ALTERAÇÕES DOS SEIOS MAXILARES EM TOMOGRAFIAS COMPUTADORIZADAS SOLICITADAS PARA PLANEJAMENTO DE IMPLANTES DENTÁRIOS JULIANA PELINSARI LANA

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1 Pontifícia Universidade Católica de Minas Gerais Departamento de Odontologia ALTERAÇÕES DOS SEIOS MAXILARES EM TOMOGRAFIAS COMPUTADORIZADAS SOLICITADAS PARA PLANEJAMENTO DE IMPLANTES DENTÁRIOS JULIANA PELINSARI LANA Belo Horizonte 2010

2 Juliana Pelinsari Lana ALTERAÇÕES DOS SEIOS MAXILARES EM TOMOGRAFIAS COMPUTADORIZADAS SOLICITADAS PARA PLANEJAMENTO DE IMPLANTES DENTÁRIOS Dissertação apresentada ao Programa de Mestrado em Odontologia da Pontifícia Universidade Católica de Minas Gerais, como requisito parcial para obtenção do título de Mestre em Odontologia. Área de concentração: Clínicas Odontológicas. Ênfase: Radiologia Odontológica e Imaginologia. Orientador: Prof. Dr. Martinho Campolina Rebello Horta Belo Horizonte 2010

3 FICHA CATALOGRÁFICA Elaborada pela Biblioteca da Pontifícia Universidade Católica de Minas Gerais L243a Lana, Juliana Pelinsari Alterações dos seios maxilares em tomografias computadorizadas solicitadas para planejamento de implantes dentários / Juliana Pelinsari Lana. Belo Horizonte, f. : il. Orientador: Martinho Campolina Rebello Horta Dissertação (Mestrado) Pontifícia Universidade Católica de Minas Gerais. Programa de Pós-Graduação em Odontologia. 1. Implantes dentários. 2. Seio do maxilar. 3. Tomografia computadorizada. I. Horta, Martinho Campolina Rebello. II. Pontifícia Universidade Católica de Minas Gerais. Programa de Pós-Graduação em Odontologia. III. Título. CDU:

4 FOLHA DE APROVAÇÃO

5 RESUMO O desenvolvimento dos implantes dentários ao longo dos últimos anos desencadeou um aumento na demanda por serviços de radiologia oral e maxilofacial. A tomografia computadorizada de feixes cônicos (TCFC) é atualmente um dos métodos de imagem mais utilizado para planejamento de implantes dentários. Os seios maxilares são estruturas anatômicas de grande importância na prática odontológica, sendo essencial o reconhecimento de suas variações anatômicas e processos patológicos em exames de imagem. O objetivo do presente estudo foi avaliar a presença de variações anatômicas e processos patológicos nos seios maxilares em tomografias computadorizadas de feixes cônicos da maxila, solicitadas para planejamento de implantes dentários. O estudo, do tipo transversal de prevalência, utilizou uma amostra de conveniência de 500 exames de TCFC da maxila solicitados para planejamento de implantes dentários. Os exames de TCFC foram analisados independentemente por dois cirurgiões-dentistas radiologistas, que avaliaram a presença de variações anatômicas e processos patológicos nos seios maxilares. As variações anatômicas observadas foram: pneumatização (83.2%), desvio de septo nasal (53.2%), septo intra-sinusal (44.4%), óstio secundário/acessório (13.4%), hipoplasia (4.8%), exostose (2.6%), seio etmomaxilar (1.2%) e células de Haller (0.6%). Os processos patológicos identificados foram: espessamento do revestimento mucoso (<3mm em 62.6% e >3mm em 54.8%), lesões polipóides (21.4%), descontinuidade óssea do assoalho do seio maxilar (17.4%), nível hidroaéreo (4.4%), espessamento ósseo da parede do seio maxilar (3.8%), antrólito (3.2%), descontinuidade óssea da parede lateral do seio maxilar (2.6%), opacificação/velamento (1.8%) e corpo estranho (1.6%). O reconhecimento das variações anatômicas e dos processos patológicos dos seios maxilares é de grande importância na prática odontológica, principalmente na implantodontia. Além de modificar o planejamento de implantes dentários, algumas dessas condições exigem tratamento especializado. Palavras-chave: Seios maxilares. Tomografia computadorizada de feixes cônicos. Implantes dentários.

6 ABSTRACT The growing development of dental implants has triggered an increasing demand for oral and maxillofacial radiology services. Cone-beam computed tomography is currently the most used image exam for dental implant planning. The maxillary sinuses are anatomical structures of great importance in dental practice and the recognition of its anatomic variations and lesions in image exams is essential. The aim of this study was to evaluate the presence of anatomic variations and lesions of the maxillary sinus in cone-beam computed tomography (CBCT) of the maxilla required for dental implant planning. This transversal prevalence study evaluated a convenient sample of 500 CBCT exams. The inclusion criteria were CBCT exams of the maxilla required for dental implant planning. The exams were performed by the i- CAT cone-beam computed tomograph. Image analysis was performed on the i-cat software. The CBCT exams were independently evaluated by two oral and maxillofacial radiologists who assessed the presence of anatomic variations and lesions of the maxillary sinus. Doubtful cases were reanalyzed and a consensus agreed. The anatomic variations detected were pneumatization (83.2%), nasal septum deviation (53.2%), antral septa (44.4%), secondary ostium (13.4%), hypoplasia (4.8%), exostosis (2.6%), ethmomaxillary sinus (1.2%), and Haller cells (0.6%). The identified lesions were mucosal thickening (<3mm in 62.6% and >3mm in 54.8%), polypoid lesions (21.4%), discontinuity of the sinus floor (17.4%), air-fluid level (4.4%), bone thickening of the maxillary sinus wall (3.8%), antroliths (3.2%), discontinuity of the sinus lateral wall (2.6%), sinus opacification (1.8%), and foreign body (1.6%). The recognition of anatomic variations and lesions of the maxillary sinuses is noteworthy in dental practice and especially in implantology. In addition to modify dental implant planning, some of these conditions require specialized treatment. Key words: Maxillary sinus. Cone beam computed tomography. Dental implants.

7 LISTA DE ARTIGOS Esta dissertação gerou as seguintes propostas de artigos: 1. Anatomic variations and lesions of the maxillary sinus detected in cone beam computed tomography for dental implants...19 (A ser submetido ao periódico Clinical Oral Implants Research Qualis A2) 2. Bone discontinuity of the maxillary sinus floor: A series of cases detected by cone beam computed tomography for dental implant planning...43 (A ser submetido ao periódico Quintessence International Qualis B1)

8 SUMÁRIO INTRODUÇÃO... Tomografia computadorizada de feixes cônicos e sua importância para a implantodontia... Variações anatômicas e processos patológicos dos seios maxilares CONSIDERAÇÕES GERAIS OBJETIVOS... Objetivo Geral... Objetivos Específicos REFERÊNCIAS GERAIS APÊNDICE 1 - Artigo I APÊNDICE 2 - Artigo II ANEXO 1 - Carta de aprovação do comitê de ética... 60

9 7 1 INTRODUÇÃO 1.1 Tomografia computadorizada de feixes cônicos e sua importância para a implantodontia Implantes dentários podem permitir a restauração funcional e estética ideal e estão disponíveis há muitos anos, mas nem sempre foram tão convenientes e acessíveis, como neste momento (VAN DER ZEL, 2008). Os Implantes dentários requerem suficiente osso alveolar residual para sua colocação. Como o osso alveolar é reabsorvido em segmentos edêntulos, exames por imagem são necessários para avaliação da altura, largura e qualidade do osso residual (ABRAHAMS, 1993). Além disso, a reabilitação com implantes dentários tem enfrentado demandas nas áreas de prótese e estética devido à necessidade de resultados cada vez mais próximos do ideal, que exigem planejamento e posicionamento cirúrgico preciso (VAN DER ZEL, 2008). Atualmente, existem muitas técnicas radiográficas disponíveis para orientar o clínico no planejamento do tratamento com implante (HANSEN, GRÖNDAHL e EKESTUBBE, 2009). Radiografias intrabucais e radiografias panorâmicas fornecem apenas informações em duas dimensões (HANSEN, GRÖNDAHL e EKESTUBBE, 2009). Soma-se a isto o fato de que radiografias panorâmicas sofrem magnificação imprevisível, não permitindo uma avaliação da largura óssea no sentido vestíbulolingual/palatal (ABRAHAMS, 1993). Dados radiográficos precisos permitem uma cirurgia para inserção de implante mais meticulosa e previsível, e possibilitam ao cirurgião o planejamento correto do tratamento e avaliação do resultado cirúrgico (HANSEN, GRÖNDAHL e EKESTUBBE, 2009). A avaliação da localização do canal mandibular, seios maxilares, cavidade nasal, assim como a angulação da crista alveolar, são prérequisitos para um planejamento adequado em implantodontia (HANSEN, GRÖNDAHL e EKESTUBBE, 2009). Portanto, a técnica de escolha para avaliação pré-operatória para colocação de implantes dentários é a tomografia computadorizada (multislice ou de feixes cônicos) (ABRAHAMS, 1993). Utilizando um sistema de planejamento baseado em tomografia computadorizada, o cirurgião é capaz de selecionar os locais ideais para a colocação do implante (VAN DER ZEL, 2008). A maxila posterior edêntula, por exemplo, geralmente apresenta uma

10 8 quantidade limitada de volume ósseo, devido à atrofia do rebordo alveolar e pneumatização do seio maxilar. Por conseguinte, a colocação de implantes dentários nessa região pode ser complicada. Como estes implantes são normalmente inseridos margiando o assoalho do seio maxilar, esta abordagem tem um risco elevado de inserir o parafuso no interior do seio maxilar (JUNG et al., 2007). Um procedimento de levantamento de seio maxilar, com colocação de enxerto ósseo em posição subperiostial no assoalho do seio, pode ser usado para complementar a altura óssea antes da colocação do implante. Portanto, doenças sinusais e septações antrais inferiores devem ser sempre observados (BOEDDINGHAUS e WHYTE, 2008). A tomografia computadorizada (TC) é um método de diagnóstico por imagem que utiliza a radiação X e permite obter a reprodução de uma secção do corpo humano em quaisquer uns dos três planos do espaço (GARIB et al., 2007). É considerada uma importante ferramenta para a visualização tridimensional das estruturas anatômicas e de processos patológicos (BUENO et al., 2007). A tomografia computadorizada de feixes cônicos (TCFC) utiliza um feixe de Raios X, em forma de cone, para aquisição de dados através de um detector de projeção plana, durante uma única rotação de 360 o, da qual um conjunto de dados volumétricos é reconstruído utilizando algoritmos similares àqueles utilizados na tomografia computadorizada convencional. Isso resulta em uma menor dose de radiação do que na tomografia computadorizada convencional, mas não é adequada para avaliação de tecido mole (BOEDDINGHAUS e WHYTE, 2008). A tomografia de feixes cônicos proporciona uma menor dose de radiação e uma excelente qualidade de imagem, com distinção de estruturas delicadas, como do esmalte, dentina, cavidade pulpar e cortical alveolar (BUENO et al., 2007). O pioneirismo do aprimoramento desta técnica para Odontologia se desenvolveu no Japão por Arai et al. (1997), considerado o pai da tomografia de feixes cônicos na Odontologia (Universidade de Nihon, 1997). Mozzo et al. em 1998 foram os responsáveis pelo primeiro tomógrafo comercial (Newton-9000) (BUENO et al., 2007). A TCFC tem um grande potencial no que diz respeito à imagem préoperatória para implante (MONSOUR e DUDHIA, 2008). As principais vantagens da tomografia cone beam são: aparelhos mais compactos, excelente resolução, pequeno FOV (possibilidade de imagens somente da região de interesse), menor quantidade de artefatos metálicos, possibilidade de

