Comportamento mastigatório de adolescentes com sobrepeso e obesidade = Masticatory behaviour of overweight and obese adolescents

UNIVERSIDADE ESTADUAL DE CAMPINAS FACULDADE DE ODONTOLOGIA DE PIRACICABA

ALINE PEDRONI PEREIRA

COMPORTAMENTO MASTIGATÓRIO DE ADOLESCENTES

COM SOBREPESO E OBESIDADE

MASTICATORY BEHAVIOR OF OVERWEIGHT AND

OBESE ADOLESCENTS

Piracicaba 2016

ALINE PEDRONI PEREIRA

COMPORTAMENTO MASTIGATÓRIO DE ADOLESCENTES

COM SOBREPESO E OBESIDADE

MASTICATORY BEHAVIOR OF OVERWEIGHT AND

OBESE ADOLESCENTS

Dissertação apresentada à Faculdade de Odontologia de Piracicaba da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de Mestra em Odontologia, na Área de Odontopediatria.

Dissertation presented to the Piracicaba Dental School of the University of Campinas in partial fulfillment of the requirements for the degree of Master in Dentistry, in Pediatric Dentistry area.

Orientadora: Profa. Dra. Paula Midori Castelo Ferrua

Piracicaba 2016

ESTE EXEMPLAR CORRESPONDE À VERSÃO FINAL DA DISSERTAÇÃO DEFENDIDA PELA ALUNA ALINE PEDRONI PEREIRA E ORIENTADA PELA PROFA. DRA. PAULA MIDORI CASTELO FERRUA.

DEDICATÓRIA

Agradeço...

À Deus, pela minha vida e por mais uma etapa concluída.

Dedico esta conquista...

À minha mãe, Rita de Cássia Olmos Pedroni, por me dar apoio e suporte para realizar

meus sonhos. Pela confiança em mim depositada e pelo exemplo de amor e dedicação à

profissão.

AGRADECIMENTOS ESPECIAIS

À minha orientadora, Prof

_Dr

_{Paula Midori Castelo Ferrua, pela confiança}

depositada na realização deste trabalho. Obrigada por compartilhar da sua sabedoria, por

respeitar os meus erros e delicadamente me guiar para o caminho correto. Por ser tão

competente e ao mesmo tempo tão humana. Por dispor do seu tempo para me orientar e pelos

bons e agradáveis momentos de convivência. Muito obrigada.

AGRADECIMENTOS

Ao Magnífico Reitor da Universidade Estadual de Campinas, Prof .Dr. José

Tadeu Jorge.

À Faculdade de Odontologia de Piracicaba, na pessoa do seu diretor, Prof. Dr.

Guilherme Elias Pessanha Henriques.

Agradeço a todos os professores do curso de pós-graduação em Odontologia da

Faculdade de Odontologia de Piracicaba, da Universidade Estadual de Campinas, pelos

ensinamentos que tanto contribuíram para meu crescimento e formação pessoal/profissional.

Aos professores Dr. Paulo Henrique Ferreira Caria, Dr. Francisco José de

Moraes Macedo, Dr

_{Rosana Boni, Dr}

_{Regina Maria Puppin Rontani, Dr}

_{Maria Beatriz}

Duarte Gavião pela leitura atenta e crítica ao texto e sugestões apresentadas.

À Prof

_Dr

_{Débora Alves Nunes Leite Lima, pela contribuição, gentileza,}

disponibilidade em ajudar e materiais concedidos.

Às professoras do departamento de Odontologia Infantil, Área de

Odontopediatria da Faculdade de Odontologia de Piracicaba: Prof

_Dr

_{Maria Beatriz}

Duarte Gavião, Prof

_Dr

_{Regina Maria Puppin Rontani, por serem grandes exemplos de}

profissionais e pesquisadoras. Muito obrigada por todos os ensinamentos, por dividirem tão

bem os seus conhecimentos clínicos e teóricos e pelas contribuições a este trabalho. Prof

_Dr

Marinês Nobre dos Santos, Prof

_Dr

_{Carolina Alarcon, Prof}

_Dr

_{Fernanda Pascon, Prof}

Dr

_{Kamila Kantovitz e Prof}

_Dr

_{Taís de Souza Barbosa, pela disponibilidade, dedicação,}

profissionalismo e por todos os ensinamentos concedidos.

À Ana Paula, Erica e Domingos, secretários da Coordenadoria de Pós Graduação

da FOP-Unicamp, à Shirley, secretária do departamento de Odontologia Infantil, pela

atenção e disponibilidade.

Aos amigos da Pós Graduação: Fernanda Mazoni, Daniela Cibim, Kelly Maria,

Andréia Cardoso, Jossária Sousa, Filipe Martins , Lívia Pagotto, Alexandra Iwamoto,

Gabriela Borgui, Camila Nobre, Juana Salas, Karina Souza, Carlos Tapia, Pedro Rebouças,

Priscila Alves, Claudia Lobelli e Samuel Chaves, obrigada pelos bons momentos

compartilhados e troca constante de ajuda e conhecimentos.

Às amigas do grupo de pesquisa: Daniela de Almeida Prado, Maria Carolina

Salomé Marquezin e Kelly Guedes de Oliveira Scudine. Obrigada pelo trabalho em equipe,

pela ajuda, ensinamentos, participação e contribuições.

Aline Laignier Soares, Obrigada por estar sempre alegre e disposta a ajudar. Por

me mostrar que as pessoas ainda devem acreditar em seus ideais. Obrigada por construir

comigo uma amizade tão linda e verdadeira. Micaela Cardoso, Obrigada pelos momentos de

alegria. Por estar sempre iluminando a vida de todos ao seu redor. Por ser uma amiga tão

companheira e solícita. Mayra Miguel, pela amizade fiel que não se apaga com o tempo,

presente da FOP. Mariana Viana Vercelino, obrigada pelas longas conversas e risadas, pela

companhia sempre agradável. Fabio Fabretti, obrigada por toda ajuda sempre, por ser tão

doce e alegre. Gabriel Ward, por sonhar junto comigo e me incentivar a conhecer o mundo.

Lenita Lopes, pela gentileza e pelos bons momentos compartilhados. Darlle Santos Araujo,

grande incentivadora deste Mestrado. Obrigada por dividir esses dois anos comigo e me

ensinar tanto. Por ser essa pessoa forte, correta e justa. Por estar sempre disposta a ouvir e

ajudar. Muito obrigada por tudo!

Aos queridos professores e amigos da Ortopedia Funcional dos Maxilares, em

nome de Francisco José de Moraes Macedo e José Lázaro Barbosa dos Santos, pelo

entusiasmo em ensinar, por despertar o interesse em aprender e pela fonte inesgotável de

conhecimento. Pelas amizades construídas e momentos de alegria compartilhados.

A toda a minha família, madrinha, tios e tias que me apoiaram em todos os

momentos, em especial aos meus queridos avós, Nilbe e Clóvis Pedroni, pelas orações, pelo

amor sempre a mim dedicado, por estarem sempre tão presentes em minha vida.

Ao Rafael Dantas Matos da Paz, por nunca soltar a minha mão, pelo carinho e

amparo nos momentos de angústia e insegurança. Por acalmar meu coração e me trazer paz.

Aos meus queridos irmãos: Mariana Pedroni Pereira, por ser minha melhor

companheira. Pelas viagens e passeios que aliviavam a árdua rotina. Ana Laura Lovizaro

Pereira, presente de Deus. Obrigada por alegrar e adoçar a minha vida em todos os nossos

encontros. Rafael Pedroni Pereira, por ser exemplo de caráter e bom coração. Pelos agráveis

momentos de convivência.

