Efeito da correção cirúrgica da retração palpebral superior da

Transcription

Sara Filipa Teixeira Ribeiro
Efeito da correção cirúrgica da retração palpebral superior da orbitopatia
de Graves no contorno e cinética palpebrais
_______________________________________________________________
Effect of surgical correction of Graves upper eyelid retraction in eyelid
contour and kinematics
Porto, 2014
Título: Efeito da correção cirúrgica da retração palpebral superior da
orbitopatia de Graves no contorno e cinética palpebrais
Autor: Ribeiro, Sara Filipa Teixeira
1ª Edição
Ano: 2014
Tiragem: 100 exemplares
ISBN: 978-989-20-4876-5
Dissertação de candidatura ao grau de Doutor apresentada à
Faculdade de Medicina da Universidade do Porto
Orientador:
Professor Doutor Antonio Augusto Velasco e Cruz
Departamento de Oftalmologia, Otorrinolaringologia e Cirurgia de Cabeça e
Pescoço, Faculdade de Medicina de Ribeirão Preto, Universidade de São
Paulo, Brasil.
Co-orientadores:
Professor Doutor Fernando Manuel Mendes Falcão dos Reis
Professor Doutor Amândio António Rocha Dias de Sousa
Departamento de Órgãos dos Sentidos, Faculdade de Medicina, Universidade
do Porto.
Artigo 48, § 3º: "A Faculdade não responde pelas
doutrinas expendidas na dissertação". (Regulamento
da Faculdade de Medicina do Porto, 29 Janeiro de
1931, Decreto-Lei nº 19337).
CORPO CATEDRÁTICO DA
FACULDADE DE MEDICINA DA UNIVERSIDADE DO PORTO
Professores Catedráticos Efetivos
Doutor Alberto Manuel Barros da Silva
Doutor Altamiro Manuel Rodrigues Costa Pereira
Doutor António Albino Coelho Marques Abrantes Teixeira
Doutor António Carlos Freitas Ribeiro Saraiva
Doutor Daniel Filipe Lima Moura
Doutora Deolinda Maria Valente Alves Lima Teixeira
Doutor Francisco Fernando Rocha Gonçalves
Doutora Isabel Maria Amorim Pereira Ramos
Doutor João Francisco Montenegro Andrade Lima Bernardes
Doutor Joaquim Adelino Correia Ferreira Leite Moreira
Doutor José Agostinho Marques Lopes
Doutor José Carlos Neves da Cunha Areias
Doutor José Eduardo Torres Eckenroth Guimarães
Doutor José Henrique Dias Pinto de Barros
Doutor José Manuel Lopes Teixeira Amarante
Doutor José Manuel Pereira Dias de Castro Lopes
Doutor Manuel Alberto Coimbra Sobrinho Simões
Doutor Manuel Jesus Falcão Pestana Vasconcelos
VII
Doutora Maria Amélia Duarte Ferreira
Doutora Maria Dulce Cordeiro Madeira
Doutora Maria Fátima Machado Henriques Carneiro
Doutora Maria Leonor Martins Soares David
Doutor Patrício Manuel Vieira Araújo Soares Silva
Doutora Raquel Ângela Silva Soares Lino
Doutor Rui Manuel Almeida Mota Cardoso
Doutor Rui Manuel Lopes Nunes
VIII
Professores Jubilados e Aposentados
Doutor Abel José Sampaio da Costa Tavares
Doutor Abel Vitorino Trigo Cabral
Doutor Alexandre Alberto Guerra Sousa Pinto
Doutor Álvaro Jerónimo Leal Machado de Aguiar
Doutor Amândio Gomes Sampaio Tavares
Doutor António Augusto Lopes Vaz
Doutor António Carvalho Almeida Coimbra
Doutor António Fernandes da Fonseca
Doutor António Fernandes Oliveira Barbosa Ribeiro Braga
Doutor António Germano Pina Silva Leal
Doutor António José Pacheco Palha
Doutor António Manuel Sampaio de Araújo Teixeira
Doutor Belmiro dos Santos Patrício
Doutor Cândido Alves Hipólito Reis
Doutor Carlos Rodrigo Magalhães Ramalhão
Doutor Cassiano Pena de Abreu e Lima
Doutor Daniel Santos Pinto Serrão
Doutor Eduardo Jorge Cunha Rodrigues Pereira
Doutor Fernando de Carvalho Cerqueira Magro Ferreira
Doutor Fernando Tavarela Veloso
Doutor Francisco de Sousa Lé
IX
Doutor Henrique José Ferreira Gonçalves Lecour de Menezes
Doutor Jorge Manuel Mergulhão Castro Tavares
Doutor José Carvalho de Oliveira
Doutor José Fernando Barros Castro Correia
Doutor José Luís Medina Vieira
Doutor José Manuel Costa Mesquita Guimarães
Doutor Levi Eugénio Ribeiro Guerra
Doutor Luís Alberto Martins Gomes de Almeida
Doutor Manuel António Caldeira Pais Clemente
Doutor Manuel Augusto Cardoso de Oliveira
Doutor Manuel Machado Rodrigues Gomes
Doutor Manuel Maria Paula Barbosa
Doutora Maria da Conceição Fernandes Marques Magalhães
Doutora Maria Isabel Amorim de Azevedo
Doutor Mário José Cerqueira Gomes Braga
Doutor Serafim Correia Pinto Guimarães
Doutor Valdemar Miguel Botelho dos Santos Cardoso
Doutor Walter Friedrich Alfred Osswald
X
JÚRI
Presidente
Doutor José Agostinho Marques Lopes
Professor Catedrático da Faculdade de Medicina da Universidade do Porto
Diretor da Faculdade de Medicina da Universidade do Porto
Vogais
Doutor Antonio Augusto Velasco e Cruz
Professor Catedrático da Universidade de São Paulo
Doutor Carlos Alberto Matinho Marques Neves
Professor Auxiliar Convidado da Faculdade de Medicina da Universidade de
Lisboa
Doutor Manuel do Rosário Caneira da Silva
Professor Auxiliar Convidado da Faculdade de Medicina da Universidade de
Lisboa
Doutor José Paulo Alves Vieira de Andrade
Professor Associado da Faculdade de Medicina da Universidade do Porto
Doutor Jorge Eduardo de Freitas Spratley
Professor Auxiliar Convidado da Faculdade de Medicina da Universidade do
Porto
XI
Ao abrigo do artigo 8.º do Decreto-Lei nº 388/70, fazem parte integrante desta
dissertação os seguintes trabalhos:
- Trabalhos publicados que integram a temática principal da tese
Cruz AA, Ribeiro SF, Garcia DM, Akaíshi PM, Pinto CT. "Graves upper
eyelid retraction." Surv Ophthalmol 2013; 58: 63-76.
