or were younger
than 2 years of age were excluded from the analysis. Therefore, the
sample of this cross-sectional study totaled 401 patients.
All subjects were evaluated by otorhinolaryngologists to
confirm mouth breathing resulting from at least one of the
following airway pathologies: obstructive tonsillar hyperplasia,
obstructive adenoidal hyperplasia and allergic rhinitis. The
children whose obstruction by one of these conditions could
not be diagnosed were classified as functional mouth breathers
[16].
The participant’s rights were protected, and informed consent
and assent were obtained according to the Ethics Committee of the
Federal University of Minas Gerais.
2.2. ENT data collection
An interview with children’s parents, or guardians, asking about
the quality of the children’s sleep, snoring, oral breathing and
throat infections, confirmed the ‘‘chief complaint’’ of mouth
breathing. Parents were also asked if the child had been undergone
an adenoidectomy or tonsillectomy earlier. Clinical ENT examination was performed by two of the authors (L.F. and H.B.), according
to the following guidelines.
Palatine tonsil hypertrophy was classified by mouth examination according to the criteria of Brodsky and Koch [17] as
follows: grade 0, tonsils limited to the tonsillar fossa; grade 1,
tonsils occupying up to 25% of the space between the anterior
pillars in the oropharynx; grade 2, tonsils occupying 25–50% of
the space between the anterior pillars; grade 3, tonsils occupying
50–75% of the space between the anterior pillars; and grade 4,
tonsils occupying 75–100% of the space between the anterior
pillars.
Tonsils grade 0, 1 and 2 were considered as non-obstructive and
those classified as grade 3 and 4 were named as obstructive [18].
Adenoids were assessed by flexible nasoendoscopy and were
grouped into two categories based on nasopharyngeal obstruction
(<75% and 75%). A cut-point of 75% was chosen to classify the
blockage of the nasopharynx as obstructive or non-obstructive [19].
2.3. Allergological data collection
The allergological assessment, to diagnose allergic rhinitis,
included a structured medical interview, physical examination,
following the standard volar forearm skin prick method, as
described elsewhere [20]. These exams were performed in 326
children under the supervision of one of the authors (J.P).
2.4. Dental data collection
The dental clinical examination was performed by a team of
orthodontists, who worked together for at least 10 years, and were
previously calibrated. The subjects were grouped by stage of
dental development, according to the variation in primary and
permanent teeth eruption, into deciduous, mixed and permanent
periods.
The inter-arch occlusion dental classification was based on
Barnett [21]:
Vertical: relationship was classified as (1) normal, (2) anterior
open bite or (3) deep bite. An open bite was registered in cases
that lacked any overbite, regardless of the amount. A deep bite
was registered when more than half of the lower incisors were
overlapped by the incisal edges of the upper incisors.
Transversal: relationship was classified as (1) normal, (2)
posterior crossbite, without mandibular functional shift, and
(3) posterior bite, with mandibular functional shift.
Sagital: relationship was classified as (a) normal occlusion, (b)
class I malocclusion, (c) class II malocclusion and (d) class III
malocclusion. During the deciduous and mixed dentitions, it
was considered a class I dental relationship when the upper
deciduous cuspid intercuspation was set between the lower
deciduous cuspid and first deciduous molar. When in permanent dentition the Angle classification was followed.
2.5. Dental data comparison
A large number of studies on the prevalence of malocclusion in
different populations have been published. These data served as a
reference of what should be the distribution on inter-arch
anomalies among a general population, where mouth and nasal
breathers were sampled together [28–32,35–41].
2.6. Statistics
Epi-data was used to enter data. SPSS version 12.0 was used for
the analysis. Descriptive statistics and univariate analysis in crosstables are showed. The significance level of p < 0.05 was chosen.
Normality of age distribution was tested using Kolmogorov–
Smirnov test.
For each dental and ENT variable, the number of children with
the diagnosed status (n) and its prevalence (%) are given.