Ao meu pai, Filemon Marques Pereira Filho pelo investimento em amor e nos

estudos. Por me ‘’acudir’’ em todos os momentos de apuro e nunca me deixar sozinha. Pelo

amor que sente por mim, por entender minhas escolhas e minha ausência. Muito obrigada por

tudo que sempre dedicou a mim. À minha madrasta, Luciana Pisoni Lovizaro, pela torcida

sempre, por todos os conselhos, pelo amor e dedicação à família.

À minha mãe Rita de Cássia Olmos Pedroni, por não medir esforços para me

ajudar, por nunca me deixar desistir, por abrir as portas do mundo para mim, pelas viagens e

congressos. Obrigada por sempre me incentivar a querer ser mais, por participar e contribuir

com os meus trabalhos. Por todos os esforços dedicados a mim. Por me amar

incondicionalmente, confiar em mim de olhos fechados e apoiar todas as minhas decisões.

Não existem palavras suficientes para expressar meu agradecimento.

Aos pacientes, personagens principais do meu aprendizado.

Às escolas, diretores, professores, funcionários e alunos voluntários da pesquisa,

que foram fundamentais para a existência deste trabalho.

‘’A frase ‘a pessoa se fez sozinha’, não existe, carece de veracidade. Todos nós somos feitos

por outras milhares de pessoas. Cada ser que fez algo de bom para nós, ou nos disse algumas

palavras de conforto ou aprovação, influenciou em nossa personalidade e nossos atos. É por

isso que elas se transformam em parte de qualquer sucesso nosso’’.

RESUMO

Aspectos fisiológicos e comportamentais da mastigação podem influir no estado nutricional, o que tem sido pouco explorado em estudos. Assim, o objetivo deste estudo foi avaliar aspectos objetivos, subjetivos e comportamentais da função mastigatória em 231 adolescentes (112♂/119♀), com idades entre 14 e 17 anos, escolares da rede pública do município de Piracicaba (SP) e comparar estes parâmetros entre aqueles com peso normal (n=115) e com sobrepeso ou obesidade (n=116). O exame físico envolveu as medidas de estatura, peso, massa de gordura e massa de músculo esquelético corporal por meio de um estadiômetro digital e impedância bioelétrica, classificando-os em eutrofia, sobrepeso e obesidade. A saúde dentária e oclusão morfológica também foram avaliadas. As avaliações objetivas foram realizadas pelo Protocolo de Avaliação Miofuncional Orofacial expandido (AMIOFE-e), que verifica o tipo (lado) mastigatório, tempo/frequência mastigatória, alteração nos movimentos, entre outros; performance mastigatória pelo método colorimétrico (goma de mascar) e mensuração da máxima força de mordida unilateral por meio de gnatodinamômetro digital. Já a avaliação da qualidade mastigatória foi realizada por meio do instrumento validado Questionário de Avaliação da Qualidade da Mastigação (QAQM), o qual verificou aspectos subjetivos e comportamentais. Os dados foram submetidos a testes de normalidade, qui-quadrado e teste “t” não-pareado e Mann-Whitney. Um modelo de regressão linear múltipla foi utilizado para avaliar a contribuição das variáveis em estudo na variação na porcentagem de gordura corporal (α=0,05). Os resultados mostraram que o escore total do AMIOFE-e diferiu significativamente entre os adolescentes de peso normal e com sobrepeso/obesidade em ambos os sexos, ou seja, indivíduos com sobrepeso/obesidade apresentaram mais alterações nos aspectos miofuncionais oro-faciais. Nas meninas, a mastigação unilateral foi mais frequente no grupo sobrepeso/obesidade. Também, meninas com excesso de peso apresentaram maiores escores nos domínios ‘’Hábitos’’ e ‘’Frutas’’ da avaliação subjetiva da qualidade da mastigação (maior dificuldade na função mastigatória); elas também relataram a necessidade de adicionar molho à refeição para facilitar a deglutição e o hábito de descascar e cortar frutas (maçãs) em pedaços pequenos, a fim de facilitar a mastigação. O escore total do AMIOFE-e também mostrou uma relação significativa com o percentual de gordura corporal. A performance mastigatória avaliada por meio de goma de mascar e a força de mordida não diferiram entre os grupos. Este estudo mostrou que adolescentes com excesso de peso apresentaram alterações no comportamento mastigatório e maior dificuldade para realizar a função quando comparados com indivíduos com peso normal.

ABSTRACT

The physiological and behavioral aspects of masticatory function may have an impact on nutritional status, which has been little studied. The aim was to perform a comprehensive evaluation of objective, subjective and behavioral aspects of masticatory function in 231 adolescents (112♂/119♀), aged 14-17 years, from public Schools of Piracicaba (SP, Brazil) and compare these parameters between normal-weight (n=115) and overweight/obese (n=116) adolescents. The physical examination involved measurements of stature, weight, body fat mass and skeletal muscle mass using digital stadiometer and bioelectric impedance. Dental health and occlusion were also assessed. The objective evaluations were performed by using the protocol Oro-facial Myofunctional Evaluation expanded (OMES-e), which determines the masticatory type, chewing time/frequency, abnormal movements, and other; masticatory performance (color changeable chewing gum) and maximum bite force. The subjective and behavioral evaluations were performed by the Quality of Mastication Function Questionnaire, a validated questionnaire which explores the masticatory behavior and frequency/intensity of difficulty in chewing different types of foods. Results were submitted to normality tests, Chi-square, unpaired t-test and Mann-Whitney. A multiple linear regression model was used to evaluate which of the variables under study contributed to the variation in Percent Body Fat (α=0.05). The results showed that OMES-e total score differed significantly between normal-weight and overweight/obese adolescents in both genders, that is, overweight/obese individuals showed more changes in oro-facial myofunctional aspects than normal-weight ones. Unilateral mastication was more frequent among overweight/obese than normal-weight females. Females with weight excess also showed higher scores on Habits and Fruit domains in the subjective evaluation of masticatory quality (greater difficulty); they also reported the need of adding sauce to the meal to facilitate swallowing and peeling and cutting fruits (apples) in small pieces in order to chew them. OMES-e total score also showed a significant relationship with Percent Body Fat. Masticatory performance evaluated by chewing gum and bite force did not differ between groups. This study showed that adolescents with weight excess presented changes in masticatory behavior and greater difficulty in performing the masticatory function comparing to normal-weight ones.

SUMÁRIO

1 INTRODUÇÃO 14

2 ARTIGO - Chewing in overweight and obese adolescents: an exploratory study with behavioral approach

18

3 CONCLUSÃO 42

REFERÊNCIAS 43

ANEXOS 48

ANEXO 1 - Certificado do Comitê de Ética em Pesquisa da FOP 48

ANEXO 2 - Questionário de avaliação da qualidade da mastigação 49

APÊNDICES 52

APÊNDICE 1 - Termo de consentimento livre e esclarecido 52

APÊNDICE 2 - Figuras ilustrativas com a descrição da metodologia empregada no estudo

55

1 INTRODUÇÃO

O excesso de peso tornou-se a condição crônica mais comum na infância e adolescência no mundo. O aumento da incidência de obesidade na infância pode estar relacionado a diversos fatores, tais como o desmame precoce, distúrbios alimentares, problemas nas relações familiares, estilo de vida e/ou hábitos alimentares inadequados (Bass e Beresin, 2009; Gupta et al., 2012). A indústria alimentícia disponibiliza muitos alimentos com alto teor de energia, palatáveis e de baixo nível nutricional, servidos em grandes porções que, somados à diminuição na prática de exercícios físicos, contribuem para o aumento dos índices de sobrepeso e obesidade (Drewnowski e Specter, 2004; McCormack et al., 2014).