Ribeiro SF, Milbratz GH, Garcia DM, Fernandes VL, Rocha-Sousa A,
Falcão-Reis FM, Cruz AA. "Lateral and medial upper eyelid contour
abnormalities in Graves orbitopathy: the influence of the degree of
retraction." Ophthal Plast Reconstr Surg 2013; 29: 40-3.
Wambier SPF, Ribeiro SF, Garcia DM, Brigato RR, Messias A, Cruz
AA. "Two dimensional video analysis of the upper eyelid motion
during spontaneous blinking." Ophthal Plast Reconstr Surg 2014; 30:
146-51.
Ribeiro SF, Milbratz GH, Garcia DM, Devoto M, Neto GH,
Mörschbächer R, Pereira FJ, Cruz AA. "Pre- and postoperative
quantitative analysis of contour abnormalities in Graves upper
eyelid retraction." Ophthal Plast Reconstr Surg 2012; 28:429-33.
Ribeiro SF, Garcia DM, Leal V, Faria-Correia F, Rocha-Sousa A,
Falcão-Reis F, Cruz AA. "Graded müllerectomy for correction of
Graves upper eyelid retraction: effect on eyelid movements."
Ophthal Plast Reconstr Surg 2014; Apr 25 [Epub ahead of print].
Em cumprimento do disposto no referido Decreto-Lei declara que, nos
trabalhos em que é primeira autora, participou ativamente na recolha e no
estudo do material, tendo redigido os textos com a colaboração dos outros
autores. Nos trabalhos em que é segunda autora, colaborou com os outros
XIII
autores no estudo do material, na redação dos textos e na respetiva
documentação.
XIV
LISTA DE ABREVIATURAS
AMEPS - Aponevrose do músculo elevador da pálpebra superior
DMCP - Distância margem palpebral superior - centro pupilar
ITP - Intervalo de tempo entre pestanejos
LED - Díodo emissor de luz infravermelha
LIT - Ligamento intermuscular transverso
LW - Ligamento de Whitnall
MEPS - Músculo elevador da pálpebra superior
MM - Músculo de Müller
mm - Milímetros
MOO - Músculo orbicular do olho
MRD1 - Distância margem-reflexo 1
ms - Milissegundos
OG - Orbitopatia de Graves
º - Grau
PE - Pestanejo espontâneo
TPE - Taxa de pestanejo espontâneo
TRAb - Autoanticorpos anti-recetor da hormona estimulante da tiróide
TSH - Hormona estimulante da tiróide
XV
PREFÁCIO
A atividade de investigação que conduziu à elaboração desta
dissertação de doutoramento decorreu no Hospital das Clínicas de Ribeirão
Preto, Universidade de São Paulo (Brasil) e no Centro Hospitalar de São João,
Faculdade de Medicina da Universidade do Porto. Inicialmente o nosso
trabalho centrou-se na pesquisa bibliográfica, de forma a adquirir todo o
conhecimento científico sobre retração palpebral superior da orbitopatia de
Graves. Verificamos a escassez de estudos relativos à avaliação quantitativa
do contorno palpebral nesta patologia e ao efeito da cirurgia de retração
palpebral superior no contorno e cinética palpebrais.
Tradicionalmente o cirurgião oculoplástico realiza a avaliação do
contorno palpebral de forma subjetiva, e a necessidade de desenvolvimento de
um método capaz de tornar objetiva esta avaliação tem assumido maior
importância nas últimas décadas (Shore 1996). O nosso primeiro objetivo foi
caracterizar quantitativamente as anomalias de contorno induzidas pela
retração
palpebral
superior
nesta
doença.
Este
estudo
permitiu
o
aprofundamento do conhecimento sobre o papel da magnitude da retração
palpebral e da exoftalmometria nas deformidades do contorno da pálpebra
superior secundárias à orbitopatia de Graves. De seguida otimizamos e
aplicamos um método simples, portátil e fiável de quantificação dos
movimentos palpebrais utilizando um sistema de vídeo. Por fim, investigamos o
efeito da correção cirúrgica da retração palpebral superior no contorno e
cinética palpebrais.
XVII
Para a elaboração desta dissertação de doutoramento contribuíram
diversas pessoas às quais, ciente da limitação das palavras, deixo os meus
sinceros agradecimentos.
Ao Sr. Prof. Doutor Antonio Augusto Velasco e Cruz, orientador não só
desta tese, mas também do meu fellowship clínico, cirúrgico e de investigação
de "Oculoplástica, Vias Lacrimais e Órbita". Pela forma como me recebeu no
Hospital das Clínicas de Ribeirão Preto, Universidade de São Paulo, Brasil.
Pelo exemplo de competência clínica e científica, por estimular o conhecimento
e o interesse pela vida académica, pela disponibilidade permanente e pelo
apoio ao longo dos anos. Pelas ideias, críticas, correções e sugestões. Sou
grata por todos esses ensinamentos e pela sua amizade.