11 9 posicionamento do paciente sentado na maioria dos aparelhos (os exames de ATM e dos seios maxilares são mais precisos com o paciente em posição vertical) e menor dose de radiação (BUENO et al., 2007). As doses efetivas de radiação em tomográfos de feixes cônicos variam, mas podem ser quase tão baixas quanto as unidades de raios-x dentário panorâmico e consideravelmente menores do que as da tomografia computadorizada médica (PATEL et al., 2007). Como comparação, o tomógrafo de feixes cônicos requer 30 a 90 vezes menos radiação do que o tomógrafo convencional utilizado nos sistemas atuais (VAN DER ZEL, 2008). Atualmente, a tomografia computadorizada e ressonância magnética constituem os meios padrão de aquisição de imagem dos seios paranasais e cavidade nasal. TC é o método de diagnóstico por imagem mais utilizado quando se está investigando doença inflamatória benigna dos seios paranasais (SHANKAR e EVANS, 2007). A TC permite ao radiologista determinar o local e extensão da doença nos seios paranasais, bem como nos tecidos moles circundantes e identificar as variações anatômicas que podem ocorrer nos indivíduos. 1.2 Variações anatômicas e processos patológicos dos seios maxilares Os seios paranasais são formados por um grupo de cavidades aeradas que se abrem nas fossas nasais, comunicando-se com estas por intermédio de canais e orifícios ou óstios. Distribuem-se em número de quatro, e seus nomes derivam dos ossos em que estão localizados: maxilar, frontal, etmoidal e esfenoidal (HUNGRIA, 1995). Várias são as funções atribuídas aos seios paranasais, incluindo: condicionamento do ar (aquecimento e umidificação), reservatório de ar, ventilação, redução do peso do crânio, contribuição na ressonância vocal e olfato, proteção, isolantes do cérebro e órbitas e participação na formação do crânio (WHITE e PHAROAH, 2007). Os seios maxilares são estruturas anatômicas de grande importância na prática odontológica devido à sua proximidade com as estruturas dentárias. Sendo assim, deve-se conhecer o aspecto normal e as principais doenças que acometem os seios maxilares (WHITE e PHAROAH, 2007). Os seios maxilares são os primeiros dos seios paranasais a se desenvolverem, surgindo no décimo sétimo dia de vida intra-uterina (WHITE e PHAROAH, 2007). Ao nascimento, o seio maxilar possui uma dimensão de

12 10 aproximadamente 10x3x4mm em seus diâmetros súpero-inferior, ântero-posterior e latero-lateral, respectivamente, e continua seu crescimento lentamente até os 7 anos de idade, quando sua expansão ocorre mais rapidamente até que todos dentes permanentes tenham erupcionado. As médias das dimensões dos seios maxilares de um adulto são 40x26x28mm, com um volume médio de 15mL (BAILEY, 1998). A forma do seio maxilar é tipicamente piramidal com a base da pirâmide formando a parede lateral nasal e o ápice estendendo para o zigoma. O teto do seio, que também forma o assoalho da órbita, é composto por um fino osso com o feixe vásculo-nervoso infra-orbital encontrado na porção central do osso. A parede anterior corresponde à fossa canina da maxila anterior. A parede posterior separa o seio do conteúdo da fossa infra-temporal e pterigo-maxilar. O assoalho do seio é formado pelo processo alveolar da maxila e parcialmente pelo palato duro. A parede medial do seio maxilar ou parede lateral da fossa nasal contém o óstio do seio, que abre no meato médio da cavidade nasal e promove a drenagem necessária. Em 15% a 40% dos casos o óstio acessório, bem pequeno, também é encontrado (BAILEY,1998). A extensão do seio é variável no adulto. Em aproximadamente 50% da população ele pode se expandir para o processo alveolar da maxila, formando um recesso alveolar (HAUMAN, CHANDLER e TONG, 2002). As variações anatômicas do seio maxilar incluem assimetria, hipoplasia de um ou ambos os seios maxilares, seio maxilar septado, duplo seio maxilar, seio maxilar atelectásico e seio etmomaxilar. Outras variações nas estruturas do complexo ostiomeatal podem ser observadas na região ou adjacentes ao seio maxilar tais como: células de Haller, desvio de septo, pneumatizações e óstios secundários (SHANKAR e EVANS, 2007). Seio maxilar hipoplásico refere-se a uma diminuição persistente do volume da cavidade devido à retração centrípeta das paredes do seio maxilar (LOEHRL e HONG, 2006). Na hipoplasia do seio maxilar tipo I (incidência 7%) há apenas uma diminuição branda do volume do seio maxilar, com um processo uncinado normal e um infundíbulo etmoidal normal (TASAR et al., 2007; SHANKAR e EVANS, 2007). Na hipoplasia do seio maxilar tipo II (incidência 3%) há uma redução branda a moderada no volume do seio maxilar combinada com evidência, na TC, de um processo uncinado ausente ou hipoplásico e um infundíbulo etmoidal ausente ou pouco definido. Há retração acentuada da fontanela posterior para dentro da cavidade do seio maxilar, e a fontanela membranosa pode ser erradamente

13 11 diagnosticada com um nível hidro-aéreo (TASAR et al., 2007; SHANKAR e EVANS, 2007). Na hipoplasia do seio maxilar tipo III (incidência 0,5%), o seio maxilar está ausente primariamente e consiste apenas em uma fenda. O infundíbulo etmoidal e o processo uncinado estão ausentes. A cavidade nasal e a órbita no lado comprometido são usualmente aumentadas (TASAR et al., 2007; SHANKAR e EVANS, 2007). A hipoplasia adquirida do seio maxilar pode ocorrer como resultado de uma variedade de fatores: trauma, infecção, irradiação, displasia fibrosa, doença de Paget e doenças sistêmicas. Ela é representada por uma maxila de tamanho normal, com a reação inflamatória produzindo uma obliteração e reabsorção parcial ou completa da luz do seio (SHANKAR e EVANS, 2007). Hiperplasia do seio maxilar é uma condição em que houve pneumatização extensa da maxila, com grandes recessos que pneumatizam a crista alveolar e os recessos laterais do zigoma. Há estreitamento compensador da cavidade nasal (SHANKAR e EVANS, 2007). O seio maxilar septado caracteriza-se pela presença de septos fibrosos ou ósseos que dividem incompletamente o seio em duas metades desiguais (SHANKAR e EVANS, 2007). Alguns autores definem o septo ósseo como uma estrutura óssea pontiaguda, enquanto a exostose é definida como uma estrutura óssea arredondada (NAITOH et al., 2009). O seio etmomaxilar ocorre quando o seio etmoidal posterior estende-se lateralmente para a maxila. Esta variação da normalidade tem o aspecto de um seio septado (SHANKAR e EVANS, 2007). A célula de Haller é uma célula etmoidal encontrada abaixo da bulla etmoidal, fazendo parte da parede lateral do infundíbulo maxilar (ZINREICH, KENNEDY e GAYLER, 1988). Essas células ocorrem precisamente na região dos óstios dos seios maxilares (STAMMBERGER e KENNEDY, 1995; BOLGER, BUTZIN e PARSOUS, 1991). Desvio de septo nasal pode ser definido como qualquer desvio da linha média (EARWAKER, 1993), podendo ser cartilaginoso, osteocartilaginoso ou ósseo. O desvio acentuado do septo nasal pode resultar em compressão do corneto médio ou do inferior e ocasionar obstrução do fluxo normal de muco, causando inflamação e infecções secundárias (LAINE e SMOKER, 1992).

14 12 Extensões ou pneumatizações maxilares são variações em relação à forma do seio maxilar. Encontramos extensões maxilares para o rebordo alveolar, região anterior, túber da maxila, palato duro, osso zigomático e região orbitária (ARIETA et al., 2005) Óstios secundários ou acessórios do seio maxilar são pequenos defeitos frequentemente encontrados nas fontanelas nasais membranosas anterior ou posterior. São situados imediatamente acima da concha inferior e usualmente se abrem diretamente para as porções anterior ou posterior do meato médio (SHANKAR e EVANS, 2007) Os principais processos patológicos que acometem os seios maxilares são mucosite (espessamento da membrana mucosa), sinusite, cisto de retenção mucoso, pólipo antrocoanal, infecção fúngica e antrólito. O revestimento mucoso dos seios paranasais, formado por epitélio respiratório, geralmente apresenta 1mm de espessura. A mucosa sinusal normal não é visualizada radiograficamente. Entretanto, pode haver um aumento nesta espessura de 10 a 15 vezes na presença de inflamação da mucosa. Esta alteração é denominada mucosite. Um espessamento mucoso maior que 3 mm geralmente é considerado como patológico. A imagem de uma mucosa espessada é facilmente visualizada como uma área não-corticalizada e mais hiperdensa que o normal, paralela à parede óssea dos seios (WHITE e PHAROAH, 2007). Sinusite é um processo inflamatório envolvendo a membrana mucosa dos seios paranasais e/ou osso subjacente (MOMENI, ROBERTS e CHEW, 2007). A sinusite crônica é definida como inflamação da mucosa dos seios paranasais que dura por pelo menos 12 semanas consecutivas (GLIKLICH e METSON, 1995). As características em TC na sinusite crônica são espessamento mucoso ou secreção retida na luz do seio. A sinusite recorrente ou crônica produzirá osteíte com neoformação de osso ao longo dos contornos da cavidade sinusal. A esclerose resultante pode levar ao espessamento da parede do seio e um volume diminuído da sua cavidade. As paredes sinusais podem ser erodidas por inflamação benigna crônica, usualmente ocorrendo ao longo da parede medial do seio maxilar e em torno do canal infra-orbitário (SHANKAR e EVANS, 2007). O cisto de retenção mucoso ocorre após obstrução de uma glândula mucosecretora do seio maxilar. A mucina é circundada por epitélio, e não ocorre extravasamento. Geralmente é assintomático e pode ser visto como um achado