A obesidade pode levar a consequências graves no crescimento da criança, assim como a alterações nas funções respiratórias, cardiovasculares, metabólicas, ortopédicas e dermatológicas (Reilly, 2005). Além disso, pode causar alterações psicossociais, como distúrbios de comportamento, depressão, angústia, baixa autoestima e sentimento de culpa (OPAS, 2003). Uma criança obesa tem grande chance de tornar-se um adulto obeso (Rossner, 1998; Whitlock et al., 2005) e, segundo dados da Organização Mundial da Saúde (OMS, 2009), essa condição é a causa de morte de 2,8 milhões de pessoas por ano e está entre os dez principais problemas de saúde pública do mundo. No Brasil, segundo a Pesquisa Nacional de Saúde realizada pelo Instituto Brasileiro de Geografia e Estatística (IBGE, 2010), em adolescentes de 10 a 19 anos, o excesso de peso foi diagnosticado em cerca de um quinto da população estudada. Dados recentes (Brasil, 2015) mostraram que 56,9% dos brasileiros com 18 anos ou mais estão com excesso de peso. Esse índice é superior ao calculado em 2003, que registrou 42%.

A fase oral da digestão é a mais curta de todo o processo digestivo, quando comparada ao período gástrico e intestinal e, por isso, tem recebido pouca importância nos estudos que envolvem a avaliação nutricional (Hoebler et al., 1998). A mastigação é o primeiro estágio do processo digestivo, que resulta de um padrão rítmico de movimentos mandibulares onde o alimento é triturado entre as faces oclusais dos dentes sob influência da saliva (Pereira et al., 2006), preparando o bolo alimentar apto para ser deglutido e digerido (Bourne, 2004). Neste processo de fragmentação e umidificação do alimento, os estímulos sensoriais relacionados ao sabor e ao prazer de comer também são evocados (Pereira et al., 2006), causando aumento do fluxo parassimpático excitatório neural para todo o trato gastrointestinal, aumentando dessa forma as secreções salivar, de ácido gástrico, enzimático e pancreático.

Pessoas com saúde bucal prejudicada ou mesmo uma função mastigatória deficiente deglutem partículas grandes de alimento ou alteram sua dieta, evitando os mais difíceis de serem mastigados (Laurin et al., 1994; Friedlander et al., 2007). A capacidade tampão de um alimento bem mastigado é significativamente maior do que de um alimento parcialmente ou não mastigado. Também, observou-se que um alimento sólido permanece mais tempo no estômago do que um de consistência mais líquida (Dubey e Nundy, 1984). Isto poderia resultar no decréscimo da absorção de nutrientes e a ingestão não balanceada de alimentos, pelo consumo preferencial de alimentos mais macios e fáceis de serem mastigados, como os industrializados, em detrimento dos ricos em fibras e nutrientes. Nas duas situações, a dieta prejudicada pode aumentar o risco de distúrbios gastrointestinais e de doenças relacionadas a carências nutricionais (Laurin et al., 1994; Papas et al., 1998; Budtz-Jorgensen et al., 2000).

Estudos que tenham avaliado o comportamento alimentar em indivíduos obesos observaram a prática da mastigação ineficaz associada à escolha de alimentos de consistência mais friável e macios (Katagiri et al., 2011). Estes comportamentos podem se relacionar a uma situação facilitadora para um ato mastigatório, ineficiente e com menor estímulo mioneural; nestes casos, observa-se uma musculatura condizente com a falta de estímulo, com evidentes alterações (Ferla et al., 2008). A diminuição do tônus muscular dos órgãos fonoarticulatórios e a restrição dos movimentos mandibulares tornam os movimentos mastigatórios incompetentes (van der Bilt et al., 2006; Woda et al., 2006), porém estudos ainda são necessários para determinar se a escolha do alimento decorre da flacidez muscular ou se esta é quem determina a escolha intuitiva de alimentos com menor consistência. Além disso, a mudança na consistência alimentar pode influenciar a morfologia dentofacial ao alterar a demanda funcional dos músculos mastigatórios, sendo os alimentos secos, duros e fibrosos considerados importantes para o desenvolvimento do sistema estomatognático por provocarem forte estímulo durante o treino mastigatório e a maturação dessas funções (Kiliaridis, 1989; Pena et al, 2008). A diminuição da força oclusal e da mastigação necessárias para a trituração de alimentos está associada a um decréscimo no crescimento dos arcos mandibulares e maxilares em humanos (Lieberman et al., 2004).

A função mastigatória é complexa e a redução das partículas dos alimentos depende de fatores fisiológicos e comportamentais, tais como força de mordida, atividade dos músculos da mastigação, número de dentes em oclusão e dieta (Sato e Yoshiike, 2010). A avaliação objetiva da mastigação pode ser realizada pela avaliação da performance e da eficiência mastigatória, que se refere à capacidade de fragmentar um alimento ou material-teste depois de tê-lo mastigado sem deglutir (Marquezin et al., 2013). Os termos eficiência e

performance mastigatória vem sendo amplamente utilizados em pesquisas mas não são sinônimos; diferem entre si pelo método utilizado na sua obtenção. A eficiência mastigatória é mensurada investigando-se o número de ciclos mastigatórios necessários para redução do tamanho das partículas do alimento-teste. Para tanto, o alimento-teste é mastigado por diferentes números de ciclos mastigatórios, ou até que fique pronto para deglutição. Já a performance mastigatória é obtida pela análise da distribuição do tamanho das partículas do alimento-teste mastigado durante um número fixo de ciclos mastigatórios (Silva et al., 2011). A performance mastigatória também pode ser determinada pelo método colorimétrico, empregando-se material-teste artificial, cuja padronização permite maior fidedignidade dos resultados, que não envolvem perda de partes do alimento por deglutição ou variações naturais ou sazonais (Felício et al., 2008). A força de mordida também tem sido utilizada como parâmetro fidedigno na avaliação das características funcionais dos músculos da mastigação. De acordo com a literatura, assume-se que esteja relacionada com a integridade desses músculos, sendo que uma maior força de mordida resultaria em uma mastigação mais eficiente (Su et al., 2009).

A avaliação clínica da função mastigatória usando alimentos naturais tem sido aplicada para definir o tipo (lado) mastigatório e o tempo para o consumo de alimento natural (Felício et al., 2002), duração do ato mastigatório (Berretin-Felix et al., 2005), frequência mastigatória, número de ciclos mastigatórios, amplitude dos movimentos, dentre outros aspectos (Hennequin et al., 2005; Nicolas et al., 2007). Especificamente para a avaliação clínica e comportamental do sistema estomatognático foi desenvolvido e validado o protocolo de Avaliação Miofuncional Orofacial com Escores (AMIOFE) (Felício et al., 2012), o qual apresentou sensibilidade e especificidade adequadas e avalia diversos aspectos das funções que abrangem o sistema estomatognático, entre elas a mastigação.

A qualidade da mastigação também pode ser investigada sob o ponto de vista subjetivo, o que tem sido pouco explorado provavelmente pela falta de instrumentos validados. Estudos prévios se propuseram a realizar esta avaliação por meio da utilização de questionários simples relacionados à preferência alimentar (Pena et al., 2008) ou pela Escala Analógica Visual (VAS) (Peres et al., 2003; Katsuhiko et al., 2004; Prado et al., 2006); no entanto, tais avaliações mostraram-se pouco sensíveis para se determinar a capacidade mastigatória (Hilasaca-Mamani et al., 2016). O instrumento Questionário de Avaliação da Qualidade da Mastigação (QAQM) derivou do Questionnaire D'Alimentation, questionário este em língua francesa (Muller et al., 2008); sua tradução, adaptação cultural e validação em adolescentes brasileiros foram realizadas recentemente (Hilasaca-Mamani et al., 2015, 2016), cujas propriedades psicométricas mostraram-se adequadas na avaliação do

comportamento mastigatório, especificamente dos hábitos alimentares, escolha e preparo dos alimentos e percepção da dificuldade no desempenho da mastigação.