Ao Sr. Prof. Doutor Fernando Falcão-Reis, co-orientador desta tese,
pelos conhecimentos transmitidos, pelo seu empenho e pelas condições que
criou para que a concretização dos projetos fosse possível. Agradeço-lhe por
ter confiado e acreditado que eu seria capaz de superar este desafio.
Ao Sr. Prof. Doutor Amândio Rocha-Sousa, co-orientador desta tese,
pelo apoio, disponibilidade e por estimular o interesse pela atividade científica.
Demonstro a minha gratidão por ter aceite a co-orientação desta dissertação.
A todos os meus Professores da Faculdade de Medicina da
Universidade do Porto, que de uma forma ou de outra marcaram a minha vida
académica e pessoal. Um agradecimento muito especial ao Sr. Prof. Doutor
Pedro von Hafe, meu padrinho de curso; há momentos, como este, em que nos
sentimos inquietos com as palavras porque se tornam insuficientes para
expressar tão grande admiração e gratidão.
XVIII
Ao colega de laboratório e amigo Denny Garcia, agradeço o empenho, a
disponibilidade, a colaboração nos artigos científicos e os conhecimentos
transmitidos. O Denny desenvolveu o software para análise do contorno
palpebral e o sistema de vídeo para avaliação dos movimentos palpebrais. Foi
elemento fundamental em todos os trabalhos integrantes desta tese.
Ao Dr. Vítor Leal, com quem trabalho na Secção de Órbita do Centro
Hospitalar de São João, pelo incentivo, pela disponibilidade e ajuda constante.
Demonstro a minha profunda gratidão pelo seu empenho neste trabalho. Foi
um colaborador excelente nos trabalhos experimentais e científicos.
À Prof. Doutora Patrícia Akaíshi pela paciência, pelas palavras de
entusiasmo e incentivo. Pelos conhecimentos clínicos e científicos transmitidos.
Aos meus colaboradores e grandes amigos da Universidade de São
Paulo: Afra Bernardes, Gherusa Milbratz, Sarah Wambier, Carolina Pinto,
Veridiana Puppio, Ana Karina, Adriano Baccega e Rodrigo Espírito Santo.
À Dra. Ana Paula Pina e ao Dr. Sérgio Estrela Silva pela amizade e pelo
apoio. Substituíram-me inúmeras vezes nas funções desempenhadas no
Centro Hospitalar de São João. Sem eles tudo teria sido muito mais difícil.
Ao Dr. Ricardo Dias pelos seus ensinamentos e interesse demonstrado
pelos meus trabalhos.
Aos meus colegas e amigos do Serviço de Oftalmologia do Centro
Hospitalar de São João e do Hospital da Clínicas de Ribeirão Preto pelo apoio
e incentivo.
XIX
Aos voluntários que aceitaram participar neste estudo, como controles e
como pacientes. Foram essenciais para que esta tese fosse realizada.
Aos meus pais e avós pelo apoio, carinho e disponibilidade que sempre
me dispensaram. Por compreenderem os longos períodos de ausência e me
fazerem acreditar que conseguiria vencer este desafio. A pessoa que hoje sou
a eles se deve.
Ao meu irmão Tiago e à minha cunhada Manuela pelo incentivo e pela
felicidade e orgulho com que sempre reagiram aos avanços em todas as áreas
da minha vida.
Ao Fernando por entender, acreditar e incentivar as minhas escolhas.
Pelo amor, carinho, paciência e ajuda nos momentos mais difíceis.
Ao Dr. Horácio Correia e à Dra. Elza Faria Correia pela sua
preocupação, amizade e carinho. Por me terem recebido na sua família e me
apoiarem na minha vida pessoal e profissional.
Aos restantes familiares e amigos, agradeço a amizade, o entusiasmo
colocado nos meus trabalhos e o incentivo presente nas suas palavras. Uma
palavra especial aos que me acompanham mais de perto: Célia Xavier, Ana
Luísa Neves, Sofia Fonseca, Catarina Eloy, Francisco Serdoura, Ricardo
Ribeiro, Rita Cruz, Elsa Neves, Ana Duarte, Tiago Ramos, Vítor Araújo, Dr.
Fernando Parada, Adelaide Almeida, Belmira Teixeira e Teresa Marques.
