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Influência da morfologia craniofacial sobre disfunções temporomandibulares, força de mordida, performance e habilidade mastigatórias = Influence of craniofacial morphology on temporomandibular disorders, bite force, masticatory performance and chewing abi

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PAULA FURLAN BAVIA

“INFLUÊNCIA DA MORFOLOGIA CRANIOFACIAL SOBRE DISFUNÇÕES TEMPOROMANDIBULARES, FORÇA DE MORDIDA, PERFORMANCE E

HABILIDADE MASTIGATÓRIAS”

“INFLUENCE OF CRANIOFACIAL MORPHOLOGY ON

TEMPOROMANDIBULAR DISORDERS, BITE FORCE, MASTICATORY PERFORMANCE AND CHEWING ABILITY”

Piracicaba 2015

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PAULA FURLAN BAVIA

“INFLUÊNCIA DA MORFOLOGIA CRANIOFACIAL SOBRE DISFUNÇÕES TEMPOROMANDIBULARES, FORÇA DE MORDIDA, PERFORMANCE E

HABILIDADE MASTIGATÓRIAS”

“INFLUENCE OF CRANIOFACIAL MORPHOLOGY ON

TEMPOROMANDIBULAR DISORDERS, BITE FORCE, MASTICATORY PERFORMANCE AND CHEWING ABILITY”

Tese apresentada à Faculdade de Odontologia de Piracicaba da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de Doutora em Clínica Odontológica, na Área de Prótese Dental.

Thesis presented to the Piracicaba Dental School of the University of Campinas in partial fulfillment of the requirements for the degree of Doctor in Dental Clinic, in the area of Dental Prosthesis. Orientadora: Prof.a Dr.a Renata Cunha Matheus Rodrigues Garcia

Este exemplar corresponde à versão final da tese defendida pela aluna Paula Furlan Bavia, e orientada pela Prof.a Dr.a

Renata Cunha Matheus Rodrigues Garcia. ______________________________ Assinatura da Orientadora

Piracicaba 2015

UNIVERSIDADE ESTADUAL DE CAMPINAS

Faculdade de Odontologia de Piracicaba

Faculdade de Odontologia de Piracicaba

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Ficha catalográfica

Universidade Estadual de Campinas

Biblioteca da Faculdade de Odontologia de Piracicaba Marilene Girello - CRB 8/6159

Bavia, Paula Furlan,

B329i BavInfluência da morfologia craniofacial sobre disfunções temporomandibulares, força de mordida, performance e habilidade mastigatórias / Paula Furlan Bavia. – Piracicaba, SP : [s.n.], 2015.

BavOrientador: Renata Cunha Matheus Rodrigues Garcia.

BavTese (doutorado) – Universidade Estadual de Campinas, Faculdade de Odontologia de Piracicaba.

Bav1. Dor facial. 2. Mastigação. 3. Articulação temporomandibular. I. Rodrigues-Garcia, Renata Cunha Matheus,1964-. II. Universidade Estadual de Campinas. Faculdade de Odontologia de Piracicaba. III. Título.

Informações para Biblioteca Digital

Título em outro idioma: Influence of craniofacial morphology on temporomandibular disorders,

bite force, masticatory performance and chewing ability

Palavras-chave em inglês:

Facial pain Mastication

Temporomandibular joint

Área de concentração: Prótese Dental Titulação: Doutora em Clínica Odontológica Banca examinadora:

Renata Cunha Matheus Rodrigues Garcia [Orientador] Bruno D'Aurea Furquim

Larissa Soares Reis Vilanova Celia Marisa Rizzatti Barbosa Rafael Leonardo Xediek Consani

Data de defesa: 11-06-2015

Programa de Pós-Graduação: Clínica Odontológica

Powered by TCPDF (www.tcpdf.org)

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  vii   RESUMO

A morfologia craniofacial no sentido vertical está relacionada com as proporções e configurações da musculatura mastigatória, a qual pode ser influenciada pela presença de disfunções temporomandibulares (DTMs), afetando as funções orofaciais, como por exemplo, a mastigação e deglutição. Desta forma, dois estudos foram conduzidos e compõem esta tese. O objetivo no primeiro estudo foi verificar a presença da associação entre DTM e morfologia craniofacial. Para tanto, foram selecionados duzentos voluntários (com idade entre 18 e 50 anos) da Faculdade de Odontologia de Piracicaba, os quais foram divididos em dois grupos: (1) voluntários com DTM (n = 100, sendo 90 indivíduos do gênero feminino e 10 do gênero masculino) (idade média 27,80 ± 6,10 anos), e (2) voluntários sem DTM (n = 100, sendo 90 indivíduos do gênero feminino e 10 do gênero masculino) (idade média 25,90 ± 5,20 anos). O diagnóstico de DTM foi realizado por meio do sistema de diagnóstico Research Diagnostic Criteria for Temporomandibular Disorders

(RDC/TMD). Em seguida, foram obtidas telerradiografias convencionais em norma lateral e

após análise cefalométrica de Ricketts os voluntários foram classificados como Braquifaciais, Mesofaciais ou Dolicofaciais. O segundo estudo objetivou avaliar a influência da morfologia craniofacial na força máxima de mordida; na performance e habilidade mastigatórias em indivíduos com DTM sintomática. Para tanto, indivíduos do primeiro estudo que apresentaram tempo de dor de no mínimo 3 meses, com intensidade maior ou igual a cinquenta milímetros mensurada por meio da escala visual analógica (EVA) foram incluídos. Desta maneira, 48 indivíduos (com idade entre 18 e 45 anos) do gênero feminino com DTM sintomática (idade média 27,71 ± 5,79 anos) foram divididos em 3 grupos: (1) braquifacial (n = 22); (2) mesofacial (n = 13); e (3) dolicofacial (n = 13). A função mastigatória foi avaliada por meio da mensuração da força máxima de mordida, performance e habilidade mastigatórias. Para o primeiro estudo os dados foram submetidos aos testes de Tukey-Kramer e qui-quadrado de razão de verossimilhança, e para o segundo estudo foi utilizado análise de variância um fator seguido de teste de Tukey-Kramer (α = 0,05). Os resultados do primeiro estudo demonstraram que não houve associação entre a morfologia craniofacial e a presença de DTM (p = 0,6622), no entanto observou-se

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associação entre a morfologia craniofacial e a presença de dor (p = 0,0077). No segundo estudo, verificou-se diferença significante na força máxima de mordida (p = 0,0001) entre os grupos, sendo os maiores valores encontrados em indivíduos braquifaciais, no entanto não foram encontradas diferenças na performance mastigatória (p= 0,4543). Em acréscimo, houve diferença significante (p = 0,0141) entre os grupos na habilidade mastigatória de apenas um dos componentes avaliados, no qual os indivíduos braquifaciais apresentaram os melhores valores de habilidade. Apesar de não ter sido observada associação entre a morfologia craniofacial e DTM, evidencia-se a importância de uma atenção especial em indivíduos braquifaciais, os quais estão mais susceptíveis a apresentarem DTM sintomática. Além disso, a morfologia craniofacial influenciou a força máxima de mordida, mas não afetou a performance e habilidade mastigatórias em indivíduos com DTM sintomática.

Palavras-chave: Morfologia craniofacial. Mastigação. Dor facial. Articulação temporomandibular.