A obesidade na infância e adolescência é uma condição de etiologia multifatorial e de difícil reversão na fase adulta. Os fatores ambientais, por serem modificáveis, têm grande impacto na sua prevenção. A mastigação é uma das funções do sistema estomatognático que se desenvolve a partir de experiências aprendidas (Falda, 1998). Devido ao importante papel que uma adequada mastigação proporciona para a saúde geral de um indivíduo e uma vez que o estudo dos fatores potencialmente associados à esta condição pode auxiliar na prevenção e tratamento do excesso de peso, o objetivo deste estudo foi avaliar a função mastigatória de adolescentes com sobrepeso e obesidade, nos seus aspectos fisiológicos e comportamentais, comparando-os com indivíduos com peso normal.

2 ARTIGO

CHEWING IN OVERWEIGHT AND OBESE ADOLESCENTS: AN

EXPLORATORY STUDY WITH BEHAVIORAL APPROACH

Artigo submetido ao periódico Obesity (Anexo 2)

Aline Pedroni Pereira, Department of Pediatric Dentistry, Piracicaba Dental School,

University of Campinas, Piracicaba (SP), Brazil.

Darlle Santos Araújo, Department of Pediatric Dentistry, Piracicaba Dental School,

University of Campinas, Piracicaba (SP), Brazil.

Kelly Guedes de Oliveira Scudine, Department of Pediatric Dentistry, Piracicaba Dental

School, University of Campinas, Piracicaba (SP), Brazil.

Daniela Galvão de Almeida Prado, Department of Pediatric Dentistry, Piracicaba Dental

School, University of Campinas, Piracicaba (SP), Brazil.

Débora Alves Nunes Leite Lima, Department of Restorative Dentistry, Piracicaba Dental

School, State University of Campinas, Piracicaba, (SP), Brazil.

Paula Midori Castelo, Department of Biological Sciences – Universidade Federal de São

Paulo (UNIFESP), Diadema (SP), Brazil.

Correspondence to:

Professor Paula Midori Castelo

Departamento de Ciências Biológicas

Universidade Federal de São Paulo, UNIFESP – Campus Diadema R. São Nicolau, 210, Diadema, SP, Brazil. CEP 09913030

E-mail: pcastelo@yahoo.com

DECLARATION OF CONFLICT INTERESTS

ABSTRACT

The aim was to perform a comprehensive evaluation of masticatory function aspects of 231 adolescents, aged 14-17 years, comparing normal-weight (n=115) and overweight/obese (n=116) subjects. The objective evaluations were performed by Oro-facial Myofunctional Evaluation expanded (OMES-e) protocol, determining the masticatory type, chewing time/frequency, abnormal movements, and other; masticatory performance (color changeable chewing gum) and bite force. By using the Quality of Mastication Function Questionnaire, the masticatory behavior and frequency/intensity of difficulty in chewing different types of foods were explored. Data were submitted to normality and Chi-square tests, unpaired t-test/Mann-Whitney and multiple linear regression model. OMES-e total score differed significantly between normal-weight and overweight/obese adolescents in both genders, that is, overweight/obese individuals showed more changes in oro-facial myofunctional aspects. Unilateral mastication was more frequent among overweight/obese females. Females with weight excess also showed higher scores on Habits and Fruit domains in the subjective evaluation (greater difficulty); they also reported the need of adding sauce to the meal to facilitate swallowing and peeling and cutting fruit (apples) in small pieces in order to chew them. OMES-e total score also showed a significant relationship with Percent Body Fat. Masticatory performance (chewing gum) and bite force did not differ between groups. This study showed that adolescents with weight excess presented changes in masticatory behavior and greater difficulty in performing the masticatory function comparing to normal-weight ones.

INTRODUCTION

Pediatric obesity is an important health concern which requires a multidisciplinary attention (WHO, 2006). The rise in weight excess has been recently shown to occur among male and female adolescents in many countries, reaching epidemic proportions in Western industrialized (Speiser et al., 2005) and developing countries (Misra and Khurana, 2008). Adolescence is a period of rapid change in physical, psychosocial, educational, and vocational domains, also distinguished by an increase in behaviors considered to be risky, harmful, or even antisocial (Moffit et al., 1993). The increase in the prevalence of obesity places a significant burden on physical, psychological, and social health and calls for an urgent implementation of diverse treatment strategies (Doll et al., 2000; Speiser et al., 2005). Furthermore, it is known that a considerable proportion of overweight children are at risk to become obese adults (Whitlock et al., 2015).

Mastication is the first step in the digestion process and is responsible for breakdown of large food particles into smaller particles suitable for gastrointestinal absorption of nutrients and lubricating and softening food particles into a bolus conducive to swallowing, thereby facilitating gastrointestinal absorption of food particles (Pedersen et al., 2002). Obesity and diabetes have been associated with increased consumption of highly processed foods (Brennan et al., 2010), which have greater palatability, more calories, lower cost, and less consistency, while are rich in sugar and fat (Drewnowski and Specter, 2004; Bes-Rastrollo et al., 2008). According to Bellisle (2000), the consumption of such foods speeds the digestion process, decreases the chewing time and the number of masticatory cycles. Comminution of food was also shown to influence gastric emptying rates (Pera et al., 2002). In addition, previous studies suggested a relationship between eating fast and weight excess (Otsuka et al., 2006; Maruyama et al., 2008; Tanihara et al., 2011).

Due to its complexity, the masticatory function can be evaluated by different aspects; the measure of masticatory performance and efficiency may reflect the quality of mastication by determining the number of chews necessary to render food ready for swallowing (Pedersen et al., 2002). Muscle (bite) force and the number of functional tooth units are determinants of masticatory performance, which suggests that their maintenance may be important for promoting healthful functional status of the stomatognathic system (Hatch et al., 2000). Masticatory function can also be evaluated subjectively, using questionnaires or visual analogic scales (VAS) in which the individual's chewing behavior and any difficulties while performing the function are assessed (Hilasaca-Mamani et al., 2015, 2016). Masticatory efficiency and masticatory behavior are aspects that in general are

not directly related; hence, both indexes should be used with sufficient consideration of their differences (Sato and Yoshiike, 2010). Using a validated questionnaire, it is possible to assess if the subject avoids certain kind of food because of its size or consistency or if the individual cut food into small pieces and/or eat food together with beverages to facilitate chewing and swallowing.

As weight excess may be related to dietary behavior and alterations in some masticatory functional aspects (Kibayashi, 2011), the aim of the present study was to perform a comprehensive evaluation of masticatory function and behavior in adolescents with different nutritional status, including objective and subjective aspects in a cross-sectional study.

2. MATERIALS AND METHODS

2.1. Ethical and reporting considerations

This study was approved by the Research and Ethics Committee of Piracicaba Dental School – University of Campinas (protocol n. 152/2014). The procedures and possible discomforts or risks were fully explained to the adolescent and their parents⁄guardians. Each subject and his /parent/guardian gave voluntary consent to participate in this research by signing an informed assent form and a parental/guardian consent form, respectively, after having their questions and concerns addressed.

The reporting of this research follows the STROBE recommendations for reports of observational studies (Malta et al., 2010).

2.2. Sample

1585 students aged 14- 17 years from ten Public Schools of Piracicaba (SP, Brazil) were invited to participate in this study. Only 390 agreed formally to participate; from those, 231 adolescents were included considering the inclusion/exclusion criteria and divided into four groups, according to the reference data BMI-for-age and gender (WHO, 2007):

 Female normal-weight adolescents (n=60);  Male normal-weight adolescents (n=55);

 Female adolescents with overweight or obesity (n=59);  Male adolescents with overweight or obesity (n=57).