For the purpose of statistical analysis, dental variables were
binarily grouped according to the expected inter-arch relationships in mouth breathing subjects. Therefore the dependent
variables examined were class II malocclusion, anterior open bite
and posterior crossbite.
The independent ENT variables were the obstructive grade of
tonsil and adenoids and the presence of rhinitis.
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3. Results
The mean age of this sample was 6 years and 6 months and the
standard deviation was 2 years and 7 months. The age of the
children ranged between 2 and 12 years. With the exception of 38
children (9.5%), whose mouth breathing was due to functional
habit, 363 subjects had an objective airway obstructive factor. Of
these children, 288 (71.8%) were judged to have tonsil and/or
adenoid obstruction, combined or not with rhinitis. Allergic
rhinitis, as the only obstructive cause, was found in 75 children
(18.7%).
Table 1 shows the prevalence of the studied variables, by
gender. As there was no gender statistically difference (p > 0.05),
the analysis was done considering boys and girls as a single group.
As seen in Table 1, the majority of the children was within the
deciduous (41.4%) or mixed (52.1%) dentitions. In this growth
period of their lives, they were susceptible to the unbalanced
muscular adaptation to mouth breathing. Only few children (6.5%)
were in permanent dentition.
Based in Table 1, 58.1% of the sample had a normal sagital
relationship (class I dental relationship). Class I malocclusion was
found in 46.9% of these children, the other 11.2% represents the
normal occlusion children. Regarding the three stages of occlusal
development (Table 2), Class I dental relationship was found in
Table 1
Prevalence of dental and ENT findings according to gender distribution. Number of
children (n) and prevalence given in percentage (n/N 100%).
Variables
Stage of development (N = 401)
Deciduous dentition
Mixed dentition
Permanent dentition
Boys
Girls
n
%
106
110
12
26.4
27.4
3.0
n
60
99
14
Total
%
n
%
15.0
24.7
3.5
166
209
26
41.4
52.1
6.5
2
x = 6.050 (2 d.f.) p value = 0.05
Sagital relationship (N = 384)
Normal occlusion
Class I malocclusion
Class II malocclusion
Class III malocclusion
26
97
64
30
6.8
25.3
16.7
7.8
17
83
51
16
4.4
21.6
13.3
4.2
43
180
115
46
11.2
46.9
29.9
12.0
x2 = 2.230 (3 d.f.) p value = 0.526
Vertical relationship (N = 385)
Normal
Deep bite
Open bite
115
38
67
29.9
9.9
17.4
98
21
46
25.5
5.5
11.9
213
59
113
55.3
15.3
29.4
Transversal relationship (N = 392)
Normal
158
Posterior crossbite w/o shift
31
Posterior crossbite w shift
32
40.3
7.9
8.2
116
22
33
29.6
5.6
8.4
274
53
65
69.9
13.5
16.6
141
86
35.3
21.6
95
77
23.8
19.3
236
163
59.1
40.9
Adenoid obstruction status (N = 390)
<75%
95
75%
124
24.4
31.8
70
101
17.9
25.9
165
225
42.3
57.7
40.8
15.6
102
40
31.3
12.3
235
91
72.1
27.9
x2 = 2.349 (2 d.f.) p value = 0.309
x2 = 1.631 (2 d.f.) p value = 0.443
Tonsils status (N = 399)
Grades 0, I, II
Grades III, IV
x2 = 1.918 (1 d.f.) p value = 0.166
x2 = 0.235 (1 d.f.) p value = 0.628
Rhinitis (N = 326)
Yes
No
x2 = 0.008 (1 d.f.) p value = 0.928
133
51
769
Table 2
Prevalence of dental and ENT findings in the deciduous. Mixed and permanent
dentitions. Number of children (n) and prevalence given in percentage (n/
N 100%).