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  ix   ABSTRACT

Vertical craniofacial morphology is related with the proportions and settings of masticatory muscles, which can be influenced by temporomandibular disorders (TMD), affecting the orofacial functions, such as mastication and deglutition. Thus, two studies were conducted and compose this thesis. The aim of the first study was to investigate the presence of association between craniofacial morphology and TMD. Two hundred subjects (ranging from 18 to 50 years) were selected from Piracicaba Dental School and were divided into two groups: 1) subjects with TMD (n = 100, 90 females and 10 males) (mean age 27.80 ± 6.10 years), and 2) subjects without TMD (n = 100, 90 females and 10 males) (mean age 25.90 ± 5.20 years). TMD was diagnosed by the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD). Subsequently, lateral cephalometric radiographs were obtained and analyzed by Ricketts' cephalometric analysis and the subjects were classified as Brachyfacial, Mesofacial or Dolichofacial. The second study assessed the influence of craniofacial morphology on maximum bite force; masticatory performance and chewing ability in subjects with painful TMD. Subjects from the first study presenting pain for at least 3 months, with a minimum pain intensity of 50 mm measured using a visual analog scale (VAS) were included. Thus, fourty-eight female subjects with TMD (ranging from 18 to 45 years) (mean age 27.71 ± 5.79 years) were divided into three groups: 1) brachyfacial (n = 22); 2) mesofacial (n = 13); and 3) dolichofacial (n = 13). Masticatory function was assessed through maximum bite force, masticatory performance and chewing ability tests. For the first study data were submitted to Tukey-Kramer and to the Likelihood Ratio Chi-Square tests and for the second, data were analyzed using ANOVA one-way, followed by Tukey-Kramer test (α = 0,05). The results of the first study demonstrated that there was no association between craniofacial morphology and TMD (p = 0.6622). However, craniofacial morphology was associated with painful TMD (p = 0.0077). In the second study, significant difference (p = 0.0001) was observed in maximum bite force values among the three groups, being the higher values exhibited by brachyfacial individuals. No difference (p > 0.05) was found for masticatory performance values among groups. In addition, the ability to chew only one of

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the evaluated foods was significant among the groups (p = 0.0141), and brachyfacial subjects showed the best chewing ability. Although there was no association between craniofacial morphology and TMD, attention should be given to brachyfacial subjects, which are more susceptible to present TMD pain symptoms. In addition, craniofacial morphology influenced the maximum bite force, without impairing the masticatory performance and chewing ability of painful TMD subjects.

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  xi   SUMÁRIO DEDICATÓRIA ... xiii AGRADECIMENTO ESPECIAL ... xv AGRADECIMENTOS ... xvii INTRODUÇÃO ... 1

CAPÍTULO 1: Craniofacial morphology and its association with painful temporomandibular disorders ... 4

CAPÍTULO 2: Craniofacial morphology affects maximum bite force in patients with painful temporomandibular disorders ... 19

CONCLUSÃO ... 35

REFERÊNCIAS ... 36

ANEXOS ... 40

ANEXO 1 – Certificado de aprovação do Comitê de Ética em Pesquisa da Faculdade de Odontologia de Piracicaba ... 40

ANEXO 2 - Figuras ... 41

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DEDICATÓRIA

À Deus, por me dar forças e coragem para vencer cada obstáculo enfrentado e por me iluminar na concretização deste sonho.

Aos meu pais, Paulo Domingos Bavia e Marlene Furlan Bavia. Muito obrigada seria pouco para agradecer à vocês pelo exemplo, amor e dedicação. A realização deste sonho não seria possível sem o incentivo de vocês.

Dedico essa tese à vocês!

À minha irmã Ana Carla Furlan Bavia Tripoloni, pelo amor incondicional. Obrigada por me fortalecer sempre com suas palavras de amor. Nos momentos difíceis, sei que meu nome estava sempre em suas orações. Essa conquista também é sua!

Ao meu esposo e eterno companheiro, André Barbisan de Souza, por não medir esforços para me ajudar nos momentos em que mais precisei. Obrigada por me encorajar em tudo o que faço e por ser sempre tão paciente comigo. Obrigada por estar ao meu lado em mais uma vitória!

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AGRADECIMENTO ESPECIAL

À Profa. Dra. Renata Cunha Matheus Rodrigues Garcia, obrigada pela orientação, pelos conhecimentos transmitidos e pela confiança em mim depositada ao longo destes anos. Obrigada por tornar possível a realização deste doutorado.

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AGRADECIMENTOS

À Universidade Estadual de Campinas, na pessoa do Magnífico Reitor Prof. Dr. José Tadeu Jorge.

À Faculdade de Odontologia de Piracicaba da Universidade Estadual de Campinas, na pessoa de seu Diretor, Prof. Dr. Guilherme Elias Pessanha Henriques, e de seu Diretor Associado, Prof. Dr. Francisco Haiter Neto.

À Coordenadora dos Cursos de Pós-Graduação da Faculdade de Odontologia de Piracicaba da Universidade Estadual de Campinas, Profa. Dra. Cínthia Pereira Machado Tabchoury.

À Coordenadora do Programa de Pós-Graduação em Clínica Odontológica da Faculdade de Odontologia de Piracicaba, Profa. Dra. Karina Gonzales Silvério Ruiz.

Às Professoras Dras. Altair Antoninha Del Bel Cury e Célia Marisa Rizatti Barbosa e ao Prof. Wander José da Silva, pelo apoio e ensinamentos, os quais contribuíram para meu amadurecimento profissional.

A todos os docentes do Programa de Pós-Graduação em Clínica Odontológica da Faculdade de Odontologia de Piracicaba, Universidade Estadual de Campinas, que de alguma forma contribuíram para meu crescimento profissional.

Aos voluntários da pesquisa, fundamentais para a realização deste trabalho. Aos meus pais Paulo Domingos Bavia e Marlene Furlan Bavia, obrigada pela minha formação, por me guiar pelo caminho do bem, pelos valores transmitidos e sobretudo por acreditarem em mim e por sonharem comigo.

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À minha irmã Ana Carla Furlan Bavia Tripoloni e ao meu cunhado Antonio Tripoloni Neto, obrigada por torcerem sempre por mim e por vibrarem com as minhas conquistas.

Ao meu esposo André Barbisan de Souza, obrigada por estar sempre perto apesar da distância física e por me apoiar desde o início dessa trajetória, sempre com muita paciência e compreensão.

Aos meus avós Jacinto e Ana Furlan, obrigada pelas orações, pelo amor e por sempre torcerem pelo meu sucesso.

Aos meus avós José (in memorian) e Carlita Bavia, por seus ensinamentos e por demonstrarem seu orgulho e confiança na sua eterna “doutorzinha”.

À toda a minha família, tios, tias e primos. A união desta família maravilhosa me fortalece muito e ameniza qualquer distância ou dificuldade. Obrigada pelo carinho e pelo apoio.

Aos meus sogros Alcílio José de Souza Filho e Márcia Regina Barbisan de Souza, obrigada pelo incentivo e por acreditarem em mim.

Aos meus amigos Fabrício Kaminagakura, Rayssa Rossi, Nathália Ribeiro, Kelly Rodrigues e Cynthia Muller, que mesmo à distância, nunca se fizeram ausentes, apoiando minhas decisões e vibrando com minhas conquistas.

Às grandes amigas que fiz em Piracicaba Ana Paula Varella, Bruna Alfenas, Camila Heitor, Cindy Dodo, Indira Cavalcanti, Germana Camargos, Gisele Ribeiro, Larissa Vilanova, Lis Meirelles, Priscilla Lazari, Raissa Machado, obrigada pela amizade e pelo agradável convívio ao longo destes anos. Amigas que levarei para a vida toda.

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À amiga Lis Meirelles, minha companheira inseparável em Piracicaba, a quem devo muito, por estar sempre disposta a me ouvir e me apoiar desde o início da pós-graduação.

À amiga e querida técnica do Laboratório de Prótese Parcial Removível, Sra. Gislaine Regiane Alves Piton, por ser sempre tão prestativa e disposta a ajudar desde o início da pós-graduação. Obrigada por me auxiliar sempre de forma atenciosa e pelas palavras de apoio em diversos momentos desta trajetória.

A todos colegas do laboratório e da pós-graduação Bruno Zen, Conrado Caetano, Cláudia Brilhante, Kelly Andrade, Thaís Gonçalves, Dimorvan Bordin, Antônio Pedro Ricomini Filho, Marcele Pimentel, Sílvia Lucena, Luana Aquino, Giancarlo de La Torre, Edmara Bergamo, Samilly Souza, Aline Sampaio, Marco Aurélio de Carvalho, Plínio Senna, Andréa Araújo, obrigada pelo convívio e troca de experiências durante o curso.