XX
ÍNDICE
Capítulo I - Introdução Geral e Objetivos ....................................................... 3
1. Estrutura anatomofuncional da pálpebra superior ...................................... 5
1.1. Elementos anatómicos da dinâmica e contorno palpebrais .................. 5
1.1.1. Músculo orbicular do olho ............................................................... 6
1.1.2. Estrutura tarsoligamentar ............................................................... 7
1.1.3. Retratores palpebrais ..................................................................... 8
1.1.4. Ligamento de Whitnall .................................................................. 11
1.1.5. Contorno palpebral ....................................................................... 13
1.2. Movimentos Palpebrais....................................................................... 17
1.2.1. Movimento persecutório palpebral ................................................ 17
1.2.2. Movimento sacádico palpebral ..................................................... 18
1.3.3. Pestanejo...................................................................................... 18
1.2.3.1. Pestanejo espontâneo ............................................................ 19
1.3. Métodos de medição dos movimentos palpebrais .............................. 19
1.3.1 Magnetic Search Coil..................................................................... 20
1.4 Cinética Palpebral ................................................................................... 23
1.4.1. Forças ativas e passivas intervenientes no movimento da pálpebra
superior durante o pestanejo e os movimentos sacádicos palpebrais .... 23
1.4.2. Parâmetros de avaliação cinética ................................................. 26
1.4.2.1. Amplitude e velocidade máxima ............................................. 26
1.4.2.2. Main sequence: relação entre amplitude, velocidade máxima e
duração ............................................................................................... 28
1.4.2.3. Taxa de pestanejo espontâneo .............................................. 29
1.4.2.4. Distribuição dos intervalos de tempo entre pestanejos .......... 32
1.5. Orbitopatia de Graves ......................................................................... 33
1.5.1 Retração palpebral superior .......................................................... 42
Capítulo II - Anomalias de contorno induzidas pela retração palpebral
superior da orbitopatia de Graves ................................................................ 59
Capítulo III – Validação de um sistema de vídeo digital como método de
registo e quantificação dos movimentos palpebrais .................................. 65
Capítulo IV - Efeito da correção cirúrgica da retração palpebral superior
no contorno palpebral ................................................................................... 73
Capítulo V - Efeito da correção cirúrgica da retração palpebral superior
(por müllerectomia via posterior) na cinética palpebral ............................. 81
Capítulo VI - Discussão Global e Conclusões ............................................. 89
Capítulo VII - Resumo .................................................................................. 111
Capítulo VIII - Abstract ................................................................................. 115
Capítulo IX - Bibliografia.............................................................................. 119
2
Capítulo I - Introdução Geral e Objetivos
______________________________
Introdução Geral e Objetivos
A semiologia oculoplástica depende, em grande parte, de medidas
orbito-palpebrais obtidas no exame físico. Para que estas medições sejam
efetuadas de forma correta é necessário que o examinador conheça a
anatomia das estruturas analisadas e compreenda os fatores fisiológicos
condicionantes dos padrões de normalidade das medidas clínicas (Hanada, de
Souza, Moribe and Cruz 2001; Schellini, Sverzut, Hoyama, Padovani and Cruz
2006; van den Bosch, Leenders and Mulder 1999).
1. Estrutura anatomofuncional da pálpebra superior
1.1. Elementos anatómicos da dinâmica e contorno palpebrais
As pálpebras são estruturas complexas cuja função principal é manter a
integridade do globo ocular. Este papel protetor é basicamente função das
propriedades motoras palpebrais, que além de ocluírem a fenda palpebral em
situações de risco (pestanejo reflexo), distribuem o filme lacrimal sobre a
superfície ocular, humedecendo-a (pestanejo espontâneo) (Owens and Phillips
2001; Palakuru, Wang and Aquavella 2007). A pálpebra superior é mais móvel
que a inferior (Leite, Cruz, Messias and Malbouisson 2006), cobrindo a maior
parte da superfície ocular durante o seu movimento. Por este motivo, tem
grande importância no estudo da dinâmica palpebral (Evinger, Manning and
Sibony 1991).
Para melhor compreensão dos estudos descritos nesta tese, é
necessário descrever as estruturas presentes na pálpebra superior. Estas
estruturas condicionam o contorno palpebral e são as responsáveis por gerar
os movimentos palpebrais ou têm influência direta ou indireta na dinâmica dos
5
seus movimentos. As informações sobre este assunto foram, em grande parte,
retiradas
do
clássico
livro
de
Whitnall
(Whitnall
1932).
Referências
complementares serão citadas no decorrer deste capítulo.
Na clínica, é comum dividir a estrutura palpebral em duas lamelas: a
anterior e a posterior (Nerad 2001). A lamela anterior é constituída pela pele e
músculo orbicular do olho (MOO) e a posterior pelo tarso e conjuntiva. Entre as
duas lamelas, há ainda, o septo orbitário e os elementos retratores, que no
caso da pálpebra superior são a aponevrose do músculo elevador da pálpebra
superior (AMEPS) e o músculo de Müller (MM) (Figura 1).
Figura 1 - Corte sagital da pálpebra superior evidenciando as estruturas presentes nas duas lamelas palpebrais
(Dutton, Gayre and Proia 2007).
1.1.1. Músculo orbicular do olho
O MOO faz parte do conjunto de músculos responsáveis pela mímica
facial. A contração destes músculos controla movimentos específicos da face
como o das pálpebras, nariz, boca e determina a expressão facial (Gray 1995).
6
O MOO é um músculo facial complexo, inervado pelo VII nervo craniano
(nervo facial) e a sua contração é responsável pelo encerramento da fenda
palpebral. Embora seja uma estrutura contínua, é geralmente dividido em
relação ao rebordo orbitário em porção orbitária e porção palpebral (Figura 2).
A parte palpebral é denominada, de acordo com as estruturas com as quais se
relaciona, em pré-septal e pré-tarsal; está relacionada com o pestanejo e o
encerramento palpebral voluntário. A porção orbitária é periférica e está
relacionada com o encerramento voluntário forçado (Lander, Wirtschafter and
McLoon 1996; Schmidtke and Buttner-Ennever 1992).
Figura 2 - Músculo orbicular do olho, mostrando as suas divisões (Dutton 1994).
1.1.2. Estrutura tarsoligamentar
O tarso é um importante elemento estrutural da pálpebra superior. Mede,
em média, 25 milímetros (mm) horizontalmente e 8 a 12 mm verticalmente. É
composto por uma densa placa de tecido fibroelástico, localizada abaixo da
porção pré-tarsal do MOO. A placa tarsal superior está inserida no rebordo
7
orbitário por meio de ligamentos ou tendões cantais (lateral e medial) (Figura
3). O conjunto é denominado estrutura tarsoligamentar, sendo responsável pelo
suporte, estabilidade e elasticidade palpebral durante o movimento e em
repouso (Kuwabara, Cogan and Johnson 1975; Sisler 1973).
A estrutura tarsoligamentar é muito importante na génese dos
movimentos da pálpebra superior, pois durante o estado de vigília, com os
olhos abertos, ela é deformada pelo tónus do músculo elevador da pálpebra
superior (MEPS), o que permite o armazenamento de certa quantidade de
energia potencial (Evinger, Manning and Sibony 1991).
Figura 3 - Estrutura tarsoligamentar da pálpebra superior (Dutton 2011).