Variable
Dental
Sagital relationship (N = 384)
Normal occlusion
Class I malocclusion
Class II malocclusion
Class III malocclusion
Deciduous
Mixed
n
%
n
%
n
Permanent
%
159
24
78
43
14
15.1
49.1
27.0
8.8
201
19
89
66
27
9.5
44.3
32.8
13.4
24
1
12
6
5
4.2
50.0
25.0
20.8
165
87
27
51
52.7
16.4
30.9
195
111
27
57
56.9
13.8
29.2
25
15
5
5
60.0
20.0
20.0
164
118
19
27
72.0
11.6
16.5
203
143
29
31
70.4
14.3
15.3
25
13
5
7
52.0
20.0
28.0
165
83
82
50.3
49.7
208
133
75
63.9
36.1
26
20
6
76.9
23.1
x2 p value = 0.196
Vertical relationship (N = 385)
Normal
Deep bite
Open bite
x2 p value = 0.731
Transversal relationship (N = 392)
Normal
Posterior crossbite w/o shift
Posterior crossbite w shift
x2 p value = 0.314
ENT
Tonsils status (N = 399)
Grades 0, I, II
Grades III, IV
x2 p value = 0.005
Adenoid obstruction status
(N = 390)
<75%
75%
161
205
24
43
118
26.7
73.3
102
103
49.8
50.2
20
4
83.3
16.7
137
79
58
57.7
42.3
168
136
32
81
19
21
20
1
95.2
4.8
x2 p value = 0.000
Rhinitis (N = 326)
Yes
No
x2 p value = 0.000
Note: x2 based on n 3 tables. n = variable.
64.2% during deciduous dentition, 53.8% and 54.2% during mixed
and permanent dentitions, respectively.
About 42% of this sample presented with a sagital disharmony,
represented by class II or III. The prevalence of class III gets higher
as kids get older (Table 1).
Considering the 384 children whose sagital classification was
done, dental Class II was the sagital relationship of 27% during
primary dentition, 32.8% on mixed dentition and 25% on
permanent dentition (Table 2).
The vertical inter-arch relationship must be studied in the
dental stage of development because of its known physiologic
difference along the growing period. Nevertheless, Table 2 brings
the information that a normal vertical relationship was found in, at
least, 52.7% of the sample, regardless of the dental stage of
development. Open bite prevalence was around 30% during the
deciduous and mixed dentitions and 20% in permanent dentition.
In the transversal analysis, posterior crossbite was detected in
close to 30% of the kids during deciduous and mixed dentitions and
48% in permanent dentition (Table 2).
All comparisons in Table 2 demonstrate that there is no
difference in the malocclusion occurrence when comparing the
three stages of dental development (p values >0.05).
Regarding the tonsils (Table 1), the more obstructing grades (3
and 4) were found in about 40.9% of the kids, but considering the
stratified groups by age (Table 2), kids during early stages
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770
Table 3
Univariate analysis between grouped malocclusion (dependent variable) and the
obstructive causes for mouth breathing (independent variables).
Variables
Tonsil/adenoid
obstruction
Rhinitis
only
No obstructive
cause diagnosed
p value
Class II malocclusion
Yes
78
No
196
24
49
13
24
0.589
Anterior open bite
Yes
79
No
198
24
48
10
26
0.710
Posterior crossbite
Yes
85
No
197
26
48
7
29
0.242
(deciduous dentition) had a higher prevalence (49.7%) than latter
stages (36.1% and 23.1% during mixed and permanent dentitions,
respectively). Table 2 also illustrate that the distribution of
tonsillar obstruction shifted according to aging. Children during
the deciduous dentition stage of development have more
obstructive tonsils than older ones (p < 0.05).
The adenoid’s obstruction of the nasopharynx showed similar
epidemiological behavior. Although the average prevalence of the
obstructive group (75% occupation of nasopharynx space) was
57.7% (Table 1), when analyzing this variable under the perspective
of dental stage of development, it is clear that prevalence declines
steeply from 73.3% to 16.7% along the aging (Table 2), with
statistically significant difference (p < 0.05).
The overall prevalence of allergic rhinitis was 72.1% (n = 235/
326), as demonstrated in Table 1. During mixed and permanent
dentitions the proportion of subjects with rhinitis was bigger (81%
and 95.2%, respectively) than in deciduous dentition 57.7%
(Table 2), a statistically significant difference (p < 0.05).