Ao Santuário Nossa Senhora dos Prazeres, na pessoa do Padre Edvaldo, lugar iluminado e abençoado onde vivenciei momentos de paz e encontrei palavras de conforto.

À Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP, pela concessão de bolsa de estudo, processo número 2012/07282-9.

À Faepex, pela concessão de auxílio à pesquisa, processo número 519.292.

Às Sras. Érica Alessandra Pinho Sinhoreti, Ana Paula Carone e Raquel Q. Marcondes Cesar Sacchi secretárias da Coordenadoria dos Programas de Pós-Graduação da Faculdade de Odontologia de Piracicaba e à Sra. Eliete Aparecida Ferreira Marim secretária do Departamento de Prótese e Periodontia da Faculdade de Odontologia de Piracicaba, por estarem sempre prontas a ajudar.

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  1   INTRODUÇÃO

A disfunção temporomandibular (DTM) é uma patologia do sistema estomatognático relacionada a sinais e sintomas que podem acometer as articulações temporomandibulares (ATM) e a musculatura mastigatória, bem como estruturas correlatas (LeResche e Drangsholt, 2008; de Leeuw, 2013). Considerada como condição clínica relevante Manfredini et al. (2011) verificaram, por meio de revisão sistemática, que 45,3% da população adulta apresentam algum tipo de desordem muscular, 41,1% apresentam desordens articulares, especialmente deslocamento do disco articular, e 30,1% apresentam artralgia, osteoartrite e osteoartrose. Observou-se também que a maioria dos pacientes que busca tratamento para DTM é do gênero feminino, numa proporção de 3,3 : 1 (Manfredini

et al., 2011), e que os sinais e sintomas de DTM são frequentemente observados em

indíviduos adultos jovens ou de meia idade (Anastassaki Kohler et al., 2012).

A etiologia dos sinais e sintomas de DTM possui caráter multifatorial, apresentando fatores predisponentes, desencadeantes e perpetuantes, como hábitos parafuncionais (Blanco Aguilera et al., 2014; Fernandes et al., 2015); traumas (Häggman-Henrikson et al., 2014), além de problemas emocionais e psicológicos, como estresse, ansiedade e depressão (Manfredini et al., 2010; Reissman et al., 2014). Em acréscimo, características da morfologia craniofacial, como tamanho, formato e posicionamento da mandíbula, podem também estar relacionadas à DTM (Kwon et al., 2013). Estudos recentes (Bertram et al., 2012; Yang et al., 2012; Kwon et al., 2013) verificaram por meio de cefalometria que indivíduos com deslocamento de disco articular com e sem redução apresentaram ramo mandibular diminuído, ângulo goníaco e comprimento mandibular aumentados e rotação mandibular no sentido horário quando comparados a indivíduos sem deslocamento de disco. Além disso, essas diferenças no tamanho e na morfologia mandibular podem influenciar a relação maxilomandibular, bem como os aspectos esqueléticos relacionados à morfologia craniofacial no sentido vertical (Kwon et al., 2013). No entanto, pouco se sabe sobre a associação entre a morfologia craniofacial no sentido vertical e DTM.

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pode ser determinada por meio da análise de Ricketts, na qual são utilizadas cinco variáveis cefalométricas: (1) eixo facial; (2) altura facial anteroinferior; (3) profundidade facial; (4) plano mandibular; e (5) arco mandibular. A média aritmética destas variáveis determina o índice Vert que classifica os indivíduos em três padrões faciais denominados: (1) braquifacial,

caracterizado como face mais curta e larga e terço inferior da face diminuído; (2)

mesofacial, por apresentar terços faciais equidistantes; e (3) dolicofacial, definido pelo excesso vertical ou face longa e pela maior dimensão do terço inferior da face (Ricketts et

al., 1981). Sabe-se que indivíduos dolicofaciais apresentam diminuição da força máxima de

mordida (Abu Alhaija et al., 2010; Custodio et al., 2011), independente da presença de DTM. Em acréscimo, a presença da dor muscular, frequentemente observada em indivíduos com DTM (de Leeuw, 2013), pode também ocasionar a redução da capacidade da musculatura mastigatória e, consequentemente, diminuir a força máxima de mordida (Strini

et al., 2013). Desta forma, como a força de mordida está relacionada ao proceso de

mastigação (Gambareli et al., 2007), sugere-se que a morfologia craniofacial no sentido vertical pode, portanto, influenciar a mastigação de indivíduos com DTM sintomática.

A mastigação é um processo fisiológico complexo (van der Bilt et al., 2006) que envolve atividades neuromusculares e digestivas (Soboleva et al., 2005). Este processo é controlado pelo núcleo motor do nervo trigêmeo (Morquette et al., 2012), o qual recebe impulsos provenientes do córtex cerebral ativando os músculos abaixadores da mandíbula (pterigoideo lateral e supra-hioideos) (Westberg e Kolta, 2011), para que ocorra a abertura da boca, e consequentemente a entrada do alimento. Em seguida, os músculos elevadores (temporal, masseter e pterigoideo medial) da mandíbula são ativados, gerando sequência rítmica (Pereira et al., 2006) de abaixamento, elevação e lateralização da mandíbula ocorrendo a mastigação.

Considerada como a primeira etapa do processo digestivo, durante a mastigação, a língua, a musculatura facial e mastigatória agem simultaneamente posicionando o alimento entre os dentes (Trulsson et al., 2012), triturando-o em partículas menores a fim de facilitar a atividade enzimática e, consequentemente, a digestão (Abrahamsson et al., 2015). A avaliação da mastigação pode ser feita de forma objetiva por meio da mensuração da força de mordida e da performance mastigatória (Ikebe et al.,

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2005). A força de mordida está relacionada ao processo de trituração dos alimentos, previamente à deglutição (Gambareli et al., 2007). A performance mastigatória consiste na mensuração da capacidade do indivíduo em fragmentar os alimentos a partir de uma determinada quantidade de ciclos mastigatórios (Van der Bilt et al., 2002) e, pode, por sua vez, ser alterada pela força de mordida. De acordo com Pereira et al. (2009) indivíduos sem DTM apresentaram maiores valores de força de mordida e melhor performance mastigatória em comparação a indivíduos com DTM sintomática, sugerindo que quanto maior a força de mordida melhor é a performance (Lepley et al., 2011) e, consequentemente, a função mastigatória.

Além da avaliação objetiva, a mastigação pode ser subjetivamente avaliada por meio da verificação da habilidade mastigatória (Feine & Lund, 2006), a qual relaciona-se com a auto-percepção do indivíduo em avaliar sua própria função mastigatória (Carlsson, 1984). A dor e a limitação de abertura bucal durante a mastigação são as principais queixas relatadas em indivíduos com DTM (Ahn et al., 2011). Kurita et al., (2001) demonstraram que portadores de DTM apresentam habilidade mastigatória deficiente e verificaram que indivíduos sem DTM ingerem quaisquer tipos de alimentos sem dificuldade, enquanto que aqueles diagnosticados como portadores de DTM articular sintomática apresentam incapacidade severa para ingerir os mesmos alimentos. Além disso, foi observado também a correlação entre a ingestão de alimentos mais consistentes e presença de ruídos, dores articulares e limitação de abertura bucal, indicando que os hábitos alimentares podem estar associados com sintomas de DTM (Akhter et al., 2004). No entanto, não foram encontrados estudos comparando a habilidade mastigatória em indivíduos com diferentes padrões faciais.

Desta forma, tendo em vista que a morfologia craniofacial pode estar associada à presença de sinais e sintomas de DTM, os quais podem influenciar o padrão de mastigação, neste estudo o objetivo foi verificar a associação entre a morfologia craniofacial e DTM, bem como avaliar a influência desta associação sobre os parâmetros objetivos (força máxima de mordida e performance mastigatória) e subjetivo (habilidade mastigatória) da função mastigatória de indivíduos adultos.