1.1.3. Retratores palpebrais
Na pálpebra superior existem dois músculos responsáveis pela elevação
(retração) da pálpebra: o MEPS e o MM. O músculo frontal, inervado pelo VII
nervo craniano, exerce uma ação elevadora acessória. A sua ação faz-se
notar, principalmente, nas blefaroptoses importantes suprindo parcialmente a
8
hipofunção do MEPS, sendo evidenciada por um intenso pregueamento da
região frontal e arqueamento do supracílio (Cruz 1997).
O MEPS é o principal retrator da pálpebra superior. Trata-se de um
músculo estriado, inervado pelo III nervo craniano (oculomotor) e composto de
fibras de contração rápida. Origina-se de um pequeno tendão sobreposto aos
tendões do músculo reto superior e oblíquo superior no ápice da órbita, logo
acima do anel tendinoso de Zinn. A partir deste ponto projeta-se anteriormente
entre o teto da órbita e o músculo reto superior até o rebordo orbitário, na
região do ligamento de Whitnall (LW), onde passa a dirigir-se no sentido
anteroinferior e as suas fibras sofrem transição gradual de musculares para
aponevróticas (Collin, Beard and Wood 1978; Dutton 1994; Jones 1964).
A
AMEPS
é
uma
estrutura
fibroelástica
que
se
estende
anteroinferiormente até ao bordo superior do tarso, onde gradualmente se
divide em duas inserções: as fibras anteriores inserem-se nos septos
intermusculares das fibras do MOO e as posteriores, mais espessas, dirigemse inferiormente e inserem-se na superfície anterior do tarso. Além das
inserções palpebrais, a AMEPS expande-se, em forma de leque constituindo os
cornos lateral e medial (Figura 4) que se inserem no rebordo orbitário. O corno
medial passa sobre a bainha do tendão do músculo oblíquo superior, fundindose com a porção posterior do ligamento cantal medial e fibras do septo
orbitário. O corno lateral é mais espesso que o medial e passa através da
glândula lacrimal, dividindo-a em lobos palpebral e orbitário, inserindo-se,
então, no bordo superior do ligamento cantal lateral e periórbita do tubérculo
orbitário (Anderson and Beard 1977).
9
Figura 4 - Corte frontal das relações anatómicas do músculo elevador da pálpebra superior (Dutton 2011).
O outro músculo responsável pela elevação da pálpebra superior é o
MM ou músculo tarsal superior. Trata-se de um músculo liso, involuntário,
inervado pelo sistema nervoso autónomo (Sistema Nervoso Simpático). O MM
tem cerca de 10 mm de comprimento e origina-se na face profunda do MEPS,
ao nível do LW; apresenta-se firmemente aderido à conjuntiva subjacente e
insere-se no bordo superior do tarso (Kuwabara, Cogan and Johnson 1975). O
MM apresenta portanto estreita relação com a AMEPS, ocorrendo um
entrelaçamento das suas fibras (Berke and Wadsworth 1955). Tem o papel de
elevar a pálpebra superior 2 a 3 mm, em condições fisiológicas (Beard 1985).
10
Figura 5 - Representação anatómica do músculo de Müller (Dutton 1994).
1.1.4. Ligamento de Whitnall
O LW pode ser descrito como uma espessa condensação fibrosa, vista
como uma linha branca no limite entre o MEPS e a sua aponevrose (Dutton
1989; Whitnall 1910). Estende-se da parede lateral da órbita, onde está fundida
com a cápsula da glândula lacrimal e periósteo lateral, até à parede medial da
tróclea (Codere, Tucker and Renaldi 1995).
A função exata do LW é controversa. Classicamente é atribuída a este
ligamento uma função de suporte superior da órbita, funcionando como um
ponto de apoio fixo onde se altera a direção da força do MEPS (de
anteroposterior para vertical) (Anderson 1985; Anderson and Dixon 1979;
Anderson, Jordan and Dutton 1990). Este conceito defende que o ligamento
seria uma estrutura importante na elevação da pálpebra superior e que,
portanto, nunca deveria ser cortado na cirurgia da ptose (Anderson 1985;
Anderson and Dixon 1979; Anderson, Jordan and Dutton 1990).
11
No entanto, estudos recentes demonstram
que o conceito do LW como uma estrutura fixa
e ponto onde se modifica o vetor de ação do
MEPS não parece ser correto. A ressonância
magnética nuclear e as disseções anatómicas
indicam que a conexão entre o LW e a
periórbita, do teto da órbita, é indireta e
mediada por uma cápsula de gordura préFigura 6 - Músculo elevador da pálpebra
superior (MEPS) entre o ligamento de
Whitnall (LW) e o ligamento intermuscular
transverso (setas) (Lukas, Priglinger, Denk and
Mayr 1996).
aponevrótica (Nemoto 1996); que o ligamento
não é fixo e se move seguindo os movimentos
sacádicos verticais do olho (Goldberg, Wu,
Jesmanowicz and Hyde 1992); e que o
ligamento está situado anteriormente ao ponto
onde se modifica o vetor de ação do MEPS,
não sendo responsável pelo movimento curvo
do músculo (Ettl, Zonneveld, Daxer and
Koornneef 1998).
O ligamento intermuscular transverso
(LIT) (Lukas, Priglinger, Denk and Mayr 1996),
Figura 7 - Ligamento intermuscular
transverso (LIT) separado do músculo
elevador da pálpebra superior (MEPS) que se
encontra
levantado.
Conexões
entre
ligamento de Whitnall e ligamento
intermuscular transverso (setas) (Lukas,
Priglinger, Denk and Mayr 1996).
também descrito como o componente inferior
do
LW,
considerar
é
uma
na
estrutura
discussão
importante
da
função
a
do
ligamento (Codere, Tucker and Renaldi 1995).