Table 3 shows the univariate analysis between grouped
malocclusion (dependent variable) and the ENT independent
variables. No association was found between the expected type of
malocclusion for mouth breathers and the presence of variables
that obstruct the nasal airflow (p > 0.05).
The comparison between our findings and the literature data
inter-arch prevalence is done in Section 4.
4. Discussion
Several reports have associated mouth breathing with dental
malocclusion. The first papers were limited to clinical impressions of
dentistry pioneers who related the disturbance on facial and occlusal
harmony to the impairment of nasal breathing in their patients.
Later, many papers published reports based on the findings of
scientific data collection, mostly considering the skeletal outcome
evaluated by cephalometry. However, data on occlusal clinical
parameters of mouth breathing children are scarce.
Dental inter-arch relationship, in the three planes of space, is
the basic clinical parameter in understanding the patient’s
occlusion and its behavior when exposed to unbalanced muscular
activity. Therefore, it is important to assess the occurrence of
occlusal disorders among mouth breathing children.
Despite the large sample size of this study, the limitations of a
cross-sectional design needs to be considered. As our sample is
comprised only of mouth breathers, the prevalence of dental interarch status had to be compared with other epidemiological reports
on a general population [28–32,35–41]. This methodology brings
at least two biases: (1) it is fact that in a general population a
significant number of children are mouth breathers [22–24]. Thus,
the difference between the prevalence of malocclusion in this
mouth breathing population and a ‘‘normal breathing’’ population
would be greater. (2) The reported prevalence varies considerably
between the different studies, even among the same population.
This divergence in prevalence figures may depend not only on
differences for specific ethnic groups [25], but also on wide ranges
in number and age among the examined subjects. However,
differences in registration methods, i.e. the criteria for the recorded
items, are probably the most important factor explaining these
differences. Despite these methodological limitations, this study
brings results that deserve further discussion.
Our study compared the prevalence of only one malocclusion in
each plane of space: class II (sagital), anterior open bite (vertical)
and posterior crossbite (transversal), since an occlusal pattern for
mouth breathers is well described.
Anomaly studies usually report findings by chronological age.
Malocclusion, however, is a manifestation that is related to
development of the dentition. Given the great individual variations
in dental maturation, it seems logical to determine the prevalence
of malocclusion for groups at different stages of dental development, rather than for different age groups. It is interesting to point
out that the pattern of distribution of the prevalence of
malocclusions does not show any statistical difference among
the three stages of dental development (Table 2), as it occurs in the
general population [26]. It is expected that the prevalence of each
malocclusion changes among the growth period. This fact suggests
that in a mouth breathing population, the increase in the
prevalence of some malocclusions alter the common pattern.
Regarding the sagital relationship, it is known that race impacts
significantly the prevalence of classes I, II and III malocclusions [27].
Therefore, a good comparison is made only with Brazilian data. This
was possible in the first two stages of dental development. During
primary dentition, the prevalence of class II in our mouth breathing
group was 27%. The prevalence found in previous publications in
Brazil varies between 6.8% and 30% [28–30]. Our findings are quite
similar to a large sample study (n = 2139) conducted by Tomita et al.
[28]. However our prevalence is higher than found in other studies
[29,30]. Kataoka et al. [29] concluded that the prevalence of class II in
their sample was low (6.8%) because their population was
comprised only by Japanese-Brazilian ethnic children. This fact,
explains the difference between our findings. However, the
difference in relation to the results found by Sadakyio et al. [30]
(15.6%) can be justified by data collection methodology discrepancies or differences due to mouth breathing.
In mixed dentition, our study’s class II prevalence (32.8%) is
much higher than the 12.5% reported by Zanetti [31]. This
significant discrepancy suggests that in older children, the
perverse impact of mouth breathing, on sagital inter-arch
development, is greater than on the deciduous dentition. Cheng
et al. [11] noted that the younger a subject is, at the time of
evaluation, the less the ‘‘adenoid’’ type of facial characteristics is
expressed. This opinion corroborates our findings. We can
hypothesize that the longer the exposure to the unbalanced
muscular function, due to mouth breathing, the greater the risk of
developing class II malocclusion. More epidemiological reports on
sagital relationship during the mixed dentition stage would be
helpful in testing this hypothesis, but only one was found.