15 13 incidental em 2 a 5% das radiografias dos seios da face. Radiograficamente há uma densidade em forma de cúpula, usualmente originando-se ao longo de uma parede do seio. Estes cistos são de densidade de líquido em imagens de TC e não podem ser diferenciados de pólipos. Esta diferenciação é clinicamente irrelevante, uma vez que ambas entidades são benignas e o tratamento das duas condições é idêntico (SHANKAR e EVANS, 2007). Pólipo antrocoanal, também denominado pólipo de Killian, é uma lesão polipóide benigna que se origina da mucosa do seio maxilar, atravessa seu óstio, e estende-se até as coanas. É mais freqüente em homens do que em mulheres, sendo mais prevalente em crianças e adultos jovens (FRANCHE et al., 2007). A etiologia dos pólipos antrocoanais não está clara. Um pólipo antrocoanal possui dois componentes: uma parte cística preenchendo o seio maxilar e uma parte sólida, que se estende por um pedículo através do óstio maxilar, ou por um óstio acessório para dentro do meato médio. Imagens de TC mostram uma massa dentro do antro que é contígua com uma massa de tecido mole de densidade uniforme na cavidade nasal ipsolateral (SHANKAR e EVANS, 2007). O termo sinusite fúngica engloba uma grande variedade de doenças infecciosas fúngicas, desde formas relativamente inócuas até variedades potencialmente fatais. As duas formas primárias da doença fúngica incluem sinusite fúngica alérgica e sinusite fúngica invasiva. A sinusite fúngica alérgica é uma doença benigna, não invasiva, causada por uma reação de hipersensibilidade à presença de fungos nos seios. A sinusite fúngica invasiva ocorre principalmente em indivíduos imunossuprimidos (MOMENI, ROBERTS e CHEW, 2007). Na infecção fúngica dos seios paranasais há espessamento mucoperióstico nodular, ausência de níveis hidroaéreos, opacificação dos seios etmoidais e erosão óssea. Áreas de atenuação aumentadas em um seio doente são sugestivas de infecção fúngica (SHANKAR e EVANS, 2007). Os antrólitos são cálculos localizados no seio maxilar, formados como resultado da deposição de sais minerais ao redor de um nicho orgânico (GÜNERI, KAYA e ÇALISKAN, 2005). São estruturas bem delimitadas, podendo apresentar um formato regular ou irregular. O aspecto da densidade interna pode variar desde uma leve radiopacidade até uma estrutura extremamente radiopaca. A densidade interna pode ser homogênea ou heterogênea (WHITE e PHAROAH, 2007).

16 14 2 CONSIDERAÇÕES GERAIS A tomografia computadorizada de feixes cônicos é atualmente o recurso imaginológico mais utilizado para planejamento de implantes dentários. Esses exames permitem visualizar estruturas anatômicas importantes para este planejamento, entre as quais se destacam os seios maxilares. Os seios maxilares podem apresentar variações anatômicas e processos patológicos que, além de apresentar relevância clínica, podem modificar o planejamento dos implantes.

17 15 3 OBJETIVOS 3.1 Objetivo geral Avaliar a presença de alterações nos seios maxilares em tomografias computadorizadas de feixes cônicos da maxila solicitadas para planejamento de implantes dentários. 3.2 Objetivos específicos Avaliar a frequência de variações anatômicas nos seios maxilares em tomografias computadorizadas de feixes cônicos da maxila solicitadas para planejamento de implantes dentários. Avaliar a frequência de processos patológicos nos seios maxilares em tomografias computadorizadas de feixes cônicos da maxila solicitadas para planejamento de implantes dentários.

18 16 REFERÊNCIAS GERAIS ABRAHAMS, J.J. The role of diagnostic imaging in dental implantology. Radiologic Clinics of North America, v.31, p , ARIETA, L.C. et al. Extensões dos seios maxilares detectadas em radiografias periapicais. Revista Odonto Ciência Faculdade Odonto/PUCRS, v.20, n.47, p.18-22, Janeiro/Março BAILEY, B.J. Head and Neck Surgery-Otolaryngology. 2. ed. Philadelphia, USA: Lippincott-Raven Publishers, BOEDDINGHAUS, R.; WHYTE, A. Current concepts in maxillofacial imaging. European Journal of Radiology, v.66, p , BOLGER, W.E.; BUTZIN, C.A.; PARSONS, D.S. Paranasal sinus bony anatomic variations and mucosal abnormalities: CT analysis for endoscopic sinus surgery. The Laryngoscope, v.101, p.56-64, BUENO, M.R. et al. Tomografia computadorizada Cone Beam: revolução na Odontologia. Revista da Associação Paulista de Cirurgiões Dentistas, v.61, n.4, p , EARWAKER, J. Anatomic variants in sinonasal CT. RadioGraphics, v.13, p , FRANCHE, G.L.S. et al. Polipectomia endoscópica com meatotomia média como tratamento de pólipo antrocoanal. Revista Brasileira de Otorrinolaringologia, v.73, n.5, p , Setembro/Outubro GARIB, D.G. et al. Tomografia computadorizada de feixe cônico (Cone Beam): entendendo este novo método de diagnóstico por imagem com promissora aplicabilidade na Ortodontia. Revista Dental Press Ortodontia e Ortopedia Facial, v.12, n.2, p , Março/Abril GLIKLICH, R.E.; METSON, R. The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngology-Head and Neck Surgery, v.113, n.1, p , July 1995.

19 17 GÜNERI, P.; KAYA, A.; ÇALISKAN, M.K. Antroliths: Survey of the literature and report of a case. Oral Surgery Oral Medicine Oral Pathology Oral Radiology & Endodontics, v.99, p , HANSEN, S.L.; GRÖNDAHL, K.; EKESTUBBE, A. Cone-Beam CT for Preoperative Implant Planning in the Posterior Mandible: Visibility of Anatomic Landmarks. Clinical Implant Dentistry and Related Research, v.11, n.3, p , HAUMAN, C.H.J.; CHANDLER, N.P.; TONG, D.C. Endodontic implications of the maxillary sinus: a review. International Endodontic Journal, v.35, p , HUNGRIA, H. Anatomia e fisiologia dos seios paranasais. Otorrinolaringologia. 7. ed. Rio de Janeiro: Guanabara Koogan, JUNG, J.H. et al. A retrospective study of the effects on sinus complications of exposing dental implants to the maxillary sinus cavity. Oral Surgery Oral Medicine Oral Pathology Oral Radiology & Endodontics, v.103, p , LAINE, F.J.; SMOKER, W.R. The ostiomeatal unit and endoscopic surgery: anatomy, variations and imaging findings in inflammatory diseases. American Journal of Roentgenology, v.159, p , LOEHRL, T.A.; HONG, S.H. The hypoplastic maxillary sinus and the orbital floor. Current Opinion in Otolaryngology & Head and Neck Surgery, v.14, p.35-37, MOMENI, A.K.; ROBERTS, C.C.; CHEW, F.S. Imaging of Chronic and Exotic Sinonasal Disease: Review. American Journal of Roentgenology, v.189, p.35-45, December MONSOUR, P.A.; DUDHIA, R. Implant radiography and radiology. Australian Dental Journal, v.53, p.s11-s25, NAITOH, M. et al. Assessment of maxillary sinus septa using cone-beam computed tomography: Etiological consideration. Clinical Implant Dentistry and Related Research, v.11, n.1, p.e52-58, PATEL, S. et al. The potential applications of cone beam computed tomography in the management of endodontic problems. International Endodontic Journal, v.40, p , 2007.

20 18 SHANKAR, L; EVANS, K. Atlas de Imagem dos Seios Paranasais. 2. ed. Rio de Janeiro: Editora Revinter, STAMMBERGER, H.R.; KENNEDY, D.W. Paranasal sinuses: anatomic terminology and nomenclature. The Anatomic Terminology Group. The Annals of Otology, Rhinology and Laryngology, v.167, p.7-16, TASAR, M. et al. Bilateral maxillary sinus hypoplasia and aplasia: radiological and clinical findings. Dentomaxillofacial Radiology, v.36, p , VAN DER ZEL, J.M. Implant Planning and Placement Using Optical Scanning and Cone Beam CT Technology. Journal of Prosthodontics, v.17, p , WHITE, S.C.; PHAROAH, M.J. Radiologia Oral: Fundamentos e Interpretação. 5. ed. Rio de Janeiro: Elsevier Editora, ZINREICH, S.J.; KENNEDY, D.W.; GAYLER, B.W. Computed tomography of nasal cavity and paranasal sinuses: an evaluation of anatomy for endoscopic sinus Surgery. Clear Images, v.1, p.2-10, 1988.

21 19 APÊNDICE 1 Artigo principal da dissertação que será submetido ao periódico Clinical Oral Implants Research (Qualis A2) As normas do periódico podem ser acessadas em:

22 20 Anatomic variations and lesions of the maxillary sinus detected in cone beam computed tomography for dental implants Juliana Pelinsari Lana 1 2 Pollyanna Moura Rodrigues Carneiro 1 Vinícius de Carvalho Machado 2 Paulo Eduardo Alencar de Souza 1 Flávio Ricardo Manzi 1 Martinho Campolina Rebello Horta 1 1 Department of Dentistry, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil 2 Slice Diagnóstico Volumétrico por Imagem, Belo Horizonte, Minas Gerais, Brazil Running title: Maxillary sinus alterations detected in cone beam tomography Key words: maxillary sinus; cone beam computed tomography; dental implants Corresponding author: Martinho Campolina Rebello Horta Pontifícia Universidade Católica de Minas Gerais - Departamento de Odontologia Av. Dom José Gaspar Prédio 45 - Sala 110 Belo Horizonte - MG - Brasil - CEP: Phone: (+55) Fax: (+55) martinhohorta@pucminas.br

23 21 Abstract Objective: To evaluate the presence of anatomic variations and lesions of the maxillary sinus in cone beam computed tomography (CBCT) of the maxilla required for dental implant planning. Material and methods: This transversal prevalence study evaluated a convenient sample of 500 CBCT exams. The inclusion criteria were CBCT exams of the maxilla required for dental implant planning. The CBCT exams were independently evaluated by two oral and maxillofacial radiologists who assessed the presence of anatomic variations and lesions of the maxillary sinus. Results: The anatomic variations detected were pneumatization (83.2%), nasal septum deviation (53.2%), antral septa (44.4%), secondary ostium (13.4%), hypoplasia (4.8%), exostosis (2.6%), ethmomaxillary sinus (1.2%), and Haller cells (0.6%). The identified lesions were mucosal thickening (<3mm in 62.6% and >3mm in 54.8%), polypoid lesions (21.4%), discontinuity of the sinus floor (17.4%), air-fluid level (4.4%), bone thickening of the maxillary sinus wall (3.8%), antroliths (3.2%), discontinuity of the sinus lateral wall (2.6%), sinus opacification (1.8%), and foreign body (1.6%). Conclusion: Anatomic variations and lesions of the maxillary sinus are common findings. The recognition of these alterations is noteworthy in dental practice and especially in implantology. In addition to modify dental implant planning, some of these conditions must require specialized treatment. Introduction The growing development and popularity of dental implants has triggered an increasing demand for oral and maxillofacial radiology services (Tsiklakis et al. 2005; Dula et al. 2001; Bou Serhal et al. 2001a). Computed tomography (CT) images allow the location of anatomic structures and provide information about bone dimensions and morphology, information of great importance for dental implant planning (Tsiklakis et al. 2005; Dula et al. 2001; Bou Serhal et al. 2001b; Cohnen et al. 2002). Using a CT scan-based planning system, the surgeon can select the best locations for implant placement (van der Zel 2008). Cone beam computed tomography (CBCT) utilizes a coneshaped X-ray beam to obtain projection data from a flat detector during a single 360 o rotation, in which a volumetric data set is reconstructed using algorithms similar to those used in