Sample size was calculated from results of a previous study (Kibayashi, 2011), which examined the ability of mastication in obese and non-obese children. Considering a power of

the test=0.80 and alpha level=0.05, a minimum of 51 subjects in each group would be necessary to perform such evaluations.

2.3. Anamnesis

The anamnesis was structured in order to verify the medical and dental history by using a questionnaire applied to the adolescent. The following data were collected: history/presence of deleterious habits (sucking, nail biting, bruxism, somnambulism, nocturnal / daytime mouth breathing, snoring, asthma and bronchitis); medical and dental treatments; chronic use of medications or drugs; symptoms of orofacial pain/temporomandibular disorders (TMD). The inclusion factor was the presence of permanent dentition established, with the exception of third molars. The exclusion criteria were: presence of caries and/or tooth loss; periodontal disease (pockets >3 mm); pain of dental origin; history/current orthodontic treatment; chronic diseases such as asthma/bronchitis, epilepsy, cancer, rheumatoid arthritis, diabetes mellitus or hypertension; chronic use of drugs such as benzodiazepines, anti-inflammatories, steroids and antidepressants; presence of dietary restrictions; xerostomia complaints or salivary glands diseases; and inappropriate behavior and/or refusal to cooperate in the proposed evaluations. Subjects presenting thinness and severe thinness were also excluded.

TMD was screened using a questionnaire proposed by the American Academy of Orofacial Pain (AAOP), which consists of ten questions with yes/no responses exploring TMJ sounds and pain, masticatory muscle pain or fatigue, and difficulty during opening the mouth (Chaves et al., 2008). The subject was first asked if he/she has had any of the symptoms investigated. If the answer was positive, the respondent was asked about the presence of the symptom more than once. Finally, the respondent was asked if he/she had the symptom in the last month. Only the previous month was considered for capturing information on TMD (Gonçalves et al., 2010).

2.4. Clinical Oral Examination

The oral examination was performed at school, using a clinical mirror with LED light, exploratory probe, after performing biofilm control. Caries experience was evaluated by determining the number of decayed, missing, and filled permanent teeth (DMFT). The presence of periodontal pockets was recorded according to the Community Periodontal Index (WHO, 1997), and the index teeth were: 11, 31, 16, 26, 36, 46.

The assessment of the severity of malocclusion was performed using the Peer Assessment Rating (PAR) index, which was based on the sum of 11 weighted

components of malocclusion including posterior right, posterior left and anterior tooth displacement (maxillary and mandibular), right and left buccal occlusion, overjet, overbite, and midline discrepancy (Richmond et al., 1992). The assessments were made directly on the patient's mouth, using a mirror and millimeter probe. The records were performed by a trained examiner (KGOS).

2.5. Anthropometric evaluation

Anthropometric and nutritional evaluations involved the measurements of height, weight, and body skeletal muscle mass, by means of a digital stadiometer scale and bioelectric impedance analysis. Body mass index (BMI = kg/m2) was determined in order to classify the selected sample into normal weight, overweight, and obesity, according to the reference data BMI-for-age and gender (5–19 years) (WHO, 2007). To determine the body fat, abdominal obesity degree and body skeletal muscle mass, bioelectric impedance analysis was performed (InBody 230, Biospace Co. Ltd., Gangnan-gu, Seul, South Korea). The measurement system is tetra-polar with eight tactile electrodes: two sets of electrodes in metal plates for each foot on which the subject was placed; at the top part of the scale column, there are two devices for the hands, which were held by the subject at the time of analysis. The adolescents were in a standing position, with the arms and legs extended, in accordance with the manufacturer’s instructions; the analyses were performed in the morning, without the subject having done exercise or eaten before this (at least 2 hours after the last meal).

2.6. Evaluation of Maximum Bite Force

The maximum unilateral bite force was measured using a digital gnatodynamometer (model DDK, Kratos Equipamentos Industriais Ltda., Cotia, SP, Brazil), as described previously (Kobayashi et al., 2014). The equipment has a 10 mm force fork connected to a digital appliance, which provided the maximum bite force values in Newtons (N). During the evaluation, the subject remained seated, with the head in a relaxed position and the fork was placed between the maxillary and mandibular arches, at the permanent first molars. The adolescent was instructed and trained before to bite it with maximum force, and two measurements were made for each side of the dental arches (left and right). The maximum value of the two measurements on each side was considered as final value, with an approximation of 0.1N.

Masticatory performance was measured by colorimetric method using a color-changeable chewing gum specifically developed for this purpose. The chewing gum changes color as mastication proceeds. The gum base contains red, yellow, and blue dyes, citric acid and xylitol. The red dye is pH-sensitive and appears under neutral or alkaline conditions. As the pH inside the chewing gum is kept low by the citric acid, the color of the chewing gum remains yellowish-green before chewing. With the progression of chewing, the color of the chewing gum turns from yellowish-green to red because the yellow and blue dyes seep into saliva, and the red dye appears as a result of elution of the citric acid (Komagamine et al., 2011). After chewing, color measurement can be performed using a spectrophotometer or a color scale.

Subjects were asked to chew the color-changeable chewing gum for 1 minute, as they usually chew (“Please chew the gum well”). The time spent was measured with a chronometer. In the measurement, the chewed gum extracted immediately after chewing was compressed between two plastic films and pressed into an approximately 30-mm diameter disk. Color was measured using a color scale (Figure 1), a method previously developed and validated (Hayakawa et al, 1998, Hama et al., 2014) to assess color change by visually.

The test was repeated twice for the same subject. Two examiners evaluated the color (APP and DSA), who were trained before with both methods: color scale and reflectance spectrophotomer. A spectrophotometer (Konica Minolta CM-700d-Konica Minolta Investment Ltd. Sensing Business Division, Shanghai, China) was used to measure the colour of the chewing gum, based on the CIE L*a*b* colour space system; the Spearman correlation coefficient obtained between spectrophotomer and examiner 1 (scale) was 0.84 (p=0.0006) and the correlation coefficient between spectrophotomer and examiner 2 was 0.92 (p<0.0001). After this, all chewed color-changeable chewing gums were evaluated using the color scale.

Figure 1. Color scale specifically designed for the evaluation of color changes of the chewing gum from yellowish-green to red (Hama et al., 2014)

2.8. Oro-facial myofunctional evaluation

The expanded protocol Oro-facial myofunctional evaluation with scores (OMES-e) (Felício et al., 2012), was developed and validated in order to perform a comprehensive evaluation of the alterations⁄dysfunctions of the appearance, posture and⁄or mobility of the lips, tongue, mandible and cheeks and of the stomatognathic functions: deglutition, mastication, respiration and speech; in the present study, the domain “Mastication” was used.

The protocol includes the analysis of the incision (bite), masticatory type, movements of the head or other body parts, altered head posture, food escape and masticatory duration by using a standardized food (Bono® cookie, Nestlé, São Paulo, SP, Brazil). The assessments were recorded using a camera (Sony Cyber Shot DSC-HX300, São Paulo, Brazil) and the respective analysis was performed by an independent (blinded), trained and calibrated examiner (DGAP; Speech-Language Pathologist, PhD in Oral Physiology). According to the protocol, mastication was recorded with the individual sitting in a chair with a backrest, the feet resting on the floor at a standardized distance (1 m) from the camera lens, which was supported by a tripod with focus on the face, neck and shoulders. The individuals chewed the chocolate-flavored cookie and were instructed to chew it in their habitual manner (free chewing).

Further, all video-recordings were evaluated and each item scored, considering that higher the score, better the function performed. The type of incision was classified as: incision by incisors (score 4), canines or premolars (score 3), molars (score 2) or the lack of incision (score 1).