Longitudinal cohort studies are necessary to test if this hypothesis
is correct.
During permanent dentition, the prevalence of class II in this
sample was 25%. A comparison with Brazilian data was not
possible because no epidemiological study involving general
population at this stage was found, regarding this type of
malocclusion. Comparing to Horowitz [32], who evaluated
American subjects, the prevalence numbers (22.5%) are quite
similar to our results. This observation corroborates the conclusions of Howard [33], Leech [34] and McNamara [3]. Nevertheless,
comparing our permanent dentition class II findings with the
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classic study of Emrich et al. [35], also in the United States, who
found 14%, our prevalence was higher. As the size of permanent
dentition sample, in our study, was small (n = 24), we suggest that
other studies, with larger samples, should test this association.
Regarding the vertical inter-arch relationship, the same type of
association described to class II was found. Compared to the
literature data, the prevalence of open bite during deciduous
dentition, in the investigated mouth breathers, was quite similar.
While our children’s anterior open bite prevalence during
deciduous dentition was 30.9%, the revised literature on general
population varied between 20.6% and 46.3% [28,44–46]. But, when
analyzing the older children (mixed dentition), an important
difference was noted. The prevalence of open bite reported in the
reference articles [31,36–39] varies between 12.00% and 20.1%,
while our sample had a prevalence of 29.2%.
In the transverse dimension we found the most significant
discrepancy in the prevalence of malocclusion. Dental literature
data shows that the prevalence of posterior crossbite ranges from
8% to 22% [40]. Prevalence studies on posterior crossbite during
permanent dentition are rare, but Thilander et al. [41] found a
prevalence of 3.9% during this stage. Therefore we considered 22%
as the top value. We found a prevalence of 30.1% of posterior
crossbite in whole group. This prevalence of close to 30% in the
primary and mixed dentitions and almost 50% in the permanent
one is higher than in the general population and deserves
additional consideration.
As the etiology of malocclusion has singular characteristics
when considering the three different planes of space, this
heterogeneity can help with the comprehension of our findings.
Sagital dental inter-arch relationship is mostly determined by
heredity [27] and therefore mouth breathing is only a secondary
etiological factor to class II development. Most likely, the power of
the unbalanced muscular activities, due to mouth breathing, is not
enough to shift a solid class I or III patterns into a class II. Maybe
those children with a tendency toward a class II, who could growth
into class I, depending on environmental factors, are the
population candidates who develop class II, when exposed to
mouth breathing. Therefore, in an epidemiological analysis, as we
did, the prevalence of class II is higher than in the general
population, especially in older children.
Vertical dental relationship also has heredity as the major
determinant, but environmental factors such as non-nutritious
sucking habits and mouth breathing work as secondary causes of
anterior open bite [42]. During deciduous dentition, when sucking
habits are highly prevalent in Brazil [43], the prevalence of anterior
open bite found in our sample of nasal impaired children was
within the range cited in previous Brazilian studies [40–42].
However, during mixed and permanent dentitions, as these
sucking habits decline in the general population, the difference
with our data gets bigger.
The transversal dental relationship, although governed by
individual facial genotype [47], suffers greatly from environmental
perverse factors [40]. Mocellin et al. [48], found 63.3% of palatal
constriction in mouth breathers and 5% in nasal breathers. This fact
explains why the discrepancy in the prevalence of posterior
crossbite was so significant between the mouth breathers and the
general population. As ethnic difference does not influence
posterior crossbite [25], the comparison with data from other
studies is feasible.
The triad of class II malocclusion, anterior open bite and
posterior crossbite, despite showing a higher prevalence in a
mouth breather sample than in the general population, is not the
most prevalent inter-arch relationship among the studied nasal
impaired children. In fact, a significant number of children
showed a normal occlusion, even growing with this perverse
habit.