24 22 conventional computed tomography (Boeddinghaus & Whyte 2008). In the last years, this technique has proved to be more economical and efficient than conventional CT for dental implant planning (White & Pharaoh 2004). This type of scanner has reduced radiation dose and provides adequate images for evaluation of high-contrast structures in the oral and maxillofacial region (Ludlow et al. 2006; Palomo et al. 2008). Therefore, is not appropriate for soft tissue assessment (Boeddinghaus & Whyte 2008). The paranasal sinuses include maxillary, frontal, ethmoid, and sphenoid sinuses. The main functions of the paranasal sinuses are humidification and warming of inspired air, regulation of intranasal pressure, increasing the surface area of the olfactory membrane, lightening the skull, imparting voice resonance, shock absorption, and contributing to facial growth (Bailey 1998). The anatomic variations of the maxillary sinus are pneumatization, asymmetry, hypoplasia, antral septa, double maxillary sinus, atelectasic maxillary sinus, and ethmomaxillary sinus. Ostiomeatal complex anatomic variations as nasal septum deviation, secondary ostium and Haller cells should also be considered (Shankar & Evans 2006). Mucosal thickening, sinusitis, mucous retention cyst, antrochoanal polyp, fungal infection, and antrolith are examples of maxillary sinus lesions (Shankar & Evans 2006). Since the maxillary sinuses are anatomical structures of great importance in dental practice (White & Pharaoh 2004) and CBCT is currently the most used image exam for dental implant planning (Ludlow & Ivanovic 2008), the recognition of anatomic variations and lesions of the maxillary sinuses in CBCT is noteworthy. Therefore, the aim of this study was to evaluate the presence of anatomic variations and lesions of the maxillary sinus in CBCT of the maxilla required for dental implant planning. Material and methods Study design This transversal prevalence study evaluated a convenient sample of 500 CBCT exams. The CBCT exams were made in a private dental radiology clinic in Belo Horizonte, Brazil, between March and September of The study was approved by the local ethics committee.

25 23 The following inclusion criteria were applied: 1) CBCT exams of the maxilla; 2) CBCT exams required for implant planning; 3) CBCT exams from patients who accepted to participate in the study. CBCT exams were excluded on the basis of: 1) exams not displaying all the extension of the lower third of the maxillary sinus; 2) presence of technical artifacts that could difficult the evaluation of the maxillary sinus. Image acquisition and analysis The exams were performed by the i-cat cone beam computed tomograph (Imaging Sciences International, Hatfield, PA, USA). The tomograph specifications were: Field of view: 6 cm covering the maxilla region; Voxel: 0.2 mm; Scan time: 40 seconds. Image analysis was performed on the i-cat software, on a multiplanar reconstruction window in which the axial, coronal and sagittal planes could be visualized in 0.2 mm intervals. The CBCT exams were independently evaluated by two authors who assessed the presence of anatomic variations and lesions of the maxillary sinus. Doubtful cases were reanalyzed and a consensus agreed. The following anatomic variations were considered: 1) Pneumatization; 2) Nasal septum deviation; 3) Antral septa; 4) Secondary ostium; 5) Hypoplasia; 6) Ethmomaxillary sinus; 7) Haller cells, 8) Exostosis. The following lesions were considered: 1) Mucosal thickening (<3mm and >3mm); 2) Polypoid lesions (mucous retention cyst and/or antrochoanal polyp); 3) Discontinuity of the sinus wall; 4) Air-fluid level; 5) Bone thickening; 6) Antrolith; 7) Sinus opacification; 8) Foreign body. Results In a total of 500 CBCT exams, 262 (52.4%) were from female and 238 (47.6%) from male patients. The patient s age range was years, with a median age of 52 years. The identified maxillary sinus alterations are referred in Tables 1 and 2 as well as illustrated in Figure 1, Figure 2, and Figure 3. Maxillary sinus pneumatization (Figure 1 a) was the most common anatomic variation detected, observed in 416 patients (83.2%). Alveolar pneumatization was

26 24 present in all of the 416 cases. Pneumatization sites were multiple in 191 (46%) and single in 225 (54%) cases, in which it was always alveolar. Nasal septum deviation (Figure 1 b) was identified in 266 cases (53.2%), in which 87 showed a bone spur. In 29 patients (5.8%) the image limits did not allow the evaluation of this variation. Antral septa (Figure 1 c) were found in 222 (44.4%) cases. Secondary ostium (Figure 1 d) was identified in 67 (13.4%) cases. Nevertheless, in 353 exams (70.6%) the site of this anatomic variation was out of the image limits. Maxillary sinus hypoplasia (Figure 1 e) was apparent in only 24 cases (4.8%). Exostosis (Figure 1 f) was identified in 13 (2.6%) patients. Ethmomaxillary sinus (Figure 1 g) was identified in only 6 (1.2%) and Haller cells (Figure 1 h) in just 3 (0.6%) of the cases. Nonetheless, as these anatomic variations are located near the maxillary sinus roof, the image limits did not allow the evaluation of these variations in respectively 461 (92.2%) and 462 (92.4%) of the 500 exams. Maxillary sinus mucosal thickening was the most detected lesion (Figure 2 a and b). The mucosal thickening was considered as <3mm in 313 (62.6%) and as >3mm in 274 (54.8%) cases. Polypoid lesions (Figure 3 a and b) were identified in 107 (21.4%) patients. Discontinuity of the sinus floor was found in 87 (17.4%) cases. Of these 87 cases, 25 were associated to periapical lesions (Figure 2 c), 24 to intrasinus bone graft (Figure 2 d), 20 to implant fenestration (Figure 2 e), 7 to tooth extraction (Figure 2 f), 3 to both intra-sinus bone graft and implant, 1 to endodontic filling material fenestration (Figure 2 g), and 7 to no apparent cause (Figure 2 h). Airfluid level (Figure 3 c), bone thickening of the maxillary sinus wall (Figure 3 d), and antroliths (Figure 3 e) were respectively found in 22 (4.4%), 19 (3.8%), and 16(3.2%) cases. Discontinuity of the sinus lateral wall (Figure 3 f) was identified in 13 (2.6%) patients. Sinus opacification (Figure 3 g) and foreign body (Figure 3 h) were respectively found in only 9 (1.8%) and 8 (1.6%) patients. Discussion Maxillary sinus pneumatization was the most common anatomic variation detected. This entity was observed in 416 patients (83.2%). Pneumatization is an anatomic variation characterized by the maxillary sinus enlargement. The sinus can extend to alveolar ridge, anterior region, maxillary tuber, palate, zygomatic bone and/or orbitary region (Sicher 1975, White & Pharaoh 2004). Alveolar pneumatization has been reported in approximately 50% of the population (Schuh et al. 1984) and

27 25 was present in all of the 416 patients showing sinus pneumatization. Atrophy of the maxilla caused by edentulism is characterized by vertical and horizontal bone loss (Gosau et al. 2009). The maxillary sinus pneumatization, particularly the alveolar extension, can exacerbate the problem of reminiscent bone caused by atrophy of the maxilla, leaving only few millimeters of bone to implant insertion (Blake et al. 2008). Anterior extension of the maxillary sinus can also affect implant planning, although is not a common finding (Schuh et al. 1984). This type of pneumatization was in fact identified in only 26 (5.2%) patients, always associated with alveolar pneumatization. Nasal septum deviation can be defined as any deviation from the midline and can be cartilaginous, osseous or osteocartilaginous (Earwaker 1993). This entity was evaluated in this study, in conjunction with the maxillary sinus anatomic variations, since severe deviation of the nasal septum can compress the middle or inferior nasal turbinate causing obstruction of the mucus flow and, consequently, inflammation or secondary infection of the maxillary sinus (Laine & Smoker 1992; Kayalioglu et al. 2000). Nasal septum deviation was identified in 266 cases (53.2%), in which 87 showed a bone spur. The prevalence of this anatomic variation has been reported as 14,1% (Dutra & Marchiori 2002), 23,3% (Kinsui et al. 2002), 36% (Arslan et al. 1999), 44% (Earwaker 1993), and 80% (Perez-Piñas et al. 2000). Antral septa are osseous or fibrous septa that incompletely divide the maxillary sinus (Shankar & Evans 2006). Its prevalence ranges from 16% to 58% (Underwood 1910; Betts & Miloro 1994; Ulm et al. 1995; Krennmair et al. 1997; Velasquez-Plata et al. 2002). In this study, antral septa were detected in almost half of the evaluated cases (44.4%). It is important to emphasize that the presence of antral septa might increase the risk of sinus membrane perforation during the maxillary sinus floor elevation surgery (van den Bergh et al. 2000; Tatum 1986; Krennmair et al. 1999). The accidental perforation of this membrane can lead to development of acute or chronic sinusitis as well as subsequent bone graft resorption (Abrahams et al. 2000; Aimetti et al. 2001; Kunkel & Reichert 2003). Furthermore, antral septa can difficult the lifting of the bone plate and of the sinus membrane during surgery (Tidwell et al., 1992). Secondary or accessory ostium of the maxillary sinus are small defects often found in the anterior and posterior nasal fontanelles, located immediately above the inferior turbinate. Secondary ostium usually opens directly to the anterior or posterior portions of the middle meatus (Shankar & Evans, 2006). This anatomic variation has