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Craniofacial morphology and its association with painful temporomandibular disorders

This manuscript was submitted to Cranio. Journal of Craniomandibular Practice.

Paula Furlan Bavia, DDS, MSa

Larissa Soares Reis Vilanova, DDS, MSa Renata Cunha Matheus Rodrigues Garcia, Ph.D.b

a Graduate student

Department of Prosthodontics and Periodontology, Piracicaba Dental School, University of Campinas Piracicaba, Sao Paulo, Brazil.

b Professor

Department of Prosthodontics and Periodontology Piracicaba Dental School, University of Campinas Piracicaba, Sao Paulo, Brazil.

Paula Furlan Bavia graduated in Dentistry in 2011, at State University of Maringa – UEM, Maringa, Brazil. During undergraduation, she participated at the Orofacial Pain Clinic at State University of Maringa. She also attended a theoretical/practical course to improve her knowledge and skills in Occlusion & Orofacial Pain in 2010. Currently, she is a Ph.D Student, at Piracicaba Dental School, University of Campinas – UNICAMP, Sao Paulo, Brazil.

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Dr. Larissa Soares Reis Vilanova received her D.D.S. degree from Federal University of Goiás-UFG, Goiania, Brazil in 2010. As a Visitor Ph.D Student she developed part of her Ph.D research, between 2013-2014, at Malmo University. In 2014, she received her Ph.D. degree in Prosthodontics, at Piracicaba Dental School, University of Campinas – UNICAMP, Sao Paulo, Brazil. She is currently a Postdoctoral Student, at Federal University of Goias-UFG, Goiania, Brazil.

Dr. Renata Cunha Matheus Rodrigues Garcia is a Professor in the Department of Prosthodontics and Periodontology at Piracicaba Dental School, University of Campinas, Brazil. Since she received her Ph.D. degree in Prosthodontics in 1995 at the same University, she has been involved in Clinical Research. In 1997, she took Post-doctoral training in Craniomandibular Disorders at the University of Texas, Health Science Center at San Antonio, USA.

Corresponding author:

Renata Cunha Matheus Rodrigues Garcia

Department of Prosthodontics and Periodontology Piracicaba Dental School, University of Campinas

Av. Limeira, nº 901, Bairro Areião, Piracicaba, SP, Brazil, 13414-903 Phone Number: + 55 19 2106-5240 Fax number: + 55 19 2106-5211 e-mail: regarcia@fop.unicamp.br

Authors have no conflict of interest.

Acknowledgement

This research was supported by Sao Paulo Research Foundation – FAPESP (Grant number 2012/07282-9) and FAEPEX – UNICAMP (Grant number 519.292).

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  6   ABSTRACT

Objective: This study investigated the association between craniofacial morphology and temporomandibular disorders (TMD) in adults. The influence of different craniofacial morphologies on painful TMD was also evaluated.

Methods: Subjects (n = 200; mean age = 27.34 ± 6.46 years; range 18 to 50 years) were divided into two groups (n = 100 each) with and without TMD. TMD was diagnosed by Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD). Lateral cephalometric radiographs were obtained and subjects were classified as brachyfacial, mesofacial, or dolichofacial by Ricketts' analysis. Data were analyzed by Tukey-Kramer and Chi-Square tests.

Results: No association between craniofacial morphology and TMD was found (P = 0.6622). However, craniofacial brachyfacial morphology influences the presence of painful TMD (P = 0.0077).

Discussion: Although no association existed between craniofacial morphology and TMD, attention should be given to brachyfacial subjects, which are susceptible to having painful TMD.

Keywords: Temporomandibular disorders; Orofacial pain; Craniofacial morphology; Cephalometry.

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  7   INTRODUCTION

Temporomandibular disorders (TMD) are the most common cause of orofacial pain of non dental origin1 and are characterized by pain in the temporomandibular joint and/or masticatory muscles, which can be aggravated by chewing and other mandibular activities.1 Signs and symptoms of TMD occur frequently in the general population2 and may arise from numerous etiological factors.3

The etiology of TMD is generally accepted as multifactorial.3 It has been demonstrated that several factors, such as the presence of parafunctional habits,4,5 traumas,6 and emotional/psychological aspects7,8 influence the development and/or maintenance of TMD signs and symptoms.9 Furthermore, craniofacial morphology has been considered another factor related with TMD.10

Previous studies11-14 have reported association of disc displacement (DD) with/without reduction and specific characteristics of craniofacial morphology. Individuals with DD usually have short ramus height/mandibular body length and a backward rotation of the ramus and mandible.11,14 Furthermore, it was found that TMJ disc displacement was positively associated with mandibular asymmetry.12,13 On the other hand, craniofacial features such as angulation of the Frankfurt/occlusal plane and interpupillary axis were not related to TMD.15 However, the methods used to diagnose TMD in some of those studies11,14,15 were based only on clinical observations, such as: the presence of TMJ sounds, tenderness or pain on temporomandibular joint or masticatory muscles, palpation, and limited mandibular movement, rather than a standardized method of TMD evaluation.

Beyond the different methods used to assess TMD,11,14,15 there are no studies focusing on the relationship between vertical craniofacial morphology (i.e., brachyfacial, mesofacial, and dolichofacial patterns) and TMD, highlighting the importance of the subject. Thus, the aim of this study was to investigate the association between vertical craniofacial morphology and TMD in adults diagnosed by the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD), as well as verify the influence of different craniofacial morphologies on painful TMD.

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Subjects

This cross-sectional study consisted of 200 subjects ranging from 18 to 50 years of age (mean age = 27.34 ± 6.46 years), which were divided into two groups (n = 100 each). The first group was diagnosed with painful or non-painful TMD (experimental) and the second group did not have TMD (control). A sample size test based on previous study16 indicated that 100 volunteers in each group would be enough to detect significant differences with a test power of 80% and an error probability of 5%. Subjects were recruited from patients seeking for dental treatment at the Piracicaba Dental School, University of Campinas, as well as, from students and staff at the same institution. To be included in the experimental group, subjects were required to present with: TMD, diagnosed by RDC/TMD; complete natural dentition (except for missing third molars); and good general and oral health. The control group had to meet the same criteria, except they were not diagnosed with TMD. Subjects were excluded if they presented malocclusions such as anterior open bite, unilateral or bilateral posterior crossbite and deep bite; parafunctional habits (bruxism or tooth grinding); facial deformities (severe facial asymmetry, cleft palate, cleft lip, masseteric hypertrophy); previous maxillofacial surgery; current neurological or psychological disorders treatment; pregnancy; removable partial or complete dentures; and/or intraoral appliances were excluded. From the 296 subjects initially examined, 96 were excluded for the following reasons: having missing teeth (n = 49), malocclusions (n = 9), parafunctional habits (n = 20), orthodontic treatment (n = 2), maxillofacial surgery (n = 1), pregnancy (n = 1), and missing radiography (n = 14). All subjects had a RDC/TMD examination and then they were divided into experimental and control groups. All clinical assessments were performed according to the ethical guidelines of research protocol #022/2012, which was approved by the Ethics Committee of Piracicaba Dental School. All participants signed a written consent form. The study was also entered in the Brazilian Registry of Clinical Trials database (No. RBR-87rdwv).

After selection, all participants underwent to conventional lateral cephalograms followed by cephalometric analysis to determine craniofacial morphology. Participants were also measured and weighed on a mechanical scale (MIC 1/C A, Micheletti, Sao Paulo,

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SP, Brazil) while standing with their feet together and Frankfurt plane parallel to the floor. Body Mass Index (BMI) was calculated as the ratio between weight and height (kg/m2).17

TMD Diagnoses

All participants were submitted to clinical examinations to diagnose TMD using axis I of RDC/TMD. They were evaluated by a single, trained researcher who had been previously calibrated. Calibration consisted of 2 examiners (one of them being an RDC/TMD expert) who applied the RDC/TMD on 12 subjects with TMD signs and symptoms and 8 healthy subjects. The Kappa index was 0.96 (95% confidence interval, 0.89–1.00).