The mastication type was determined by counting the number of masticatory strokes (jaw movements of opening and closing until occurrence of contact of teeth). The following scores were attributed:

score 1 = when the patient did not perform the function;

score 2 = chronic unilateral, when the masticatory strokes occurred on the same side 95– 100% of the time, or anterior when the masticatory strokes occurred in the region of the incisors and canines;

score 4 = unilateral preference grade 2, when the masticatory strokes occurred on the same side 78–94% of the times;

score 6 = unilateral preference grade 1, when the masticatory strokes occurred on the same side 61–77% of the times;

score 8=simultaneously bilateral, with the masticatory strokes occurring on both sides of the oral cavity 95% of the times;

score 10= when it was bilateral and alternate, i.e. the masticatory strokes occurred on each side 50% of the times, or 40% on one side and 60% on the other.

In addition, the presence of other behaviors and signs of alterations were analyzed, such as movement and/or altered posture of the head and of other parts of the body, food escape and uncoordinated jaw movements. Score 1 was attributed to the presence of each of these items, and score 2 to the absence. The total time spent to consume the food was measured using a chronometer, which was started after the food was placed in the oral cavity and stopped after final swallowing of the food, in order to determined the chewing time in seconds (time taken for eating the test meal) and chewing frequency (cycles/min).

2.9. Subjective evaluation of masticatory quality

The subjective evaluation was carried out using a specific self-applied questionnaire translated to Portuguese from the original French version (Muller et al., 2008) and validated to be used in Brazilian adolescents (Hilasaca-Mamani et al., 2015, 2016). This questionnaire consists of 26 questions specifically related to the frequency of and difficulty of chewing different types of foods during the two weeks before the evaluation. The domains Food-Mastication, Habits, Meats, Fruits and Vegetables have 5 Likert-response options ranging from “always” to “never” or “a lot” to “no difficulty” and explore the difficulty with mastication in daily life. In addition, the domains Meats, Fruits and Vegetables also present an alternative to be checked (not applicable - N/A) if the subject does not usually eat these foods. Higher the score, worse the quality of mastication.

The following are examples of these questions:

 Do you have difficulty chewing hard, raw fruits, without cutting them (e.g.: apples)?  Do you have to drink while eating to facilitate swallowing?

 In general, is the food well chewed before being swallowed?  Do you have to add sauce to your meal to facilitate swallowing?

 Is it necessary to cut the apples into small pieces in order to chew them?  Has it been necessary to convert meet into puree in order to eat?

The questionnaire was applied in a reserved classroom. It was answered without any interference from the researcher.

2.10. Statistical analysis

Statistical analyses were performed with the statistical software packages BioEstat 5.3 (Mamirauá, Belém, PA, Brazil) and SigmaPlot 13 (Systat Software Inc., San Jose, CA, USA). A p-value of 0.05 was considered significant.

A pilot study was conducted before beginning the data collection to verify the reproducibility of the measurements made, and later calculation of agreement (Kappa test) and intraclass correlation coefficient (ICC).

The descriptive statistics consisted of means, standard deviation, median, interquartile range and percentages; normality tests were used to verify the distribution of the variables. Comparisons between normal-weight and overweight/obese groups for each gender were performed using unpaired t-test or Mann-Whitney test, where appropriate. Frequencies and proportions were tested using Chi-square test.

Later, a multiple linear regression model was used to evaluate which of the variables under study contributed to the variation in Percent Body Fat. The model was adjusted using the “Best Subsets”, which is an automated procedure that identifies the best-fitting regression models with predictors specified in the study with smaller variance than the full model using all predictors. In this study, the chosen model was the one which presented the highest adjusted R-square and the variance inflation factor (VIF) at or near 1.0. Based on biological plausibility, the following independent variables were added to the initial model: age, gender, masticatory performance, bite force, OMES-e total score, scores on Masticatory Quality Questionnaire, chewing time and chewing frequency.

RESULTS

The intra-examiner reproducibility observed for the studies variables ranged from satisfactory (PAR) to excellent reproducibility (DMFT), as shown in Table1.

Table 1. Measurements of reproducibility for the variables evaluated in the pilot study

Variables N Test Values

DMFT 20 Kappa 0.97 PAR OMES-e 15 15 Intraclass Correlation Intraclass Correlation 0.48 0.86

Bite Force 15 Intraclass Correlation 0.97

MP – examiner 1 12 Intraclass Correlation 0.66 MP – examiner 2 12 Intraclass Correlation 0.78 MP – between examiners 1 and 2 12 Intraclass Correlation 0.90

DMFT, index of decayed missing and filled permanent teeth; PAR, Peer Assessment Rating index; OMES-e, oro-facial myofunctional evaluation with scores; MP, masticatory performance.

Table 2 shows the clinical and anthropometric characteristics of the sample. Age and PAR index (malocclusion) did not differ significantly between the groups (normal-weight, overweight/obese). As expected, BMI, percent of body fat and abdominal obesity degree were higher in overweight/obese groups and in females, while greater skeletal muscle mass was observed in normal-weight groups and in males.

Table 2. Sample characteristics according to anthropometric measurements

Groups (n)

Age (y) PAR index BMI

(Kg/m2) Percent Body Fat Abdominal Obesity Degree Skeletal muscle mass/ total weight Mean (SD) Median (25-75%) Median (25-75%) Mean (SD) Mean (SD) Mean (SD) Girls (119) Normal-weight (60) 15.88 (0.96) 6.00 (2.25-11.0) 20.18† (19.20-21.48) 26.76* (5.58) 0.86†† (0.84-0.89) 0.40†† (0.38-0.42) Overweight/Obese (59) 16.01 (0.98) 7.00 (3.00-12.00) 28.06† (25.32-30.32) 39.63* (6.18) 0.96†† (0.92-1.00) 0.33†† (0.31-0.35) Boys (112) Normal-weight (55) 15.95 (1.09) 6.00 (4.00-12.00) 20.16† (18.20-21.96) 13.23* (4.49) 0.79†† (0.78-0.81) 0.48†† (0.47-0.50) Overweight/Obese (57) 15.90 (0.95) 7.00 (4.00-10.60) 26.99† (25.26-30.70) 27.99* (7.70) 0.90†† (0.87-0.97) 0.41†† (0.37-0.44) Comparison between genders Normal-weight p=0.7120 p=0.4315 p=0.4447 p<0.0001** p<0.0001** p<0.0001** Overweight/Obese p=0.5373 p=0.9758 p=0.3338 p<0.001* p=0.003† _p<0.001†

SD, standard deviation; PAR, Peer Assessment Rating index; BMI, body mass index. * p<0.05 (unpaired t-test)

**p<0.0001 (unpaired t-test)

†

p<0.05 (Mann-Whitney test)

†† _{p<0.0001 (Mann-Whitney test)}

Table 3 shows the comparison of maximum bite force, masticatory performance, Orofacial myofunctional evaluation scores (OMES-e), chewing time and chewing frequency between groups. OMES-e total scores were significantly higher in overweight/obese groups, that is, more changes when performing the masticatory function. When exploring the item which significantly contributed to such difference, higher frequency of unilateral mastication was observed in females with weight excess (p=0.0217).

Masticatory performance evaluated by means of a color-changeable chewing gum did not differ between the groups. Also, maximum bite force, chewing time and chewing frequency did not differ significantly between groups.