28 26 been identified in 15% to 40% of the patients (Bailey 1998), although it not usually cooperates with the maxillary sinus drainage (Shankar & Evans 2006). Secondary ostium was identified in 67 (13.4%) cases. Nevertheless, in 353 exams (70.6%) the site of this anatomic variation was out of the image limits. Maxillary sinus hypoplasia (MSH) is the underdevelopment of the maxillary sinus. Although the MSH is a well-known condition, the complete aplasia of the maxillary sinus (sinus failure to develop at all) is rare. MSH can be classified in three types based on embryological development of the sinus and uncinate process. MSH type I exhibits slight to reasonable sinus hypoplasia, well-developed uncinate process, distinct infundibular passage and variable degrees of sinus mucosal thickening. MSH type II displays considerable sinus hypoplasia, hypoplastic uncinate process, indistinct or absent infundibular passage and total sinus opacification on CT scan. MSH type III shows severe sinus hypoplasia and hypoplastic or absent uncinate process (Tasar et al. 2007). The maxillary sinus can become hypoplastic during its embryological development or late due to trauma, iatrogeny or structural causes (Stammberger 1986). The narrow infundibular passage associated with the absence of a natural ostium cause the mucosal thickening of the hypoplastic sinus (Weed & Cole 1994). Furthermore, MSH also causes the lateral extension of the lateral nasal wall, making difficult the surgical procedures (Kapoor et al. 2002). Maxillary sinus hypoplasia was identified in only 24 cases (4.8%), in which 19 were unilateral (3.8%) and 5 bilateral (1%). Karmody et al. evaluated 750 radiographs and observed MSH in 8.93% of cases (Karmody et al. 1977). Milczuk et al. detected MSH in 20 of 114 patients with chronic rhinosinusitis (17.5%), by using paranasal sinus computed tomography (Milczuk et al. 1993). The presence of maxillary sinus exostosis was assessed in dry skulls using CBCT. The exostosis, defined as a rounded bone structure, was found in 30% of the cases (Naitoh et al. 2009). On the other hand, our results showed exostosis in only 13 patients (2.6%). The ethmomaxillary sinus is characterized by the lateral extension of the posterior ethmoid sinus to the maxilla (Shankar & Evans 2006). Even though It have been suggested that ethmomaxillary sinus could be sites of recurrent infections, the relationship between chronic sinusitis and ethmomaxillary sinus is not entirely clear (Khanobthamchai et al. 1991). The prevalence of its anatomic variation ranges from 0.7% to 2% (Khanobthamchai et al. 1991; Sirikci et al. 2004). Ethmomaxillary sinus

29 27 was identified in only 6 (1.2%) of the cases. Nevertheless, as this anatomic variation is located near the maxillary sinus roof, the image limits did not allow its evaluation in 461 (92.2%) of the 500 exams. Haller cells are ethmoid cells found below the ethmoid bulla, being part of the lateral wall of the maxillary infundibulum (Zinreich et al. 1988). As Haller cells are located exactly in the region of the maxillary sinus ostium (Stammberger & Kennedy 1995; Bolger et al. 1991), some authors believe that this anatomic variation should be an etiological factor in recurrent maxillary sinusitis (Zinreich et al. 1987). The prevalence of Haller cells in the literature ranges from 1% to 45% (Bolger et al. 1991; Tonai & Baba 1996; Arslan et al. 1999; Kayalioglu et al. 2000; Perez- Piñas et al. 2000; Kinsui et al. 2002; Dutra & Marchiori 2002). Haller cells were found in only 3 cases (0.6%). However, as it are located near the maxillary sinus roof, the image limits did not allow the evaluation of this variation in 462 (92.4%) of the 500 exams. The paranasal sinuses mucosa is lined by respiratory epithelium and normally shows 1 mm of thickness (Bailey 1998; White & Pharaoh 2004). Nevertheless, the presence of inflammation can develop an increase of 10- to 15-fold in the sinus mucosa thickness. The image of a thickened sinus mucosa is easily visualized as a non-cortical area, more hyperdense than normal and parallel to the sinus bony wall (White & Pharaoh 2004). Sinusitis is an inflammatory process involving the mucous membranes of the paranasal sinuses or the underlying bone (Momeni et al. 2007). Chronic disease is characterized by the inflammation of the paranasal sinuses mucosa for no less than 12 consecutive weeks (Gliklich & Metson 1995). The tomographic characteristics of chronic sinusitis are mucosal thickening or retained secretions in the sinus. The recurrent or chronic sinusitis produce osteitis with bone neoformation along the sinus contours (Shankar & Evans 2006). Mucosal thickening is a characteristic found in both acute and chronic sinusitis (Momeni et al. 2007). A mucosal thickening >3mm is usually considered pathologic (White & Pharoah 2004). The results demonstrated that maxillary sinus mucosal thickening (unilateral or bilateral) was the most detected lesion. The mucosal thickening was considered as <3mm in 313 (62.6%) and as >3mm in 274 (54.8%) cases. The characteristic findings of inflammatory sinus disease are air-fluid level, mucosal thickening and sinus opacification. The only distinctive feature of acute sinusitis is the air-fluid level as an isolated finding, while the characteristic feature of chronic sinusitis is the bone thickening of the maxillary sinus wall (Zinreich et al.

30 ). Sinus opacification and air-fluid level are the most specific signs of bacterial rhinosinusitis (Wald 1993). Air-fluid level, bone thickening of the maxillary sinus wall, and sinus opacification were respectively found in 22 (4.4%), 19 (3.8%), and 9 (1.8%) of the 500 evaluated cases. Fungal sinusitis includes an extensive variety of sinus infections, from relatively harmless to potentially deadly (Momeni et al. 2007). Fungal infection of the paranasal sinus shows nodular mucoperiosteal thickening, no air-fluid level, opacification of the ethmoid sinuses and bone erosion. Areas of increased attenuation in the altered sinus are suggestive of fungal infection (Shankar & Evans 2006). No tomographic image suggesting fungal infection was detected in this study, probably due to the fact that the evaluated images were from a convenient sample of CBCT exams required for implant planning. Polypoid lesions were identified in 107 (21.4%) patients, in which 87 were unilateral and 20 bilateral. The polypoid lesions of the maxillary sinus are represented by the mucous retention cyst and the antrochoanal polyp. The mucous retention cyst occurs after obstruction of mucus-secreting glands of the maxillary sinus, is usually asymptomatic and can be viewed as an incidental finding in 2% to 5% of the sinus radiographs. Radiographically, this lesion is characterized by a dome-shaped radiopacity extending from the sinus wall (Shankar & Evans 2006). Antrochoanal polyp, also called Killian polyp, is a benign polypoid lesion (Pruna et al. 2000) that originates from the maxillary sinus mucosa and extends through its ostium to the choana (Hong et al. 2001). Its etiology is unclear and the lesion is more common in children and young adults (Gendeh et al. 2004). Computed tomography shows an uniform density mass in the sinus extending to the ipsilateral nasal cavity. As both polypoid lesions (mucous retention cyst and antrochoanal polyp) show fluid density in the sinus on computed tomography, it cannot be differentiated in CBCT. However, it is important to highlight that this differentiation is clinically irrelevant, since both lesions are benign and have identical treatment (Shankar & Evans 2006). Discontinuity of the sinus floor was found in 87 (17.4%) cases. Mucosal thickening >3mm was identified in 64 of this 87 patients (73.5%). Odontogenic sinusitis usually occurs after disruption of the sinus mucous membrane by conditions as dental infection, tooth extraction, orthognathic surgery, maxillary sinus floor elevation surgery, intra-sinus bone graft, and dental implants (Kretzschmar & Kretzschmar 2003; Ueda & Kaneda 1992; Timmenga et al. 1997). Of the 87 cases

31 29 showing discontinuity of the sinus floor, 25 were associated to periapical lesions, 24 to intra-sinus bone graft, 20 to implant, 7 to tooth extraction, 3 to both intra-sinus bone graft and implant, 1 to endodontic filling materal, and 7 to no apparent cause. Antroliths are circumscribed pathologic calcifications formed as a result of mineral salt deposition around an organic nucleus in the paranasal sinuses (Nass Duce et al. 2003; Güneri et al., 2005; Rodrigues et al., 2009). Radiographically, this lesion is a radiopaque mass showing variable sizes and shapes (Güneri et al., 2005). A previous report using computed tomography has shown low prevalence of antroliths in the paranasal sinuses, found in 3 of 1957 patients (0.15%) (Nass Duce et al. 2003). Our results showed a higher prevalence, since 16 maxillary sinus antroliths were detected (3.2%). Foreign bodies were found in only 8 CBCT exams (1.6%). Foreign bodies may have access into the maxillary sinus through an oroantral communication which remains as an oroantral fistula. Furthermore, this access can also occur by the dental alveolus of a newly extracted tooth, by means of the root canal or due to a surgical procedure near the maxillary sinus. Since foreign bodies should cause complications as chronic sinusitis, its removal is indicated (Laskin &Dierks 1999). The recognition of anatomic variations and lesions of the maxillary sinuses is noteworthy in dental practice and especially in implantology. In addition to modify dental implant planning, some of these conditions must be treated by an otorhinolaryngologist or by an oral and maxillofacial surgeon. Therefore, its knowledge is essential not only to oral and maxillofacial radiologists, but also to implantologists and general practice dentists. Acknowledgements This study was partially supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, Fundação de Amparo à Pesquisa do Estado de Minas Gerais - FAPEMIG, and PUC Minas, Brazil. References Abrahams, J.J., Hayt, M.W., Rock, R. (2000) Sinus lift procedure of the maxilla in patients with inadequate bone for dental implants: radiographic appearance. American Journal of Roentgenology 174:

32 30 Aimetti, M., Romagnoli, R., Ricci, G., Massei, G. (2001) Maxillary sinus elevation: the effect of macrolacerations and microlacerations of the sinus membrane as determined by endoscopy. The International Journal of Periodontics & Restorative Dentistry 21: Arslan, H., Aydinlioglu, A., Bozkurt, M., et al. (1999) Anatomic variations of the paranasal sinuses: CT examination for endoscopic sinus surgery. Auris Nasus Larynx. 26: Bailey, B.J. (1998) Head and Neck Surgery Otolaryngology, 2nd edition, p , Philadelphia, USA: Lippincott-Raven Publishers. Betts, N.J.,Miloro, M. (1994) Modification of the sinus lift procedure for septa in the maxillary antrum. Journal of Oral and Maxillofacial Surgery 52: Blake, F.A.S., Blessmann, M., Pohlenz, P., Heiland, M. (2008) A new imaging modality for intraoperative evaluation of sinus floor augmentation. International Journal of Oral & Maxillofacial Surgery 37: Boeddinghaus, R., Whyte, A. (2008) Current concepts in maxillofacial imaging. European Journal of Radiology 66: Bolger, W.E., Butzin, C.A., Parsons, D.S. (1991) Paranasal sinus bony anatomic variations and mucosal abnormalities: CT analysis for endoscopic sinus surgery. Laryngoscope 101: Bou Serhal, C., Jacobs, R., Gijbels, F., Bosmans, H., Hermans, R., Quirynen, M., et al. (2001a) Absorbed doses from spiral CT and conventional spiral tomography: a phantom vs. cadaver study. Clinical Oral Implants Research 12: Bou Serhal, C., van Steenberghe, D., Bosmans, H., Sanderink, G.C., Quirynen, M., Jacobs, R. (2001b) Organ radiation dose assessment for conventional spiral tomography: a human cadaver study. Clinical Oral Implants Research 12: Cohnen, M., Kemper, J., Mobes, O., Pawelzik, J., Modder, U. (2002) Radiation dose in dental radiology. European Radiology 12: Dula, K., Mini, R., van der Stelt, P.F., Sanderink, G.C., Schneeberger, P., Buser, D. (2001) Comparative dose measurements by spiral tomography for preimplant diagnosis: the Scanora machine versus the Cranex Tome radiography unit. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics 91: Dutra, L.D., Marchiori, E. (2002) Tomografia computadorizada helicoidal dos seios paranasais na criança: avaliação das sinusopatias inflamatórias. Radiologia Brasileira 35: Earwaker, J. (1993) Anatomic variants in sinonasal CT. Radiographics 13:

33 31 Gendeh, B.S., Long, Y.T., Misiran, K. (2004) Antrochoanal polyps: Clinical presentation and the role of powered endoscopic polypectomy. Asian Journal of Surgery 27: Gliklich, R.E., Metson, R.N. (1995) The health impact of chronic sinusitis in patients seeking otolaryngologic care. Otolaryngology - Head and Neck Surgery 113: Gosau, M., Rink, D., Driemel, O., Draenert, F.G. (2009) Maxillary sinus anatomy: A cadaveric study with clinical implications. The Anatomical Record 292: Güneri, P., Kaya, A., Çaliskan, M.K. (2005) Antroliths: Survey of the literature and report of a case. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics 99: Hong, S.K., Min, Y.G., Kim, C.N., Byun, S.W. (2001) Endoscopic removal of the antral portion of antrochoanal polyp by powered instrumentation. Laryngoscope 111: Kapoor, P.K., Kumar, B.N., Watson, S.D. (2002) Maxillary sinus hypoplasia. The Journal of Laryngology & Otology 116: Karmody, C.S., Carter, B., Vincent, M.E. (1977) Developmental anomalies of the maxillary sinus. Transactions. Section on Otolaryngology. American Academy of Ophthalmology and Otolaryngology 84: Kayalioglu, G., Oyar, O., Govsa, F. (2000) Nasal cavity and paranasal sinus bony variations: a computed tomographic study. Rhinology 38: Khanobthamchai, K., Shankar, L., Hawke, M., et al. (1991) Ethmomaxillary sinus and hypoplasia of maxillary sinus. Journal of Otolaryngology 20: Kinsui, M.M., Guilherme, A., Yamashita, H.K. (2002) Anatomical variations and sinusitis: a computed tomographic study. Revista Brasileira de Otorrinolaringologia 68: Krennmair, G., Ulm, C., Lugmayr, H. (1997) Maxillary sinus septa: incidence, morphology, and clinical implications. Journal of CranioMaxillofacial Surgery 25: Krennmair, G., Ulm, G.W., Lugmayr, H., Solar, P. (1999) The incidence, location and height of maxillary sinus septa in the edentulous and dentate maxilla. Journal of Oral and Maxillofacial Surgery 57: Kretzschmar, D.P., Kretzschmar, J.L. (2003) Rhinosinusitis: review from a dental perspective. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics 96: Kunkel, M., Reichert, T.E. (2003) Maxillary sinusitis after internal sinus lift. Zahnarztl Mitt 93:

34 32 Laine, F.J., Smoker, W.R. (1992) The ostiomeatal unit and endoscopic surgery: anatomy, variations and imaging findings in inflammatory diseases. American Journal of Roentgenology 159: Laskin, D.M., Dierks, J.D. (1999) Diagnosis and treatment of diseases and disorders of the maxillary sinus. Oral & Maxillofacial Surgery Clinics of North America 11: Ludlow, J.B., Davies-Ludlow, L.E., Brooks, S.L., Howerton, W.B. (2006) Dosimetry of 3 CBCT devices for oral and maxillofacial radiology: CB Mercuray, NewTom 3G and i-cat. Dentomaxillofacial Radiology 35: Ludlow, J.B., Ivanovic, M. (2008) Comparative dosimetry of dental CBCT devices and 64-slice CT for oral and maxillofacial radiology. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics 106: Milczuk, H.A., Dalley, R.W., Wessbacher, F.W., Richardson, M.A. (1993) Nasal and paranasal sinus anomalies in children with chronic sinusitis. Laryngoscope 103: Momeni, A.K., Roberts, C.C., Chew, F.S. (2007) Imaging of chronic and exotic sinonasal disease: Review. American Journal of Roentgenology 189: S Naitoh, M., Suenaga, Y., Kondo, S., Gotoh, K., Ariji, E. (2009) Assessment of maxillary sinus septa using cone-beam computed tomography: Etiological consideration. Clinical Implant Dentistry and Related Research 11:e Nass Duce, M., Taals, D.Ü., Özer, C., Yildiz, A., Apaydin, D.F., Özgür, A. (2003) Antrolithiasis: a retrospective study. The Journal of Laryngology & Otology 117: Palomo, J.M., Rao, P.S., Hans, M.G. (2008) Influence of CBCT exposure conditions on radiation dose. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology & Endodontics 105: Pérez-Piñas, Sabaté, J., Carmona, A., et al. (2000) Anatomical variations in the human paranasal sinus region studied by CT. Journal of Anatomy 197: Pruna, X., Ibanez, J.M., Serres, X., Garriga, V., Barber, I., Vera, J. (2000) Antrochoanal polyps in children: CT findings and differential diagnosis. European Radiology 10: Rodrigues, M.T.V., Munhoz, E.A., Cardoso, C.L., Freitas, C.A., Damante, J.H. (2009) Chronic maxillary sinusitis associated with dental impression material. Medicina Oral, Patología Oral y Cirugía Bucal 14: E Schuh, E., Schmiedl, W., Vogel, G. (1984) Anatomic limits of endosseous implantation. Zeitschrift Stomatologie 81:

35 33 Shankar, L., Evans, K. (2006) An Atlas of Imaging of the Paranasal Sinuses, 2nd edition. Norwich, UK: Informa Healthcare. Sicher, H. (1975) The viscera of head and neck. Oral anatomy. p St Louis, MO: CV Mosby. Sirikci, A., Bayazit, Y.A., Bayram, M., et al. (2004) Ethmomaxillary sinus: a particular anatomic variation of the paranasal sinuses. European Radiology 14: Stammberger, H. (1986) Endoscopic endonasal surgery-concepts in treatment of recurring rhinosinusitis. Part I. Anatomic and pathophysiologic considerations. Otolaryngology - Head and Neck Surgery 94: Stammberger, H.R., Kennedy, D.W. (1995) Paranasal sinuses: anatomic terminology and nomenclature. The Anatomic Terminology Group. The Annals of Otology, Rhinology & Laryngology. 167 (Suppl): Tasar, M., Cankal, F., Bozlar, U., Hidir, Y., Saglam, M., Ors, F. (2007) Bilateral maxillary sinus hypoplasia and aplasia: radiological and clinical findings. Dentomaxillofacial Radiology 36: Tatum, H. (1986) Maxillary and sinus implant reconstruction. Dental Clinics of North America 30: Tidwell, J.K., Blijdorp, P.A., Stoelinga, P.J., Brouns, J.B., Hinderks, F. (1992) Composite grafting of the maxillary sinus for placement of endosteal implants. A preliminary report of 48 patients. The International Journal of Oral & Maxillofacial Surgery 21: Timmenga, N., Raghoebar, G.M., Boering, G., et al. (1997) Maxillary sinus function after sinus lifts for the insertion of dental implants. Journal of Oral and Maxillofacial Surgery 5: Tonai, A., Baba, S. (1996) Anatomic variations of the bone in sinonasal CT. Acta Otolaryngologica. 525 (Suppl): Tsiklakis, K., Donta, C., Gavala, S., Karayianni, K., Kamenopoulou, V., Hourdakis, C.J. (2005) Dose reduction in maxillofacial imaging using low dose Cone Beam CT. European Journal of Radiology 56: Ueda, M., Kaneda, T. (1992) Maxillary sinusitis caused by dental implants: report of two cases. Journal of Oral and Maxillofacial Surgery 50: Ulm, C.W., Solar, P., Krennmair, G., Matejka, M., Watzek, G. (1995) Incidence and suggested surgical management of septa in sinus-lift procedures. The International Journal of Oral & Maxillofacial Implants 10: Underwood, A.S. (1910) An inquiry into the anatomy and pathology of the maxillary sinus. Journal of Anatomy & Physiology 44:

36 34 van den Bergh, J.P., ten Bruggenkate, C.M., Disch, F.J., Tuinzing, D.B. (2000) Anatomical aspects of sinus floor elevations. Clinical Oral Implants Research 11: van der Zel, J.M. (2008) Implant planning and placement using optical scanning and cone beam CT technology. Journal of Prosthodontics 17: Velasquez-Plata, D., Hovey, L.R., Peach, C.C., Alder, M.E. (2002) Maxillary sinus septa: a 3-dimensional computerized tomographic scan analysis. The International Journal of Oral & Maxillofacial Implants 17: Wald, E.R. (1993) Radiographics sinusitis: illusion or delusion? The Pediatric Infectious Disease Journal 12: Weed, D.T., Cole, R.R. (1994) Maxillary sinus hypoplasia and vertical dystopia of the orbit. Laryngoscope 104: White, S.C., Pharoah, M.J. (2004) Oral Radiology Principles and Interpretation, 5th edition. St. Louis, MO: Mosby. Zinreich, S.J., Abayram, S., Benson, M.L., Oliverio, P.J. (2003) The ostiomeatal complex and functional endoscopic surgery. In: Som, P.M. & Curtin, H.D., eds. Head and neck imaging, 4th edition, p St. Louis, MO: Mosby. Zinreich, S.J., Kennedy, D.W., Gayler, B.W. (1988) Computed tomography of nasal cavity and paranasal sinuses: an evaluation of anatomy for endoscopic sinus surgery. Clear Images 1:2 10. Zinreich, S.J., Kennedy, D.W., Rosenbaum, A.E., et al. (1987) Paranasal sinuses: CT imaging requirements for endoscopic surgery. Radiology 163:

37 35 Figure 1 - Maxillary sinus pneumatization (a), nasal septum deviation with spur (b), antral septa (c), secondary ostium (d), maxillary sinus hypoplasia (e), exostosis (f), ethmomaxillary sinus (g) and Haller cells (h).

38 36

39 37 Figure 2 Maxillary sinus mucosal thickening <3mm (a) and >3mm (b). Discontinuity of the sinus floor associated to: periapical lesion (c), intra-sinus bone graft (d), implant fenestration (e), tooth extraction (f), endodontic filling material fenestration (g), no apparent cause (h).

40 38

41 39 Figure 3 - Polypoid lesions (a and b), air-fluid level (c), bone thickening of the maxillary sinus wall (d), antrolith (e), discontinuity of the sinus lateral wall (f), sinus opacification (g) and foreign body (h).

42 40

43 41 Table 1 Anatomic variations of the maxillary sinus detected in the 500 CBCT exams evaluated Anatomic variation Characteristics Frequency Pneumatization 1 Total 416 (83.2%) Alveolar (unilateral) 62 Alveolar (bilateral) 354 Tuber (unilateral) 31 Tuber (bilateral) 79 Palatine (unilateral) 34 Palatine (bilateral) 84 Anterior (unilateral) 4 Anterior (bilateral) 22 Nasal septum deviation Total 266 (53.2%) With spur 87 With no spur 179 Visualization not possible 2 29 Antral septa Total 222 (44.4%) Unilateral 121 Bilateral 101 Secondary ostium Total 67 (13.4%) Unilateral 39 Bilateral 28 Visualization not possible Hypoplasia Total 24 (4.8%) Unilateral 19 Bilateral 5 Exostosis Total 13 (2.6%) Unilateral 11 Billateral 9 Ethmomaxillary sinus Total 6 (1.2%) Unilateral 5 Bilateral 1 Visualization not possible Haller cells Total 3 (0.6%) Unilateral 2 Bilateral 1 Visualization not possible Pneumatization sites were multiple in 191 of the 416 cases showing this variation (46%). In 225 cases (54%) the pneumatization was located only in a single site (alveolar). 2 The site of the anatomic variation was out of the image limits.