O LIT é uma banda de tecido fibroelástico grande, espessa, de forma
trapezóide, localizada entre o reto superior e o MEPS, ligeiramente posterior ao
12
LW (Ettl, Priglinger, Kramer and Koornneef 1996; Ettl, Zonneveld, Daxer and
Koornneef 1998; Lukas, Priglinger, Denk and Mayr 1996). Estende-se
transversalmente a partir da parede lateral, sob o lobo orbitário da glândula
lacrimal (Kakizaki, Zako, Nakano, Asamoto, Mito and Iwaki 2005), até à parte
posterior da tróclea. Funde-se com o LW perto das inserções medial e lateral,
formando uma luva para o MEPS (Codere, Tucker and Renaldi 1995; Lukas,
Priglinger, Denk and Mayr 1996). Estudos anteriores demonstraram claramente
que o MEPS é suportado por uma manga móvel com um forte componente
inferior ao invés de apenas um único ligamento (Codere, Tucker and Renaldi
1995; Ettl, Zonneveld, Daxer and Koornneef 1998; Lukas, Priglinger, Denk and
Mayr 1996).
1.1.5. Contorno palpebral
Na posição primária do olhar, a fenda palpebral é delimitada no sentido
vertical pelas margens palpebrais superior e inferior, e no sentido horizontal
pela união das margens nos cantos lateral e medial.
O contorno da pálpebra superior, visto de uma forma bidimensional, tem
uma forma parabólica (Malbouisson, Baccega and Cruz 2000). Esta forma
deve-se à contração tónica do MEPS na posição primária do olhar, que
deforma o sistema tarsoligamentar para cima e à presença do globo ocular
(Malbouisson, Cruz, Messias, Leite and Rios 2005).
A medição do posicionamento palpebral superior tem sido objeto de
discussão. Inicialmente, a posição palpebral era determinada pelo tamanho
vertical da fenda palpebral, que em indivíduos normais é cerca de 9 mm (Cruz
and Baccega 2001; Fox 1966; Lam, Lam and Walls 1995). No entanto, a
13
quantificação do diâmetro vertical da fenda palpebral não pode ser assumido
como uma medida válida do posicionamento superior, pois esta medida inclui
uma eventual posição anómala da pálpebra inferior. O aumento do tamanho
vertical da fenda palpebral pode determinar retração da pálpebra superior, da
inferior ou de ambas. Uma situação de ptose palpebral superior e retração da
pálpebra inferior pode apresentar tamanho vertical da fenda considerado
normal. Por isso, foi proposto que o posicionamento da pálpebra superior fosse
definido pela medida da distância entre o bordo palpebral superior e o eixo
visual (eixo teórico que une a fovéola ao objeto de fixação) (Sarver and
Putterman 1985). A localização do eixo visual na córnea acontece quando o
olhar é fixado num estímulo luminoso. Este é refletido na superfície anterior da
córnea, efeito conhecido como imagem de primeira ordem de Purkinge (Uozato
and Guyton 1987). O reflexo na córnea é a imagem direta e especular da fonte
luminosa. A medida da distância entre esta imagem e a margem palpebral
superior na posição de 12 horas (90º) é denominada de distância margemreflexo 1 (em inglês, margin reflex distance 1 ou MRD1) (Chalfin and Putterman
1979; Lelli, Duoung and Kazim 2010; Sarver and Putterman 1985). A medição
da distância do reflexo luminoso à margem palpebral superior é equivalente, na
prática, à quantificação da distância entre a margem palpebral superior e o
centro da pupila (DMCP) (Small 1988; Small, Sabates and Burrows 1989).
A DMCP é usualmente medida na posição primária do olhar, com uma
régua milimétrica. Quantificações mais precisas são possíveis com recurso a
imagens digitais e utilização de técnicas computorizadas de processamento de
imagem (Cruz, Coelho, Baccega, Lucchezi, Souza and Ruiz 1998).
14
Figura 8 - Medida da distância da margem palpebral superior ao centro pupilar do olho direito, usando o programa
Image J. A linha vermelha possibilita a conversão de pixels em milímetros.
Os valores da MRD1 variam com a idade e em diferentes grupos étnicos
(Murchison, Sires and Jian-Amadi 2009; Paiva, Minare-Filho and Cruz 2001).
Valores anormalmente baixos caracterizam a ptose palpebral (Small, Sabates
and Burrows 1989), enquanto valores anormalmente altos caracterizam a
retração palpebral (Small 1988). As medidas de DMCP obtidas servem para
estabelecimento do diagnóstico (Edwards, Bartley, Hodge, Gorman and
Bradley 2004) e para quantificação do resultado do tratamento (Costa, Saraiva,
Pereira, Monteiro and Matayoshi 2009; Putterman and Urist 1972).
Considerando
a
importância
da
medida
da
MRD1
na
análise
morfométrica da fenda palpebral, outras questões levantam preocupação
(Shore 1996). Com a MRD1, a altura da porção central da pálpebra, pode ser
precisamente quantificada. Porém não nos transmite qualquer informação em
relação ao contorno palpebral como a presença de picos e depressões não
centrais nas pálpebras, as quais podem caraterizar um contorno anómalo.
Na literatura, as deformidades de contorno são abordadas desde a
década de 50, quando Berke e Johnson publicaram as suas séries de doentes
submetidos a cirurgia da ptose congénita (Berke 1945; Johnson 1954). Estas
15
anomalias têm sido identificadas subjetivamente, por meio da análise do
paciente pelo observador ou registo de imagens (Shore 1996). Sendo esta
abordagem
qualitativa
caracterizada
pela
sua
subjetividade,
tornou-se
necessário o desenvolvimento de um método de análise quantitativa do
contorno palpebral que permita objetivar esta avaliação. Esta abordagem
melhora a análise das anomalias do contorno e orienta condutas cirúrgicas.