771
It is clear that mouth breathing is capable of adding an
environmental weight to the etiology of such malocclusions.
However, since heredity plays a more important rule on facial
growth and development, we should not expect to find, on an
individual basis, many of these dental anomalies. It is not possible,
therefore, to predict with any certainty whether or not a mouth
breathing child will develop malocclusion, despite the fact that on
an epidemiological level, mouth breathers have a higher risk of
developing class II, anterior open bite and posterior crossbite than
a general population, as shown in other studies [10].
The results of this study suggest that older mouth breathing
children (mixed and permanent dentitions) have a tendency
toward increasing the prevalence of class II malocclusion and open
bite. If this assumption is true, normalizing nasal airflow passage in
younger children, instead of postponing ENT treatments, would be
beneficial from an orthodontic point of view. This hypothesis needs
to be tested in a longitudinal design study.
Our data did not show any association between the prevalence
of malocclusion and an obstructive pattern of the tonsils and/or
adenoid, nor with the presence of allergic rhinitis. This is a
controversial field in which previous studies have shown
discordant findings [2,7,49–54].
An explanation of this finding is based on morphogenetic
sensitivity in the development of malocclusion. If the child facial
type is prone to the development of one or more of the studied
inter-arch abnormalities, mouth breathing will only add an
additional etiological ‘‘push’’, regardless of the severity or the
type of the obstruction. Similarly, when a child has a low
susceptibility to the development of malocclusion, even in the
presence of a greater airflow obstruction, no dento-facial sequela
will occur.
If this explanation represents the truth, the risk of developing
malocclusion may be proportional to its morphogenetic susceptibility, but not with the severity of the obstruction. In this research,
no evaluation of the skeletal pattern was done, which would allow
the identification and stratification of the susceptibility. Therefore,
it is only possible to speculate that a full spectrum of malocclusion
was present. This balanced distribution contributed to the
interesting results of no association between malocclusion and
the grade of airflow blockage.
Secondly, another point which must be considered is the time
lapse between the initiation of mouth breathing and the
malocclusion outcome. If we theorize that, over time, children
with greater obstruction could develop more malocclusion than
children with less severity, using a young sample may explain the
lack of association between the tested variables.
One more explanation to our results could be the chosen cut
point which classified the tonsils and adenoids hyperplasia as
being obstructive or not. As no validation of these clinical criteria
was done yet, anyone can argue that a bias on the obstruction
classification interfered with the results.
As it was expected, the younger children had more tonsils and
adenoids obstruction than older ones [55]. The prevalence of
rhinitis, however, was much higher in older children. The reason is
linked to Waldeyer’s ring involution with aging, consequently
reducing the number of older subjects with adenoid or tonsil
hyperplasia referred to the hospital. Thus the respiratory ENT
complaint of older children tends to be rhinitis.
The findings of this study suggest that, based on the orthodontic
point of view, ENT doctors should consider treating all mouth
breathing children, regardless of the etiological factor, since it is
not possible to identify the risk of developing malocclusion based
solely on routinely used criteria.
Further research, with a longitudinal design and using methods
that can help in the identification of morphogenetic sensitivity
such as lateral cephalometric radiograph, and better evaluation of
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the severity of airway obstruction could add important information to this topic.
In conclusion, our study showed that the investigated nasal
impaired children had a higher prevalence of posterior crossbite
than general population at the same stage of development.
During mixed and permanent dentitions, anterior open bite and
class II malocclusion were more likely to be present in mouth
breathers. However, the majority of the children did not match
the expected ‘‘mouth breathing dental stereotype’’. We have also
showed that, in this sample of mouth breathers, adenoids/tonsils
hyperplasia or the presence of rhinitis, have no association with
the prevalence of class II malocclusion, anterior open bite and
posterior crossbite.
Acknowledgments
We thank Sidney M. Williams, DDS, for his kind contribution
reviewing the English language manuscript and Ms. Gleicilene
Fatima Silva Chaves for her contribution on data collection.
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