Clinical criteria for diagnosis among patients in the experimental group were as follows: RDC Group I, presenting with myofascial pain with or without limited opening; RDC Group II, disc displacement with or without reduction, with or without limiting opening; and RDC Group III, arthralgia or osteoarthritis or osteoarthrosis. Those who did not present with adequate criteria to be assigned in any of the RDC groups were considered to not have TMD and were included in the control group.

Craniofacial Morphology

Conventional lateral cephalograms were obtained for all subjects to identify craniofacial morphology. Subjects were covered with a lead apron, positioned in the cephalostat with the sagittal plane perpendicular to the x-ray path, the Frankfurt plane parallel to the floor, their teeth in the maximum intercuspal occlusion, and lips lightly together.18 All cephalograms were obtained following a standardized protocol using the same cephalometric unit (Kodak 8000C, Eastman Kodak Company, France). The cephalometric analyses were performed by a single investigator who was blinded to the RDC/TMD diagnoses. Images were analyzed with Radiocef Studio 2.0 software (Radiomemory, Belo Horizonte, MG, Brazil).

Craniofacial morphology was determined by the VERT index19, which is the arithmetic mean of the difference between five cephalometric measures (facial axis, anterior lower facial height, mandibular plan, mandibular arch and facial depth) divided by

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the standard deviation.19 The craniofacial morphology of each subject was classified as: dolichofacial (below -0.5), mesofacial (between -0.49 and +0.49), and brachyfacial (above +0.5)

Statistical analyses

Data were analyzed by Tukey-Kramer and Likelihood Ratio Chi-Square tests. All statistical results were considered significant when P values were <0.05. All statistical analyses were performed by SAS software (Release 9.3. SAS Institute Inc., Cary, NC).

RESULTS

The summary of the anthropometric characteristics of TMD individuals (with and without pain) and control subjects without TMD are shown in Table 1. A homogeneous distribution was observed between groups (P > 0.05). There were significant differences for age (P = 0.027) and body mass index (BMI) (P = 0.043) between groups.

Table 1. Anthropometric characteristics of subjects (mean ± standard deviation).

With TMD

(painful and non-painful) Without TMD P values

Female 90 90 -

Male 10 10 -

Age (years) 27.80 ± 6.10 25.90 ±5.20 0.027

BMI (kg/m2) 23.70 ±3.60 22.71 ±2.70 0.043

Tukey-Kramer test (P < 0.05).

Data distribution from the axis I evaluations of the RDC/TMD are presented in Table 2. Muscle disorders were present in 87 of 100 (87%) subjects. Concerning articular disorders, 37 of 100 patients (37%) had RDC Group II (disc displacements) diagnoses and 62 had RDC Group III (arthralgia/arthritis/arthrosis) diagnoses.

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Table 2. Distribution of RDC/TMD axis I diagnoses.

RDC Group Number of subjects

I) Muscle disorders

a) Myofascial pain 71

b) Myofascial pain with limited opening 16

II) Disc displacements

a) Disc displacement with reduction 36

b) Disc displacement without reduction, with limited opening 0 c) Disc displacement without reduction, without limited opening 1

III) Arthralgia, arthritis, arthrosis

a) Arthralgia 61

b) Osteoarthritis of the temporomandibular joint 1 c) Osteoarthrosis of the temporomandibular joint 0

Figure 1 shows the frequency of single and multiple RDC/TMD diagnoses. Regarding single diagnoses, group I findings (muscle disorders) were observed in 25% of the patients, group II findings (disc displacements) were observed in 8%, and group III findings (arthralgia/arthritis/arthrosis) were observed in 3%. Multiple group diagnoses were assigned to 64% of the patients.

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Figure 1 – Distribution of single and multiple RDC axis I diagnoses.

The number and frequency distribution of subjects with different craniofacial patterns of both groups (control and experimental) are described in Table 3. There was a difference (P = 0.0207) in the frequency distribution between brachy- and dolichofacial subjects in the control group (without TMD), with brachyfacial subjects being in greater proportion. On the other hand, no such difference (P = 0.1738) was found in the experimental group (with TMD). Furthermore, no association between craniofacial morphology and TMD was found (P = 0.6622).

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Table 3. Comparison of the frequency distribution and the association between different craniofacial morphologies and TMD.

Groups Craniofacial morphology P value

Brachyfacial Dolichofacial Mesofacial

Without TMD (n = 100) 46 (53.49%)a 24 (48.98%)b 30 (46.15%)a,b 0.0207 With TMD (n = 100) 40 (46.51%)a 25 (51.02%)a 35 (53.85%)a 0.1738

Likelihood Chi-square test (P = 0.6622). Distinct letters indicate intragroup (with and without TMD) differences.

Evaluating the entire group with TMD (100 subjects), pain was observed in 92 individuals (Table 4). Differences were found between brachyfacial, dolichofacial, and mesofacial craniofacial patterns in that group (P = 0.0077). Moreover, TMD subjects without pain had no differences in craniofacial morphology.

Table 4. Association between craniofacial morphology and TMD with and without pain.

Craniofacial Morphology

TMD Group (n = 100)

With pain Without pain

Brachyfacial 40 (100%)a 0 (0%)a

Dolichofacial 23 (92%)b 2 (8%)a

Mesofacial 29 (82.86%)c 6 (17.14%)a

Likelihood Chi-square test (P = 0.0077). Distinct letters indicate intragroup (with and without painful TMD) differences.

DISCUSSION

This study demonstrated that TMD, diagnosed by RDC/TMD was not associated with vertical craniofacial morphology. Regarding demographic data, differences between groups were observed for age and BMI. Since the ages of participants ranged from

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18 to 50 years old, and the BMI values of both groups fell into the normal weight category,17 it can be suggested that these differences did not interfere with the results.

Concerning the RDC axis I diagnoses, only 36 of the 100 TMD subjects had a single TMD diagnosis, while the remaining 64 subjects had multiple diagnoses. This finding is similar to previous studies that showed that a combination of muscular and articular disorders frequently occur.20,21 As TMD subjects usually have multiple diagnoses,20 this study focused on the presence of TMD to group the subjects in the experimental group, rather than further dividing them according to their RDC diagnoses.

In spite of the experimental group having a higher frequency of patients with brachyfacial morphologies, no significant difference in the frequency of craniofacial morphologies was observed. In contrast, subjects in control group did have differences between brachyfacial and dolichofacial craniofacial morphologies. Although there was a higher proportion of brachyfacial subjects without TMD, there was no association between craniofacial morphology and the presence of TMD (independent of pain). This finding disagrees from other studies10,11 and could be related to different cephalometric variables evaluated in the previous. Those studies assessed cephalometric variables individually and did not determine the vertical craniofacial morphologies in their subjects. In addition, most of the studies11,14,15 that found associations between cephalometric variables and TMD, evaluated TMD characteristics anamnestically by palpation/auscultation15 or by radiographic/magnetic resonance imaging.11 The current study, on the other hand, used the RDC/TMD Axis I diagnostic protocol, which is the most frequently used, validated, and accepted instrument for clinical research.22

The data also showed that all brachyfacial subjects in the experimental group presented painful TMD. These data can probably be explained by differences in the fiber-type composition of their masticatory muscles.23,24 There is a higher proportion of type-II fibers in the masseter of short-faced/brachyfacial subjects,25 and these fibers are characterized by rapid contraction and lower resistance to fatigue.26 Thus, as type-II fibers are less resistant to fatigue, which is often associated with the onset of muscle pain,27 it might explain the presence of pain in all brachyfacial subjects with TMD.

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diagnosis, it was not possible to evaluate the association between craniofacial morphology and the specific RDC diagnoses. Therefore, this could be a limitation of this study and additional studies, with larger sample sizes are needed to elucidate these specific associations.

It is important to emphasize that the results of this study contribute to clinical practice and demonstrate the importance of assessing craniofacial morphology when making treatment decisions in adults with TMD, in particular patients with brachyfacial morphologies, who are more susceptible to TMD-associated pain.