Recentemente, foi publicado um novo método de medição do contorno
palpebral que consiste na utilização de um software para análise da imagem da
fenda palpebral (Milbratz, Garcia, Guimaraes and Cruz 2012). O princípio é o
mesmo da DMCP; porém, além de fornecer a medida central, na posição das
12 horas, o uso do software fornece múltiplas DMCPs, radiais com origem no
centro da pupila, intervalados entre si de 15 graus (º) (figura 9). A interseção
destes raios com a margem palpebral fornece os valores angulares de DMCP,
e análises quantitativas do contorno palpebral podem ser feitas a partir destes
valores.
Figura 9 - Método de quantificação do contorno palpebral (Milbratz, Garcia, Guimaraes and Cruz 2012). Esquerda:
linhas representativas das distâncias angulares entre a margem palpebral superior e o centro pupilar intervaladas
entre si de 15 graus. Direita: gráfico polar representativo do contorno palpebral.
16
1.2. Movimentos Palpebrais
Os movimentos da pálpebra superior resultam de forças passivas e
ativas. As forças que tendem a manter a fenda palpebral aberta são todas
forças ativas, e são exercidas, principalmente, pelos músculos retratores, ou
seja, o MEPS, o MM e o músculo frontal (Cruz 1997).
A descida da pálpebra superior é promovida por forças ativas e
passivas. As forças ativas são representadas, principalmente pela atividade do
MOO, enquanto as forças passivas são representadas pelo relaxamento da
estrutura tarsoligamentar, pela relação entre as pálpebras e o globo ocular e
pela força da gravidade (Evinger, Manning and Sibony 1991).
Os movimentos palpebrais, podem-se distinguir em dois tipos de
movimentos: os que acompanham os movimentos oculares, como o sacádico e
o movimento persecutório palpebral; e os que não acompanham os
movimentos oculares como o pestanejo (Becker and Fuchs 1988).
1.2.1. Movimento persecutório palpebral
O movimento persecutório ocorre quando há fixação foveal contínua de
um objeto que se move com uma velocidade constante (Evinger and Fuchs
1978).
Os
movimentos
palpebrais
que
acompanham
os
movimentos
persecutórios oculares no meridiano vertical são chamados movimentos
persecutórios palpebrais (Evinger and Fuchs 1978; Falcão, Malbouisson, Cruz
and Messias 2008).
17
1.2.2. Movimento sacádico palpebral
Os
movimentos
sacádicos
oculares
são
movimentos
rápidos
desencadeados pela mudança de fixação foveal (Becker and Fuchs 1988;
Evinger, Manning and Sibony 1991). O termo "sacádico palpebral" foi instituído
por Becker e Fuchs em 1988, quando demonstraram que durante a
movimentação ocular (supra e infraversão) as pálpebras se movem no mesmo
sentido, com duração e velocidade semelhantes (Becker and Fuchs 1988).
Os movimentos sacádicos palpebrais podem ser divididos em dois tipos:
os ascendentes, que acompanham as rotações oculares para cima
(supraversão), e os descendentes associados à infraversão. Os movimentos
sacádicos da pálpebra superior são gerados pela ação de um único músculo, o
MEPS (Fuchs, Becker, Ling, Langer and Kaneko 1992).
1.3.3. Pestanejo
O pestanejo é o ato de abrir e fechar as pálpebras de uma forma
coordenada e extremamente rápida. Esse movimento representa o meio
encontrado pelo organismo de proteger o olho e concomitantemente manter o
sistema visual em contato com o ambiente o maior tempo possível (Nakamori,
Odawara, Nakajima, Mizutani and Tsubota 1997).
O pestanejo é comumente dividido em voluntário e involuntário (Evinger,
Manning and Sibony 1991; Ponder and Kennedy 1928). O pestanejo voluntário
é um ato consciente, acompanhado simultaneamente pela ativação das
porções palpebral e orbitária do MOO (Kirkwood 2006). O pestanejo
involuntário divide-se em reflexo e espontâneo. O pestanejo reflexo é um
fenómeno generalizado em mamíferos e reflete uma resposta rápida a
18
estímulos externos, de curta duração, tais como visuais, auditivos, táteis e
elétricos na região da face (Evinger, Manning and Sibony 1991). O pestanejo
espontâneo (PE) é um movimento simétrico e coordenado de ambas as
pálpebras superiores, que ocorre de forma inconsciente, transitória e rápida, na
ausência de qualquer estímulo evidente (Cruz, Garcia, Pinto and Cechetti
2011). Este tipo de movimento é essencial para uma melhor qualidade de visão
e para a distribuição e estabilidade do filme lacrimal sobre a superfície ocular
(Cruz, Garcia, Pinto and Cechetti 2011).
1.2.3.1. Pestanejo espontâneo
O PE é o tipo de pestanejo mais frequente, tendo sido alvo de estudo em
trabalhos de investigação descritos nesta tese.
O PE é controlado por estruturas pré-motoras situadas no tronco
cerebral, altamente influenciadas pela atividade dopaminérgica (Esteban, Traba
and Prieto 2004) e por estruturas corticais como o córtex visual e a
circunvolução frontal medial (Yoon, Chung, Song and Park 2005). A taxa de PE
reflete uma complexa interação entre influências periféricas mediadas pela
superfície
ocular
e
a
atividade
dopaminérgica
central.
É,
portanto,
extremamente variável e influenciada por fatores intrínsecos e extrínsecos,
como idade, alterações da superfície ocular, stress, doenças psiquiátricas,
entre outros (Cruz, Garcia, Pinto and Cechetti 2011).
1.3. Métodos de medição dos movimentos palpebrais
Diversas técnicas têm sido utilizadas para medir a taxa de PE e a
cinética da pálpebra superior durante o pestanejo. Não é fácil medir um
19
movimento tão rápido, que dependendo da sua amplitude pode ser concluído
em menos de 100 milissegundos (ms). Cada método tem as suas vantagens e
desvantagens, ficando a decisão pela utilização de um deles fortemente
dependente do objeto de estudo (Cruz, Garcia, Pinto and Cechetti 2011).