44 42 Table 2 Lesions of the maxillary sinus detected in the 500 CBCT exams evaluated Lesion Characteristics Frequency Mucosal thickening (>3mm) Total 313 (62.6%) Unilateral 133 Billateral 180 Mucosal thickening (<3mm) Total 274 (54.8%) Unilateral 155 Billateral 119 Polypoid lesion Total 107 (21.4%) Unilateral 87 Billateral 20 Discontinuity of the sinus floor Total 87 (17.4%) Unilateral 61 Bilateral 16 Associated to periapical lesion 25 Associated to bone graft 24 Associated to implant fenestration 20 Associated to tooth extraction 7 Associated to bone graft and implant 3 Associated to endodontic filling material 1 No apparent cause 7 Air-fluid level Total 22 (4.4%) Unilateral 19 Billateral 3 Bone thickening Total 19 (3.8%) Unilateral 18 Billateral 1 Antrolith Total 16 (3.2%) Unilateral 14 Billateral 2 Discontinuity of the sinus lateral wall Total 13 (2.6%) Unilateral 11 Billateral 2 Sinus opacification Total 9 (1.8%) Unilateral 9 Billateral 0 Foreign body Total 8 (1.6%) Unilateral 8 Billateral 0

45 43 APÊNDICE 2: Artigo de série de casos que será submetido ao periódico Quintessence International (Qualis B1) As normas do periódico podem ser acessadas em:

46 44 Bone discontinuity of the maxillary sinus floor: A series of cases detected by cone beam computed tomography for dental implant planning Juliana Pelinsari Lana, DDS, MS 1 2 Pollyanna Moura Rodrigues Carneiro, DDS, MS 1 Vinícius de Carvalho Machado, DDS 2 Paulo Eduardo Alencar de Souza, DDS, MS, PhD 1 Flávio Ricardo Manzi, DDS, MS, PhD 1 Martinho Campolina Rebello Horta, DDS, MS, PhD 1 1 Department of Dentistry, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil 2 Slice Diagnóstico Volumétrico por Imagem, Belo Horizonte, Minas Gerais, Brazil Key words: cone beam computed tomography; dental extraction; dental implants; maxillary sinus; maxillary sinusitis Corresponding author: Martinho Campolina Rebello Horta Pontifícia Universidade Católica de Minas Gerais - Departamento de Odontologia Av. Dom José Gaspar Prédio 45 - Sala 110 Belo Horizonte - MG - Brasil - CEP: Phone: (+55) Fax: (+55) martinhohorta@pucminas.br

47 45 ABSTRACT Objective: To report a series of cases of 87 patients with bone discontinuity of the maxillary sinus floor detected by cone beam computed tomography (CBCT) of the maxilla required for dental implant planning. Method and materials: This case series study evaluated a convenient sample of 87 CBCT exams showing 105 affected maxillary sinuses. The inclusion criteria were CBCT exams of the maxilla required for dental implant planning showing bone discontinuity of the maxillary sinus floor. The following features were assessed: age, gender, cause of the discontinuity, site of the discontinuity, maxillary sinus mucosal thickening, alveolar pneumatization, and sinus opacification. Results: The bone discontinuity of the maxillary sinus floor was caused by periapical lesion in 25 (28.7%) patients, by intra-sinus bone graft in 23 (26.8%), by implant fenestration in 20 (22.9%), by implant fenestration and intra-sinus bone graft in 3 (3.4%), by tooth extraction in 7 (8.0%), and by endodontic filling material fenestration in 1 (1.1%). In 7 (8%) patients, no defined cause was found. In 1 (1.1%) patient, it was caused by intra-sinus bone graft on the right sinus and showed no defined cause in the left sinus. Of the 105 affected sinuses, alveolar pneumatization was identified in 96.2%, mucosal thickening >3mm in 72.4%, and sinus opacification in 11.4%. Conclusion: The bone discontinuity of the maxillary sinus floor is highly associated to dentistry-related causes. Since this condition is an important source of sinus alterations, it should modify the dental treatment planning and must be evaluated and treated by specialized professionals. INTRODUCTION The maxillary sinuses are anatomical structures of great importance in dental practice. 1 Bone discontinuity of the maxillary sinus floor leading to perforation of the Schneiderian membrane is a significant cause of sinusitis. This lesion has been associated to several dentistry-related causes as maxillary teeth periapical inflammation, maxillary dental trauma, dental implant fenestration, dental extractions, maxillary orthognathic surgery, preprosthetic surgery, sinus floor elevation, and sinus grafting. 2,3 The cone beam computed tomography (CBCT) is currently the most used image exam for dental implant planning. 4 CBCT utilizes a coneshaped X-ray beam to

48 46 obtain projection data from a flat detector during a single 360 o rotation, in which a volumetric data set is reconstructed using algorithms similar to those used in conventional computed tomography. This scanner provides adequate images for evaluation of high-contrast structures in the oral and maxillofacial region. 5 The aim of this study was to report a series of cases of 87 patients with bone discontinuity of the maxillary sinus floor detected by CBCT of the maxilla required for dental implant planning. METHOD AND MATERIALS Study design This case series study evaluated a convenient sample of 87 CBCT exams showing 105 affected maxillary sinuses. The CBCT exams were made in a private dental radiology clinic in Belo Horizonte, Brazil, between March and September of The study was approved by the local ethics committee. The following inclusion criteria were applied: 1) CBCT exams of the maxilla; 2) CBCT exams required for implant planning; 3) CBCT exams showing bone discontinuity of the maxillary sinus floor; 4) CBCT exams from patients who accepted to participate in the study. CBCT exams were excluded on the basis of: 1) exams not displaying all the extension of the lower third of the maxillary sinus; 2) presence of technical artifacts that could difficult the evaluation of the maxillary sinus. Image acquisition and analysis The exams were performed by the i-cat cone beam computed tomograph (Imaging Sciences International, Hatfield, PA, USA). The tomograph specifications were: Field of view: 6 cm covering the maxilla region; Voxel: 0.2 mm; Scan time: 40 seconds. Image analysis was performed on the i-cat software, on a multiplanar reconstruction window in which the axial, coronal and sagittal planes could be visualized in 0.2 mm intervals. The CBCT exams were independently evaluated by two authors. Doubtful cases were reanalyzed and a consensus agreed. The following clinical and tomographic features were evaluated: 1) age; 2) gender; 3) cause of the discontinuity of the maxillary sinus floor; 4) site of the

49 47 discontinuity; 5) maxillary sinus mucosal thickening; 6) maxillary sinus alveolar pneumatization; 6) maxillary sinus opacification. RESULTS In a total of 87 CBCT exams, 46 (52.9%) were from male and 41 (47.1%) from female patients. The patient s age range was years, with a median age of 56 years. The causes of bone discontinuity of the maxillary sinus floor and its associated tomographic features are reported in Table 1 and illustrated in Figure 1. The clinical and tomographic features of all the 87 patients are referred in Table 2. The bone discontinuity of the maxillary sinus floor was caused by periapical lesion in 25 (28.7%) patients (Fig 1a and b), by intra-sinus bone graft in 23 (26.8%) patients (Fig 1c), by implant fenestration in 20 (22.9%) patients (Fig 1d), by implant fenestration and intra-sinus bone graft in 3 (3.4%) patients (Fig 1e), by tooth extraction in 7 (8.0%) patients (Fig 1f), and by endodontic filling material fenestration in 1 (1.1%) patient (Fig 1g). In 7 (8%) patients, no defined cause was found (Fig 1h). In 1 (1.1%) case, the discontinuity was caused by intra-sinus bone graft on the right sinus and showed no defined cause in the left sinus. Of the 25 patients showing discontinuity of the maxillary sinus floor caused by periapical lesions, two exhibited bilateral lesions, totaling 27 sinuses. The most identified teeth related to this problem were first molars (51.9%), followed by second molars (40.7%), third molars (3.7%), and first premolars (3.7%). All sinuses showed maxillary sinus mucosal thickening >3mm. Opacification was detected in 5 sinuses (20%) and 25 sinuses (92.6%) demonstrated alveolar pneumatization. In 36 sinuses of 24 patients, the discontinuity was caused by intra-sinus bone graft. Of these sinuses, 23 (63.9%) exhibited mucosal thickening >3mm, 11 (30.6%) mucosal thickened <3mm and 2 (5.6%) no mucosal thickened. Sinus opacification was detected in only 1 sinus (2.8%) and alveolar pneumatization in 35 (97.2%). Regarding the 20 patients who exhibited discontinuity caused by implant fenestration, only one presented bilateral lesion. Of the 21 affected sinuses, 13 (61.9%) demonstrated mucosal thickening >3mm, 7 (33.3%) mucosal thickening <3mm and 1 (4.8%) no mucosal thickening. Maxillary sinus opacification was identified in 2 sinuses (9.5%) and alveolar pneumatization in 20 (91.5%).

50 48 In 3 patients the discontinuity was caused by implant fenestration associated with intra-sinus bone graft. In one of these cases the lesion was bilateral. 50% of the sinuses showed mucosal thickening >3mm and 50% mucosal thickened <3mm. Sinus opacification was not detected. All sinuses displayed alveolar pneumatization. Discontinuity caused by tooth extraction was observed in 7 patients. Of the 8 affected sinuses, 7 (87.5%) showed mucosal thickening >3mm and 1 (12.5%) mucosal thickened <3mm. Sinus opacification was detected in half and alveolar pneumatization in all affected sinuses. The discontinuity of the maxillary sinus floor in 8 sinuses of 8 patients had no defined cause. Mucosal thickening >3mm was identified in 50% and mucosal thickening <3mm was detected in 50% of the sinuses. Sinus opacification was not detected and all sinuses showed alveolar pneumatization. One isolated case demonstrated discontinuity by endodontic filling material fenestration in the upper right first molar. Alveolar pneumatization was identified. No mucosal thickened and no opacification were detected. DISCUSSION At the outset, it is important to emphasize that maxillary sinus alveolar pneumatization was identified in 96.2% of the 105 affected sinuses of this case series. This finding highlights the significance of this anatomic variation as a predisposing factor to bone discontinuity of the maxillary sinus floor. The maxillary sinus is the widest paranasal sinus, pyramidal in shape and displaying great size variability, whereas the average size in adulthood is: base 35 x 35 mm and height 25 mm. 6 The maxillary sinus grows quickly from birth to 3 years and from 7 to 12 years of age. Among 3 and 7 years, it grows slowly. 7 Nonetheless, after 12 years of age, there is no agreement about the time when the maxillary sinus reaches its maximum dimensions. Different results, from 14 to 25 years of age, have been reported. 8 Continued expansion and pneumatization of the maxillary sinus can continue during life in dentate persons, causing inferior displacement of the sinus floor in the direction of the posterior teeth roots. 9 After maxillary tooth loss, pneumatization can progress inferiorly into the alveolar bone of the edentulous space flanked by the remaining teeth. In the completely edentulous individuals, the sinus can enlarge and extend into the alveolar bone, leaving a thin alveolar layer of bone stuck between the sinus and the oral cavity. 9