CONCLUSION

Within its limitations, this study showed no association between vertical craniofacial morphology and TMD. However, patients with brachyfacial pattern appear to be predisposed to painful TMD.

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  16   REFERENCES

1. de Leeuw R, Klasser G, editors. Orofacial pain: guidelines for assessment, diagnosis, and management. 5th ed. Quintessence Publishing Company; 2013. 2. Manfredini D, Guarda-Nardini L, Winocur E, Piccotti F, Ahlberg J, Lobbezoo F.

Research diagnostic criteria for temporomandibular disorders: a systematic review of axis I epidemiologic findings. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112(4):453-62.

3. Suvinen TI, Reade PC, Kemppainen P, Kononen M, Dworkin SF. Review of aetiological concepts of temporomandibular pain disorders: towards a biopsychosocial model for integration of physical disorder factors with psychological and psychosocial illness impact factors. Eur J Pain. 2005;9(6):613-33.

4. Blanco Aguilera A, Gonzalez Lopes L, Blanco Aguilera E, De la Hoz Aizpura JL, Rodriguez Torronteras A, Segura Saint-Gerons R, et al. Relationship between self-reported sleep bruxism and pain in patients with temporomandibular disorders. J Oral Rehabil. 2014;41(8):564-72.

5. Fernandes G, van Selms MK, Gonçalves DA, Lobbezoo F, Camparis CM. Factors associated with temporomandibular disorders pain in adolescents. J Oral Rehabil. 2015;42(2):113-9.

6. Häggman-Henrikson B, Rezvani M, List T. Prevalence of whiplash trauma in TMD patients: a systematic review. J Oral Rehabil. 2014;41(1):59-68.

7. Manfredini D, Winocur E, Ahlberg J, Guarda-Nardini L, Lobbezoo F. Psychosocial impairment in temporomandibular disorders patients. RDC/TMD axis II findings from a multicenter study. J Dent. 2010;38(10):765-72.

8. Reissman DR, John MT, Seedorf H, Doering S, Schierz O. Temporomandibular disorder pain is related to the general disposition to be anxious. J Oral Facial Pain Headache. 2014;28(4):322-30.

9. Gremillion HA. The relationship between occlusion and TMD: an evidence-based discussion. J Evid Based Dent Pract. 2006;6(1)43-7.

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analysis of mandibular morphology: discrimination among subjects with and without temporomandibular joint disk displacement and osteoarthrosis. J Oral Rehabil. 2012;39(2):93-9.

11. Yang IH, Moon BS, Lee SP, Ahn SJ. Skeletal differences in patients with temporomandibular joint disc displacement according to sagittal jaw relationship. J Oral Maxillofac Surg. 2012;70(5):349-60

12. Sakar O, Calişir F, Marşan G, Oztaş E. Evaluation of the effects of temporomandibular joint disc displacement and its progression on dentocraniofacial morphology in symptomatic patients using posteroanterior cephalometric analysis. Cranio. 2013;31(1):23-31.

13. Almăşan OC, Băciuţ M, Hedeşiu M, Bran S, Almăşan H, Băciuţ G. Posteroanterior cephalometric changes in subjects with temporomandibular joint disorders. Dentomaxillofac Radiol. 2013;42(1):20120039,8p. doi:10.1259/dmfr.20120039. 14. Kwon HB, Kim H, Jung WS, Kim TW, Ahn SJ. Gender differences in dentofacial

characteristics of adult patients with temporomandibular disc displacement. J Oral Maxillofac Surg. 2013;71(7):1178-86.

15. Ciancaglini R, Colombo-Bolla G, Gherlone EF, Radaelli G. Orientation of craniofacial planes and temporomandibular disorder in young adults with normal occlusion. J Oral Rehabil. 2003;30(9):878-86.

16. Sonnesen L, Bakke M, Solow B. Temporomandibular disorders in relation to craniofacial dimensions, head posture and bite force in children selected for orthodontic treatment. Eur J Orthod. 2001;23(2):179-92.

17. World Health Organization (WHO). Obesity: Preventing and managing the global epidemic. Report of a WHO consultation. World Health Organization Technical Report Series. 2000.

18. Bósio JA, Burch JG, Tallents RH, Wade DB, Beck FM. Lateral cephalometric analysis of asymptomatic volunteers and symptomatic patients with and without bilateral temporomandibular joint disk displacement. Am J Orthod Dentofacial Orthop. 1998;114(3):248-55.

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  18   fifty years. Angle Orthod. 1981;51(2):115-50.

20. Manfredini D, Piccotti F, Ferronato G, Guarda-Nardini L. Age peaks of different RDC/TMD diagnoses in a patient population. J Dent. 2010;38(5):392-9.

21. Wieckiewicz M, Grychowska N, Wojciechowski K, Pelc A, Augustyniak M, Sleboda A, Zietek M. Prevalence and correlation between TMD based on RDC/TMD diagnoses, oral parafunctions and psychoemotional stress in Polish university students. Biomed Res Int. 2014; 2014:472346,7p. doi:10.1155/2014/472346. Epub 2014 Jul 9.

22. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. J Craniomandib Disord. 1992;6(4):301-55.

23. Tuxen A, Bakke M, Pinholt EM. Comparative data from young men and women on masseter muscle fibres, function and facial morphology. Arch Oral Biol. 1999;44(6):509-18.

24. Rowlerson A, Raoul G, Daniel Y, Close J, Maurage CA, Ferri J, et al. Fiber type differences in masseter muscle associated with different facial morphologies. Am J Orthod Dentofac Orthop. 2005;127(1):37-46.

25. Farella M, Bakke M, Michelotti A, Rapuano A, Martina R. Masseter thickness, endurance and exercise-induced pain in subjects with different vertical craniofacial morphology. Eur J Oral Sci. 2003;111(3):183-8.

26. Korfage JA, Koolstra JH, Langenbach GE, van Eijden TM. Fiber-type composition of the human jaw muscles (Part 2). Role of hybrid fibers and factors responsible for inter-individual variation. J Den Res. 2005;84(9):784-793.

27. Maton B, Rendell J, Gentil M, Gay T. Masticatory muscle fatigue: endurance times and spectral changes in the electromyogram during the production of sustained bite forces. Arch Oral Biol. 1992;37(7): 521–9.

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Craniofacial morphology affects maximum bite force in patients with painful temporomandibular disorders

This manuscript was submitted to The Journal of International Prosthodontics.

Paula Furlan Bavia, DDSa

Renata Cunha Matheus Rodrigues Garcia, PhDb

aGraduate student

Department of Prosthodontics and Periodontology

Piracicaba Dental School, University of Campinas Piracicaba Avenida Limeira, 901; Piracicaba, São Paulo, Brazil – 13414-903

bProfessor

Department of Prosthodontics and Periodontology Piracicaba Dental School, University of Campinas

Avenida Limeira, 901; Piracicaba, São Paulo, Brazil – 13414-903

Corresponding author:

Renata Cunha Matheus Rodrigues Garcia

Department of Prosthodontics and Periodontology Piracicaba Dental School, University of Campinas

Av. Limeira, nº 901, Bairro Areião, Piracicaba, SP, Brazil, 13414-903 Phone Number: + 55 19 2106-5240, Fax number: + 55 19 2106-5211 e-mail: regarcia@fop.unicamp.br

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  20   Abstract

Aims: This study evaluated whether different craniofacial morphologies could affect masticatory parameters in subjects with painful temporomandibular disorders (TMDs). Methods: Forty-eight female subjects, 18–45 years (mean ± standard deviation [SD], 27.71 ± 5.79 years), with painful TMDs were submitted to conventional lateral cephalometric radiography and by Ricketts' cephalometric analysis and were assigned to 1 of 3 groups: (1) brachyfacial (n = 22), (2) mesofacial (n = 13), or (3) dolichofacial (n = 13). The Research Diagnostic Criteria for TMD (RDC/TMD) was used to diagnose TMD, and pain intensity was measured by using a visual analog scale (VAS). Maximum bite force (MBF) was measured by sensors placed bilaterally in the first molar region and connected to amplifying equipment. Masticatory performance was assessed by chewing an artificial test material (Optosil) and using the sieve method. Chewing ability was evaluated by a VAS questionnaire containing 7 types of food. Data were analyzed using one-way analysis of variance (ANOVA) followed by Tukey-Kramer test, with P < 0.05 considered statistically significant. Results: A difference (P = 0.0001) in maximum bite force values was detected among the 3 groups, with the highest values observed among the brachyfacial individuals. By contrast, there was no difference (P = 0.4543) in masticatory performance among the different craniofacial morphologies. These groups differed (P = 0.0141) in their ability to chew only 1 of the 7 evaluated food types. Conclusion: Craniofacial morphology affected the MBF without impairing masticatory performance and chewing ability in subjects with painful TMDs.