Table 3. Comparisons of bite force, oro-facial myofunctional evaluation with scores (OMES-e), masticatory performance, swallowing threshold and masticatory frequency between groups

Bite force (N) OMES-e total score Masticatory performance Chewing time (sec) Chewing cycles/min Mean (SD) Median (25-75%) Mean (SD) Median (25-75%) Mean (SD) Girls Normal-weight (60) 399.43 (154.57) 17.00 † (14.00-20.00) 7.25 (0.94) 48.25 (13.11) 61.50 (11.73) Overweight/Obese (59) 399.90 (188.98) 14.00 † (10.00-17.50) 7.12 (1.13) 45.66 (12.80) 61.62 (13.22) Boys Normal-weight (55) 578.65 (196.29) 16.00 †† (15.00-17.00) 7.77 (0.96) 37.67 (10.86) 67.25 (13.99) Overweight/Obese (57) 536.52 (188.19) 11.00 †† (9.00-14.00) 7.48 (0.92) 36.88 (10.71) 68.51 (10.75)

† _{p<0.05 (Mann Whitney test)} ††

p<0.0001 (Mann Whitney test)

The subjective evaluation of the masticatory quality also showed significant difference between nutritional groups among females. The scores on “Habits” and “Fruit” domains were higher among overweight/obese females when comparing with normal-weight ones, thus females with weight excess presented greater difficulty in performing the masticatory function. Each item of the “Habits” and “Fruit” domains was also tested between groups; according to the results found, overweight/obese females frequently reported the need of adding sauce to the meal to facilitate swallowing and peeling and cutting fruits (apples) in small pieces in order to chew them (p<0.05).

Table 4. Quality of Masticatory Function Questionnaire: score comparison between groups

Groups

Food-Mastication Habits Meat Fruits Vegetables

Median (25-75%) Girls Normal-weight (60) 2.00 (0.00-4.00) 4.00 † (2.00-5.00) 2.00 (0.00-5.25) 1.00† (0.00-4.00) 3.50 (0.00-5.00) Overweight/Obese (59) 2.00 (0.50-5.75) 5.00 † (3.00-6.00) 4.00 (0.00-7.00) 3.00† (1.00-6.50) 3.00 (0.00-5.00) Boys Normal-weight (55) 2.00 (0.00-4.00) 4.00 (2.00-5.50) 2.00 (0.00-4.00) 1.00 (0.00-3.00) 3.00 (2.00-4.00) Overweight/Obese (57) 2.00 (1.00-5.00) 4.00 (2.00-6.00) 1.00 (0.00-4.00) 2.00 (0.00-3.00) 3.00 (0.00-4.00) † p<0.05 (Mann-Whitney test)

Using the multiple linear regression model (Table 5), it was observed significant positive relation between the dependent variable Percent body fat and the female population, and negative relation with the OMES-e total score. A higher percentage of body fat was associated with the female gender and more changes in oro-facial myofunctional evaluation, with an adjusted R-squared equal to 43.9%.

Table 5. Multiple linear regression model of subject’s variables on Percent Body Fat

Dependent variable: Percent Body Fat

Coefficient p-value VIF

Model F (p-value) R2 adjusted Power 5% Constant 36.105 - - 19.005 (<0.001) 0.439 1.000 Gender (female) 10.627 <0.001 1.284 Bite force -0.005 0.135 1.204

OMES-e total score -0.299 0.040 1.126 Swallowing threshold 0.057 0.359 1.496

Chewing rate -0.058 0.341 1.441

Normality Test: p = 0.553 Constant Variance Test: p = 0.100

DISCUSSION

Due to the high prevalence of overweight and obesity, studies have focused on weight management and a better understanding of the factors that may influence satiety, nutrition and weight gain. The present study found that overweight/obese subjects showed more changes in oro-facial myofunctional evaluation when performing the masticatory function; the protocol covers the type of incision, mastication type, and posture alterations. The regression analysis confirmed this result, with a significant relationship between body fat percentage and OMES-e total score. The decreased muscle tone and/or the restriction of mandibular movements may impact bolus formation; in addition, large volumes of air can be swallowed together with the food, which may lead to an overload the stomach in its mechanical activity to mix a poorly prepared bolus (Gonçalves and Chehter, 2012). The subjects can also compensate an inefficient function by head/body movements, chewing using the incisors or compressing the food against the palate with the tongue (Padovani et al., 2007).

The unilateral pattern of mastication was more frequent among overweight/obese female adolescents than normal-weight. Unilateral masticatory pattern has been associated to unilateral crossbite, structural asymmetries and functional impairments (Diernberger et al., 2008). During the unilateral chewing, an increased muscle power on the working side is observed, specifically the buccinator, masseter and temporalis muscles, and the persistence of an altered function during growth promotes gradual changes in skeletal and tooth structures that may result in dentofacial asymmetries in adulthood (Poikela et al., 1995; Poikela et al., 1997; Amaral, 2000). In addition, a past study demonstrated that during unilateral chewing, saliva is not well distributed around the mouth and has a tendency to stay on the chewing side of the mouth, where saliva is predominantly produced (McDonnell and Hector, 2001). The prevalence of the vertical pattern during mandibular movements was also previously described (Gonçalves and Chehter, 2012). The implications of these altered mandibular movements on bolus formation and its characteristics in terms of viscosity, cohesion and particles size were poorly explored in previous studies and need further attention.

Although the chewing time and chewing frequency did not differ significantly between groups, alterations in the time taken for eating the test-meal and number of chews were reported among obese children (Sato and Yoshiike, 2010) and morbidly obese patients (Gonçalves and Chehter, 2012), and reported in adults using self-administered questionnaires (Sasaki et al., 2003; Otsuka et al., 2006). Recent studies corroborate the

present findings (Frecka et al., 2008; Isabel et al., 2015; Park and Shin, 2015), in which no significant differences in these objectives measures were seen. It is important to recognize that the type of food and the differences in food texture may influence the subjects’ acceptance and behavior; as this study used only one type of test-food (cookie), this may have influenced the time spent and number of chews (Bornhorst and Singh, 2012). In addition, the gender effect on bite force, bite size and chewing time seems to be of great importance, with men showing greater bite force, chewing power and frequency (Isabel et al., 2015; Park and Shin, 2015). Fast eating rate may be associated with detrimental effects, such as overeating (reduced satiety) (Zhu et al., 2013), swallowing larger particles and mechanical abrasion of the esophagus (Gonçalves and Chehter, 2012); in any situation, counseling aimed at slowing the rate of ingestion may be worth (Park and Shin, 2015).

The maximum bite force and the masticatory performance did not differ between nutritional groups. According to the literature, bite force may vary according to dental health, facial morphology, age, and, to a larger extend, to gender (Bonjardim et al., 2005; Roldán et al., 2009; Isabel et al., 2015). It is believed that subjects with greater occlusal force are able to break down food particles into the appropriate size; in addition, they would eat vegetables and fibers more frequently, once the ability of mastication is influenced by dietary behavior (Sato and Yoshiike, 2011). Previous findings also did not observe a relationship between bite force and body measurements in adults and young subjects (Gavião et al., 2007; Lujan-Climent et al., 2008; Castelo et al., 2010), although Araujo et al. (2015) showed a trend toward bite force being dependent on BMI in pre-pubertal children.

The masticatory performance evaluated by a color-changeable chewing-gum did not differ between normal-weight and overweight/obese groups, corroborating a recent study in adults which did not find significant differences in masticatory objective aspects between individuals with high and normal BMI (White et al., 2015). In contrast, in the study of Isabel et al. (2015), obese adults showed the largest median particles sizes using a test-material (Optosil), that is, they were more likely to swallow larger particles. In children, a relationship between sugar elution rate from a chewing gum and the degree of obesity was observed (Kibayashi, 2011). Previous attempts to identify differences in masticatory performance between obese and non-obese subjects have found conflicting results; as cited above, it is important to consider that the properties of the food being chewed, in terms of its hardness, fat content, size, and structure may influence the evaluations. Natural foods have the advantage of being well accepted and more pleasant taste and texture, and chewing gum also has the advantage of being routinely consumed by adolescents (Matsubara et al., 2006). The use of other types of food would be advisable, although due to the complexity of the

masticatory function, it is reasonable that differences between groups would be seen in some of the physiological (chewing time and frequency, bite force, jaw movements, chewing efficiency and/or performance) and/or behavioral (food choice and preparation) aspects, but probably not in all aspects.