51 49 Odontogenic sinusitis usually occurs after disruption of the maxillary sinus mucous membrane by conditions as dental infection, tooth extraction, orthognathic surgery, maxillary sinus floor elevation surgery, intra-sinus bone graft, and dental implants. 2,10,11 Lee & Lee (2010) studied 30 patients diagnosed with odontogenic sinusitis and shown that 37% of the cases were related to dental implants, the most common identified cause. 12 Odontogenic sinusitis related to dental implants are more prevalent in patients displaying predisposing factors as sinus pneumatization. 11,13 Even though acute odontogenic infections are extremely common, the incidence of sinusitis associated to these infections is exceptionally low. These odontogenic infections infrequently penetrate directly into the maxillary sinus, probably due to the dense cortical bone of the sinus floor when compared with the lateral wall of the maxilla. 3 The maxillary sinus mucosa is covered by ciliated pseudostratified columnar epithelium, essential to secretion of mucous through the ostium. 14 This mucosa normally shows 1 mm of thickness 1,15 and a mucosal thickening >3mm is usually considered pathologic. 1 The reported prevalence of maxillary sinus mucosal thickening of odontogenic origin varies substantially, ranging from 58% to 78%. Moreover, there is marked variation in the reported occurrence of dental induced clinical sinusitis, ranging from 4.6% to 47%. These disparities reflect not only a lack of consensus regarding diagnostic criteria but also the difficulty of establishing an exact causal relationship in many cases. 16 In this case series, 72.4% of the affected sinuses showed mucosal thickening >3mm, almost certainly caused by the bone discontinuity of the maxillary sinus floor. Moreover, 11.4% displayed sinus opacification. The results revealed that periapical lesions are an important cause of the bone discontinuity of the maxillary sinus floor. All of these cases showed maxillary sinus mucosal thickening >3mm. Sinus mucosal hyperplasia has been previous reported in approximately 80% of patients displaying teeth with periapical inflammatory processes. 17,18 It has been reported that the second molars show the closest anatomic proximity to the maxillary sinus floor, followed by first molars, third molars, second premolars, first premolars, and canines. 19 Nevertheless, the most identified teeth with periapical lesions associated to the sinus floor discontinuity were first molars (51.9%), followed by second molars (40.7%), third molars (3.7%), and first premolars (3.7%).

52 50 In this study, 20 patients exhibited discontinuity caused by implant fenestration. Of the 21 affected sinuses, 13 (61.9%) demonstrated mucosal thickening >3mm, 7 (33.3%) mucosal thickening <3mm and 1 (4.8%) no mucosal thickening. It has been reported that extension of the implants into the maxillary sinus does not play a substantial role in the implant outcome, since osseointegration was described in implants that have entered into the maxillary sinus floor. 20,21 Nevertheless, our results and other studies have described sinus complications associated to implants exposed into the maxillary sinus. It is possible that implant extension into the maxillary sinus may alter its normal function inducing mucosa irritation. 22 Jung et al. (2007) have studied nine patients presenting 23 implants that had been inserted into the maxillary sinus for more than 4 mm without lifting the sinus mucosa. No clinical signs of sinusitis, in any patient, were identified after 6 to 10 months of implant insertion. However, computed tomography exams showed postoperative sinus mucosa thickening around 14 of the 23 implants. 22 Discontinuity by intra-sinus bone graft was detected in 36 sinuses of 24 patients. Of the affected sinuses, 23 (63.9%) exhibited mucosal thickening >3mm and 11 (30.6%) mucosal thickened <3mm. Maxillary sinus floor augmentation is one of the techniques proposed to improve the long-standing retention of dental implants. 23 The grafting techniques are used when the bone height is unsatisfactory to provide implant stability. Complications of the maxillary sinus floor elevation surgery consist mainly of disturbed wound healing, hematoma, bone sequestration, and temporary maxillary sinusitis. 24 The last is considered the major problem of this procedure. 25 Sinusitis in up to 20% of patients after sinus floor augmentation has in fact been reported. 11 The new anatomic relation of the sinus floor in combination with a distended or injured lifted sinus mucosa can affect the maxillary sinus physiology. Furthermore, postoperative edema, hematoma or seroma loading the maxillary sinus can reduce the patency of the ostiomeatal complex, playing a fundamental role in the development of sinusitis. 25 The perforation of the sinus membrane during exodontia is a significant cause of maxillary sinusitis associated with dental procedures, particularly in patients showing tooth roots closeness to the maxillary sinus floor. 3 In fact, the first known formal information concerning the anatomic and clinical significance of the maxillary sinus in dental practice was reported in 1651, describing a case of maxillary sinus infection after the extraction of a superior canine. 26 During tooth extraction,

53 51 substantial forces are placed on the alveolar bone and teeth. Consequently, this process can take away the at times thin bone separating sinus membrane from the oral cavity, resulting in sinus exposure. 3 In this report, discontinuity caused by tooth extraction was found in 7 patients and 8 sinuses, of which 7 (87.5%) showed mucosal thickening >3mm and 1 (12.5%) mucosal thickened <3mm. Further cause of maxillary sinusitis related to dentistry is the perforation of the sinus mucosa by extrusion of endodontic filling materials, particularly in teeth close to the maxillary sinus floor. 3,26 In just one case of this series the discontinuity was caused by endodontic filling material fenestration. Finally, in 8 sinuses of 8 patients it was not possible to define the cause of the maxillary sinus floor discontinuity, based only on the tomographic characteristics. An interesting finding is that all of these cases showed alveolar pneumatization. CONCLUSION The bone discontinuity of the maxillary sinus floor is an important source of sinus alterations and is associated to a number of dentistry-related causes as periapical lesion, intra-sinus bone graft, implant fenestration, tooth extraction, and endodontic filling material fenestration. In addition to modify the dental treatment planning, this condition must be evaluated and treated by specialized professionals, especially if associated to maxillary sinus pathological processes. The CBCT is a suitable exam to diagnose this maxillary sinus lesion. ACKNOWLEDGEMENTS This study was partially supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, Fundação de Amparo à Pesquisa do Estado de Minas Gerais - FAPEMIG, and PUC Minas, Brazil. REFERENCES 1- White SC, Pharoah MJ. Oral Radiology Principles and Interpretation, 5th ed. St. Louis, MO: Mosby, Kretzschmar DP, Kretzschmar JL. Rhinosinusitis: review from a dental perspective. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;96:

54 52 3- Mehra P, Murad H. Maxillary sinus disease of odontogenic origin. Otolaryngol Clin N Am 2004;37: Ludlow JB, Ivanovic M. Comparative dosimetry of dental CBCT devices and 64-slice CT for oral and maxillofacial radiology. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106: Boeddinghaus R, Whyte A. Current concepts in maxillofacial imaging. Eur J Radiol 2008;66: Small SA, Zinner ID, Panno FV, Shapiro HJ, Stein JI. Augmenting the maxillary sinus for implants: report of 27 patients. Int J Oral Maxillofac Implants 1993;8: Graney DO, Rice DH. Anatomy. In: Cummings CW, Fredrickson JM, Harker LA, et al, editors. Otolaryngology head and neck surgery, 3rd ed. St. Louis, MO: Mosby Year Book, 1998: Lee CH, Rhee CS, Oh SJ, et al. Development of the paranasal sinuses in children: an MRI study. Korean J Otolaryngol 2000;43: Sicher H. The viscera of head and neck. Oral anatomy. St Louis, MO: CV Mosby, 1975: Ueda M, Kaneda T. Maxillary sinusitis caused by dental implants: report of two cases. J Oral Maxillofac Surg 1992;50: Timmenga NM, Raghoebar GM, Boering G, vanweissenbruch R. Maxillary sinus function after sinus lifts for the insertion of dental implants. J Oral Maxillofac Surg 1997;55: Lee KC, Lee SJ. Clinical features and treatments of odontogenic sinusitis. Yonsei Med J 2010;51(6): Block MS, Kent JN. Maxillary sinus grafting for totally and partially edentulous patients. J Am Dent Assoc 1993;124: Rodrigues MTV, Munhoz EA, Cardoso CL, Freitas CA, Damante JH. Chronic maxillary sinusitis associated with dental impression material. Med Oral Patol Oral Cir Bucal 2009;14(4): Bailey BJ. Head and Neck Surgery Otolaryngology, 2nd ed. Philadelphia, USA: Lippincott-Raven Publishers,1998: , Melen I, et al. Chronic maxillary sinusitis. Definition, diagnosis and relation to dental infections and nasal polyposis. Acta Otolaryngol 1986;101:

55 53 17-Matilla K. Roentgenological investigations of the relationship between periapical lesions and conditions of the mucous membrane of the maxillary sinuses. Acta Odontologica Scandinavica 1965;23: Matilla K, Altonen MA. A clinical and roentgenological study of apicectomized teeth. Odontologisk Tidskrift 1968;76: Maloney PL, Doku HC. Maxillary sinusitis of odontogenic origin. J Can Dent Assoc 1968; 34: Boyne PJ. Analysis of performance of root-form endosseous implants placed in the maxillary sinus. J Long Term Eff Med Implants 1993;3: Brånemark PI, Adell R, Albrektsson T, Lekholm U, Lindstrom J, Rockler A. An experimental and clinical study of osseointegrated implants penetrating the nasal cavity and maxillary sinus. J Oral Maxillofac Surg 1984;42: Jung JH, Choi BH, Jeong SM, Li J, Lee SH, Lee HJ. A retrospective study of the effects on sinus complications of exposing dental implants to the maxillary sinus cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103: Butz SJ, Huys LWJ. Long-term success of sinus augmentation using a synthetic alloplast: a 20 patients, 7 years clinical report. Implant Dent 2005;14: Timmenga NM, Raghoebar GM, van Weissenbruch R, Vissink A. Maxillary sinusitis after augmentation of themaxillary sinus floor: a report of 2 cases. J Oral Maxillofac Surg 2001;59: Timmenga NM, Raghoebar GM, Liem RSB, vanweissenbruch R, Manson WL, Vissink A. Effects of maxillary sinus floor elevation surgery on maxillary sinus physiology. Eur J Oral Sci 2003;111: Hauman CH, Chandler NP, Tong DC. Endodontic implications of the maxillary sinus: a review. Int Endod J 2002;35:

56 54 Figure 1 Causes of bone discontinuity of the maxillary sinus floor. Periapical lesion (a and b), intra-sinus bone graft (c), implant fenestration (d), implant fenestration and intra-sinus bone graft (e), tooth extraction (f), endodontic filling material fenestration (g), and no defined cause (h).

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