Keywords: Temporomandibular disorders, craniofacial morphology, pain measurement, bite force, mastication

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  21   Introduction

Mastication is one of the orofacial motor functions1 and is the first step in which food is broken down into smaller particles to facilitate the process of enzymatic digestion.2 During mastication, the tongue, facial, and jaw muscles act simultaneously to put the food between the teeth, cut it up, and prepare it for swallowing.3 This physiological function of the stomatognathic system is coordinated by the central nervous system4 and may be modified by several factors, such as dental occlusion, the neuromuscular system, periodontal mechanoreceptors, and pain.3,5 Thus, functional alterations of the stomatognathic system might result in poor masticatory function, which can lead to poor nutrition and ultimately poor health.6-8

Bite force (BF) is an important component in masticatory function assessment and is responsible for the process of comminuting food and triturating it in preparation for swallowing.9 Several factors, such as the number of occlusal pairs,10 masticatory muscle thickness,10 and malocclusion,11 can negatively influence BF and consequently may impair masticatory function. It has also been demonstrated that BF can be affected by craniofacial morphology, once dolichofacial patients have presented lower BF values.12-14 Temporomandibular disorders (TMDs), such as disc displacement with reduction15 and temporomandibular joint (TMJ) or muscle pain12,13,16,17 can also decrease the BF, suggesting poorer masticatory function in such subjects. Masticatory function can also be assessed by masticatory performance and chewing ability tests.18,19 The former measures the particle size of chewable test materials after a given number of chewing strokes,18,19 and the latter involves the subjects’ self-perception in the evaluation of their masticatory function.19 It was verified that masticatory performance and chewing ability, as well as BF, are reduced in subjects with TMD symptoms.2,20,21 This reduction can be related to pain during chewing in TMD patients,22,23 who usually perform slower and smaller movements in an attempt to avoid aggravating the injury24 and consequently swallow larger food particles.7 Myofascial pain may impair masticatory function due to limited jaw movements,25 and the awareness of muscle pain may also hamper proper mastication.26

However, to our knowledge, the effect of craniofacial morphology on masticatory performance and chewing ability in subjects with painful TMDs has not been

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examined and therefore warrants investigation. Considering the possibilities that TMDs might damage masticatory function,27 and different craniofacial morphologies may affect the BF,12-14 it was hypothesized that craniofacial morphology could further affect mastication in subjects with painful TMDs. Thus, the aim of this study was to investigate whether different craniofacial morphologies could have an effect on maximum bite force (MBF), masticatory performance and chewing ability in subjects with painful TMDs.

Materials and methods

Subjects

A total of 48 female subjects with painful TMDs, aged 18–45 years (mean age 27.71 ± 5.79 years), participated in this study. They were selected from a cohort of patients who sought care for facial pain and from students and staff of Piracicaba Dental School, University of Campinas, Brazil. All participants underwent to conventional lateral cephalograms followed by Ricketts' cephalometric analysis to determine the craniofacial morphology. Based on the results of this analysis, the subjects were divided into 3 groups: (1) brachyfacial (n = 22), (2) mesofacial (n = 13), and (3) dolichofacial (n = 13). The inclusion criteria were: presence of a painful TMD for at least 3 months, complete dentition, and good oral and general health. Individuals presenting severe malocclusion (e.g., anterior open bite, deep bite, unilateral or bilateral posterior crossbite), previous maxillofacial surgery, current neurological or psychological disorders treatment, parafunctional habits, facial deformities, pregnancy, removable partial or complete dentures and/or intraoral appliances, and those receiving TMD treatment or drug therapies were excluded from the study. All subjects signed the consent form approved by the Ethics Committee of Piracicaba Dental School, University of Campinas (protocol # 022/2012), and the study has been registered in the Brazilian Registry of Clinical Trials database (No. RBR-87rdwv).

Masticatory function was objectively assessed by MBF measurements and masticatory performance evaluations, and a subjective test of chewing ability was administered. During all measurements, the researcher was blinded to each participant’s

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assigned craniofacial morphology classification. All participants also received an anthropometric evaluation. Body height was measured in meters (m) with the subject in the erect position, and weight was recorded in kilograms (kg) using a mechanical scale (MIC 1/C A, Micheletti, Sao Paulo, SP, Brazil). Body mass index (BMI) was calculated as kg/m2.28

Craniofacial morphology

Lateral cephalograms were used for craniofacial morphology determination. During each radiographic procedure, a protective lead apron was placed over the subject. After being positioned in the cephalostat, the subject’s teeth were held in the maximal intercuspal position and the lips lightly held together, with the sagittal plane perpendicular to the path of the x-rays and the Frankfurt (horizontal) plane parallel to the floor.29 All cephalograms were obtained with the same radiographic unit (Kodak 8000C, Eastman Kodak Company, France), using standard procedures. A single investigator performed all cephalometric analyses in the Radiocef Studio 2.0 software package (Radiomemory, Belo Horizonte, MG, Brazil).

The vertical facial pattern was determined by calculating the VERT index (VI),30 using the following five mandibular measurements: facial axis, anterior lower facial height, mandibular plan, mandibular arch, and facial depth. VI is the arithmetic mean of the difference between each of these five cephalometric measures and the respective value considered ideal for a harmonic face divided by the standard deviation.30 Each subject was classified as dolichofacial (VI below −0.5), mesofacial (VI between −0.49 and +0.49), and brachyfacial (VI above +0.5).30 The VI is negative when the growth trend is vertical and is positive when the growth trend is horizontal.

TMD diagnosis

All participants were submitted to clinical examination for diagnosis of TMD by the Research Diagnostic Criteria for TMD (RDC/TMD) Axis I protocol. A single researcher previously trained and calibrated to perform the RDC/TMD examination evaluated all the subjects. Two examiners participated in the calibration process, one of

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them being an expert RDC/TMD examiner. The kappa index obtained was 0.96 (95% confidence interval, 0.89–1.00).

Subjects presenting with myofascial pain, with or without limited opening (RDC Group I); with a concomitant diagnosis of disc displacement with or without reduction, with or without limited opening (RDC Group II); or with concomitant arthralgia, osteoarthritis, or osteoarthrosis (RDC Group III) were included in the study. For TMD diagnosis, each subject had to be presenting with pain in the masticatory muscles and/or in the TMJ for at least 3 months. The pain intensity was assessed by using a visual analog scale (VAS). The VAS used was a 100 mm long horizontal line, anchored by word descriptors at each end, where the left side read “no pain” and the right side read “worst pain imaginable”.31,32 Each subject drew a vertical mark on the line at the point that best represented the level of their perceived pain. Only subjects presenting a pain intensity of 50 mm or more in the VAS in the moment of the tests were included in this study.