Food preparation methods, such as chopping, roasting or salting, influence the number of masticatory cycles required before swallowing (Frecka et al., 2008). Thus, when evaluating masticatory function in relation to diet, it is important to gain an understanding of how people prepare and choose their foods (Hilasaca-Mamani et al., 2016). The subjective assessment may also include other aspects of masticatory function, such as the ability to adapt to daily activities and the psychological factors, which may not be obtained by objective measures. By applying a self-administered questionnaire, it was observed that the overweight/obese females reported greater difficulty in performing the masticatory function, specifically in the “Habits” and “Fruit” domains, when compared with the normal-weight ones. Difficulty with mastication is the probable mechanism by which feeding/swallowing disorders may affect food intake, particularly foods with greater consistency, thereby impacting nutritional status. For example, in denture wearers it is possible that the need to cut or chop certain types of foods cause some inconvenience in daily routine and, over time, these individuals could start eating less amounts of harder foods, which would reflect in their nutritional parameters (Muller et al., 2008).

When testing each item of the “Habits” and “Fruit” domains, overweight/obese females reported the need of adding sauce to the meal to facilitate swallowing and peeling and cutting fruit (apples) in small pieces in order to chew them. This result shows that overweight/obese female adolescents did not differ from normal-weight ones in masticatory performance, but indeed in how food is chosen and prepared. In addition, the habit of adding sauce or gravies to moisten the meal to facilitate swallowing may facilitate the swallowing of large particles before the bolus is well formed. Further studies are needed to verify if those habits are related to fiber-rich foods avoidance, once consistent unbalanced food selection could result in poor diets, high in calories but low in fiber, vitamins, and proteins (Willett, 1994). Furthermore, changes in mastication can affect mandibular condylar cartilage growth and mandibular morphology. It is considered that dietary education at an early age is important in order to prevent disruption of the development of the mandible (Enomoto et al., 2010).

Masticatory efficiency and masticatory behavior are aspects that in general are not directly related and, thus, changes in dietary patterns may not occur solely because the individual’s chewing efficiency improves (Ellis et al., 2008; Muller et al., 2008). In addition,

dietary intake may be influenced by a variety of sociocultural factors (Drewnowski and Specter, 2004), which means that in order to promote weight maintenance it is important to understand of how the individual select and prepare his food.

Considering that the dental health may have a strong impact on mastication, it is advisable that the occlusal conditions should be similar in all groups when evaluating masticatory performance (Isabel et al., 2015), which was warranted in this study in terms of the number of teeth, tooth integrity and malocclusion. The study design - cross-sectional – limits generalization of the findings, although the results found showed important trends to be evaluated in a future longitudinal study in order to explore a cause and effect relationship.

Acknowledgments

This study was supported by the State of São Paulo Research Foundation (FAPESP, SP, Brazil, n. 2014/24804-4).

Color Scale was kindly provided by Prof. Eijiro Yamaga.

REFERENCES

Amaral DB. Unilateral Chewing X Normal Oclusion: a study about your occurrence in children of 4 to 5 years old. Rev CEFAC 2000;2, 23-30.

Araujo DS, Marquezin MCS, de Souza Barbosa T, Gavião MBD, Castelo PM. Evaluation of masticatory parameters in overweight and obese children. Eur J Orthod 2015;cjv092.

Bellisle F, Guy-Grand B, Le Magnen J. Chewing and swallowing as indices of the stimulation to eat during meals in humans: effects revealed by edogram method and video recordings. Neurosci Biobehav Ver 2000;24 (2): 223-8.

Bes-Rastrollo M, van Dam RM, Martinez-Gonzalez MA, Li TY, Sampson LL, Hu FB. Prospective study of dietary energy density and weight gain in women. Am J Clin Nutr 2008;88(3), 769-777.

Bonjardim LR, Gavião MBD, Pereira LJ, Castelo PM. Bite force determination in adolescents with and without temporomandibular dysfunction. J Oral Rehabil 2005; 32(8):577–583.

Bornhorst GM, Singh RP. Bolus formation and disintegration during digestion of food carbohydrates. Compr Rev Food Sci Food Saf 2012; 11(2), 101-118.

Brennan AM, Sweeney LL, Liu X, Mantzoros CS. Walnut consumption increases satiation but has no effect on insulin resistance or the metabolic profile over a 4-day period. Obesity (Silver Spring). 2010 Jun;18(6):1176-82.

Castelo PM, Pereira LJ, Bonjardim LR, Gavião MBD. Changes in bite force, masticatory muscle thickness, and facial morphology between primary and mixed dentition in preschool children with normal occlusion. Ann Anat 2010;192(1):23–26.

Chaves TC, Oliveira AS, Grossi DB. Principais instrumentos para avaliação da disfunção temporomandibular, parte I: índices e questionários; uma contribuição para a prática clínica e de pesquisa. Fisioter Pesq 2008;15(1):92-100.

Diernberger S, Bernhardt O, Schwahn C, Kordass B. Self-reported chewing side preference and its associations with occlusal, temporomandibular and prosthodontic factors: results from the population-based Study of Health in Pomerania (SHIP-0). J Oral Rehabil. 2008 Aug;35(8):613-20.

Doll HA, Petersen SE, Stewart-Brown SL. Obesity and physical and emotional well-being: associations between body mass index, chronic illness, and the physical and mental components of the SF-36 questionnaire. Obes Res. 2000 Mar;8(2):160-70.

Drewnowski A, Specter SE. Poverty and obesity: the role of energy density and energy costs. Am J Clin Nutr 2004;79(1), 6-16.

Ellis JS, Thomason JM, Jepson NJ, Nohl F, Smith DG, Allen PF. A randomized-controlled trial of food choices made by edentulous adults. Clin Oral Implants Res 2008;19(4):356-61.

Enomoto A, Watahiki J, Yamaguchi T, Irie T, Tachikawa T, Maki K. Effects of mastication on mandibular growth evaluated by microcomputed tomography. Eur J Orthod. 2010 Feb;32(1):66-70.

Felício CM, Ferreira CLP, Medeiros APM, Da Silva MAMR, Tartaglia GM, Sforza C. Electromyographic indices, orofacial myofunctional status and temporomandibular disorders severity: a correlation study. J Electromyogr Kinesiol 2012;22(2), 266-272.

Frecka JM, Hollis JH, Mattes RD. Effects of appetite, BMI, food form and flavor on mastication: almonds as a test food. Eur J Clin Nutr 2008;62(10):1231-8.

Gavião MBD, Raymundo VG, Rentes AM. Masticatory performance and bite force in children with primary dentition. Braz Oral Res 2007;21(2):146–152.

Gonçalves DA, Dal Fabbro AL, Campos JA, Bigal ME, Speciali JG. Symptoms of temporomandibular disorders in the population: an epidemiological study. J Orofac Pain 2010;24(3):270-8.

Gonçalves RDFM, Chehter EZ. Masticatory profile of morbidly obese patients undergoing gastroplasty. Rev CEFAC 2012;14(3), 489-497.

Hama Y, Kanazawa M, Minakuchi S, Uchida T, Sasaki Y. Reliability and validity of a quantitative color scale to evaluate masticatory performance using color-changeable chewing gum. J Med Dent Sci 2014;61, 1-6.

Hatch JP, Shinkai RSA, Sakai S, Rugh JD, Paunovich ED. Determinants of masticatory performance in dentate adults. Arch Oral Biol 2000;46(7), 641-648.

Hayakawa I, Watanabe I, Hirano S, Nagao M, Seki T. A simple method for evaluating masticatory performance using a color-changeable chewing gum. Int J Prosthodont. 1998 Mar-Apr;11(2):173-6.