MBF measurement

The MBF was measured twice with a BF transducer (Spider 8, Hottinger Baldwin Messtechnik GmbH, Darmstadt, Germany).33 The BF sensors (FSR no. 151, 1.2 mm diameter, 0.25 mm thickness; Interlink Electronics Inc., Camarillo, CA, USA) were protected from deformities on both sides during clenching with 1.0 mm thick metal disks of the same diameter and 1.7 mm wide rubber disks, resulting in a 5.65 mm wide assembly. The sensors were protected from humidity with a plastic film positioned in the bilateral first molar regions. During the procedure, the applied force was amplified, recorded, and analyzed with Catman Easy software (ver. 1.0, Hottinger Baldwin Messtechnik GmbH). Subjects were instructed to occlude with maximum force for 7 s, and after 5 min the procedure was repeated. The average of the two measurements was used as the MBF value expressed as kilogram-force (kgf).

Masticatory performance

Masticatory performance was evaluated using the sieve method. Subjects were requested to chew a portion of 17 cubes of an artificial silicon test material (Optosil; Heraus

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Kulzer, Sao Paulo, SP, Brazil)34 in their habitual way for 20 chewing strokes, counted by a single researcher.35 Thereafter, the chewed particles were collected, dried, and shaked at 2 Hz for 20 min in a sieving machine (Bertel, Caieiras, SP, Brazil), in which the particles passed through a 10-sieve stack with mesh sizes gradually decreasing from 5.6 to 0.5 mm just above the bottom plate of the stack.34 Particles retained in each sieve were weighed on an analytical balance accurate to 0.001 g (Model 2060, Bel Engineering, Monza, Italy), and the X50 value was calculated using the Rosin-Rammler equation.36 The X50 value represents the masticatory performance and corresponds to the aperture of a theoretical sieve through which 50% of the weight of comminuted food can pass.34,36 Thus, the lower the X50 value, the better masticatory performance.

Chewing ability

Chewing ability was measured with a subjective questionnaire evaluation. On this questionnaire, the chewing ability was represented as a VAS ranging from “very easy” to “very difficult”. Subjects were requested to think about their ability to chew 7 types of food with different textures and consistencies, including bread, parmesan cheese, sausage, lettuce, peanut, apple, and raw carrot. The subjects then drew a vertical mark on the line at the point that best represented their ability to chew those foods. Lower scores represent greater chewing ability.19

Statistical analyses

Continuous data are expressed as the mean ± standard deviation (SD). The normality of data distribution was assessed by the parameters of skewness and kurtosis and by Shapiro-Wilk tests. One-way analysis of variance (ANOVA) and Tukey-Kramer tests were used for analysis of pain intensity, MBF, masticatory performance, and chewing ability. All statistical analyses were performed in the SAS software package (version 9.3, SAS Institute Inc., Cary, NC, USA). A P value < 0.05 was considered statistically significant.

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  26   Results

The anthropometric characteristics of the sample are described in Table 1. Homogeneous distribution was observed among the 3 groups (P > 0.05). There was no statistical difference in age (P = 0.3360) or BMI (P = 0.7538) among the groups.

Table 1 Mean (standard deviation) of the sample characteristics. Brachyfacial Mesofacial Dolichofacial

P

(n = 22) (n = 13) (n = 13)

Age (years) 27.73 (±5.46) 26.00 (±5.61) 29.38 (±6.42) .3360 BMI (kg/m2) 24.04 (±4.04) 24.20 (±2.90) 24.93 (±3.78) .7538 One-way analysis of variance (ANOVA), (P < 0.05).

MBF values were different (P = 0.0001) among the brachyfacial, mesofacial, and dolichofacial subjects, with the highest values observed in the brachyfacial group. No difference in masticatory performance (P = 0.4543) or pain intensity values (P = 0.6720) was observed (Table 2).

Table 2 Mean (standard deviation) of pain intensity (mm), maximum bite force (Kgf) and masticatory performance (X50) for the studied groups.

Groups Brachyfacial Mesofacial Dolichofacial P

VAS (mm) 71.54 (±14.46) a 66.00 (±18.11) a 69.30 (±14.78) a .6720 MBF (KgF) 45.01 (±10.38) a 33.40 (±7.12) b 29.23 (±7.11) b .0001 MP (x50) 4.95 (±0.73) a 5.19 (±0.44) a 5.11 (0.34) a .4543 Distinct letters show significant differences among groups. One-way analysis of variance (ANOVA), Tukey-Kramer tests (P < 0.05).

These groups reported different chewing ability values (P = 0.0141), but only for 1 (sausage) of the 7 tested foods (Table 3). The brachyfacial and dolichofacial subjects

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reported the greatest and least ability, respectively to chew sausage.

Table 3 Mean (standard deviation) of chewing ability for the studied groups. Groups

Food type Brachyfacial Mesofacial Dolichofacial P

(n = 22) (n = 13) (n = 13) Bread 27.86 (±24.69) a 43.38 (±24.17) a 35.46 (±21.10) a .1789 Parmesan cheese 37.50 (±24.49) a 44.38 (±25.57) a 47.84 (18.45) a .0964 Sausage 8.95 (±7.52) a 17.23 (±13.45) b 21.30 (±15.62) c .0141 Lettuce 7.77 (±7.97) a 13.92 (±12.77) a 20.38 (±25.88) a .1874 Peanut 53.50 (±29.60) a 58.76 (±23.53) a 52.38 (±27.32) a .8120 Apple 52.31 (±27.62) a 63.07 (±26.57) a 56.92 (±23.66) a .5096 Carrot 48.27 (±28.88) a 50.30 (±33.35) a 53.15 (±31.69) a .8874 Distinct letters show significant differences among groups. One-way analysis of variance (ANOVA), Tukey-Kramer tests (P < 0.05).

Discussion

The results of this study revealed that craniofacial morphology can have an effect on MBF values but does not affect masticatory performance in females with painful TMDs. Among craniofacial morphologies studied, the self-perceived ability to chew was different only for sausage, indicating that facial pattern probably did not impair their ability to chew different types of food. MBF results are in agreement with those reported by Custodio et al.14 and Serrao et al.,37 who observed higher BF and muscular activity levels during maximum clenching in subjects with shorter vertical craniofacial morphology. The higher reflex tonus present in the masseter of short-face subjects38 may explain the higher

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  28  

BF values in those individuals, who are able to bite stronger especially during jaw closure.38 On the other hand, the MBF values obtained from our brachyfacial and mesofacial subjects were lower compared to those found by Custodio et al.14 (53.48 ± 15.60 and 39.73 ± 16.60 kgf, respectively). These differences are probably due to the presence of TMD pain, which might decrease the capacity of masticatory muscles to produce maximum effort,13,16 resulting in lower BF. Furthermore, the chronic pain might produce jaw reflexes,39 which are influenced by nociceptive activity from the TMJ region40 in an attempt to protect the temporomandibular structures and jaw muscles from damage during forceful biting or mastication.39

Considering the MBF values obtained in this study, it was expected that masticatory performance would also be affected by different craniofacial morphologies. However, the hypothesis was not confirmed. It is well known that masticatory performance can be affected by the occlusal profile,11,41 as well as by the number of occlusal contacts,2,42 which have been suggested to be of major importance in masticatory performance.10,43 Thus, given that all subjects in this study presented with complete dentition and no malocclusion, these factors could have contributed to our study outcomes. Similar to the current findings, Pereira et al.17 and Vilanova et al.44 also found no significant differences in masticatory performance in subjects with symptomatic TMDs, suggesting that the presence of pain does not damage the mastication capacity.45

In the chewing ability evaluation, the dolichofacial subjects reported the least ability to chew only sausage, which is softer than peanuts and raw carrots. This was an unexpected finding, since TMD patients, irrespective of their craniofacial morphology, usually complain of difficulty to chew46 particularly hard foods.47 A possible explanation could be related to the subjective nature of this test, in which the 7 study foods were chosen from a list of foods ranked in order of masticatory difficulty by patients with full dentures19. Because our sample comprised of dentate subjects, they might have had different dietary habits,49 which could help explain this finding. It is important to mention that other factors, such as socioeconomic status and the type of evaluated food, which the subjects might not be used to eating, may have contributed to the results. In addition, given the subjective nature of this chewing ability test, the outcomes obtained might have

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