Os primeiros sistemas utilizaram métodos mecânicos em que um "braço
elevador" era anexado à pálpebra e conectado a um dispositivo capaz de
registar o seu movimento (Kennard and Glaser 1964; Ponder and Kennedy
1928; Vandermeer and Amsel 1952). Os avanços na tecnologia de hardware e
software impulsionaram o desenvolvimento de técnicas mais sofisticadas tais
como eletro-oculografia dinâmica (Denney and Denney 1984; Stern, Walrath
and Goldstein 1984), eletromiografia (Gehricke, Ornitz and Siddarth 2002),
vídeo (Tsubota, Hata, Okusawa, Egami, Ohtsuki and Nakamori 1996), díodo
emissor de luz infravermelho (LED) (Orlowska-Majdak, Kolodziejski, Dolecki
and Traczyk 2001), optoeletrónico (Sforza, Rango, Galante, Bresolin and
Ferrario 2008) e o magnetic search coil (Garcia, Messias, Costa, Pinto,
Barbosa and Cruz 2010; Guitton, Simard and Codere 1991; Remmel 1984;
Robinson 1963), as quais estão disponíveis atualmente.
1.3.1 Magnetic Search Coil
Dentre os métodos mais utilizados destaca-se o magnetic search coil.
Foi desenvolvido por Robinson em 1963 (Robinson 1963) com o objetivo de
medir os movimentos oculares. Quando comparado com os outros métodos
este tem maior resolução, boa linearidade e baixo ruído (Remmel 1984;
Remmel 2006). Basicamente, o sistema é composto por 3 pares de bobinas
quadradas que formam um cubo, onde cada par gera um campo magnético
20
oscilante em 48, 60 e 80 quilo-hertz, respetivamente, para permitir a separação
dos componentes X, Y e Z (Figura 10 A). Por se tratar de um campo magnético
oscilante, uma bobina imersa nesse campo fica sujeita a uma corrente
induzida, segundo a Lei de indução de Faraday (Nussenzveig 2007). A
variação angular dessa bobina em relação ao campo magnético altera a
quantidade de linhas de campo (fluxo) que atravessa a bobina. O sinal gerado
é, portanto, proporcional ao ângulo da bobina com respeito às linhas de campo
magnético (Figura 10 B).
A
B
1
2
z
x
y
3
z
y
Figura 10 - A) Estrutura metálica cúbica composta pelos três pares de bobinas que geram campos magnéticos
oscilantes nas frequências de 48, 60 e 80 quilo-hertz. Uma bobina imersa nesse campo tem uma corrente induzida
devido à Lei de Faraday. B) Considerando apenas o eixo vertical (Z), na posição 1, o fluxo é máximo. Com a variação
angular da bobina em relação ao campo magnético há a diminuição do fluxo e consequente diminuição do sinal
produzido na bobina.
No início dos anos 90, este método passou a ser utilizado para medir
a dinâmica da pálpebra superior, tornando-se método padrão (Evinger,
Manning and Sibony 1991; Guitton, Simard and Codere 1991). Para essa
finalidade, utiliza-se apenas o componente vertical (Z). Sucintamente, o sujeito
é posicionado dentro da estrutura metálica e a sua cabeça é estabilizada numa
21
mentoneira. Uma pequena bobina é fixada próxima à margem da pálpebra
superior e acima da pupila (Figura 11).
Figura 11. Magnetic Search Coil. Estrutura metálica cúbica com apoio para o queixo onde será posicionado o sujeito
(A). Pequena bobina de cobre esmaltado (B) fixa na parte central da região pré-tarsal da pálpebra superior (C).
Devido à rotação que a pálpebra executa sobre a superfície ocular
durante o movimento do pestanejo, é possível medir o deslocamento da
pálpebra, em graus, tal como é representado na figura 12 através de um fator
de calibração de volt para graus. Esta mostra o registo de dois movimentos de
pestanejo. Cada ponto representa um registo de posição da pálpebra superior
numa amostra de 200 imagens por segundo. As setas vermelhas indicam início
e término do movimento e a amplitude é representada como a excursão
22
máxima realizada pela pálpebra. A distância temporal entre os picos forma o
intervalo entre pestanejos.
Figura 12 - Representação do registo do movimento palpebral realizado com a técnica magnetic search coil. As setas
vermelhas indicam início e término dos movimentos e a amplitude é representada como a excursão máxima
realizada pela pálpebra. A distância temporal entre os picos forma o intervalo entre pestanejos.
1.4 Cinética Palpebral
1.4.1. Forças ativas e passivas intervenientes no movimento da
pálpebra superior durante o pestanejo e os movimentos sacádicos
palpebrais
Diferentes forças ativas e passivas atuam na génese do pestanejo.
Estudos eletromiográficos têm demonstrado que as forças ativas que produzem
o movimento da pálpebra superior durante o pestanejo são geradas pelo MEPS
e MOO (Bjork and Kugelberg 1953; Cruz, Garcia, Pinto and Cechetti 2011;
23
Esteban and Salinero 1979; Holder, Scott, Hannaford and Stark 1987; Van
Allen and Blodi 1962).
Na posição primária do olhar, o MOO e o MEPS encontram-se
eletricamente ativos com os seus tónus em condições basais e em equilíbrio
(Bjork and Kugelberg 1953). Em qualquer tipo de pestanejo, ocorrem
fenómenos de inibição e ativação destes músculos que geram um movimento
típico da pálpebra superior, dividido em duas fases com características
cinéticas distintas: a descendente e a ascendente. A fase descendente inicia-se
com a inibição do MEPS, que precede a contração do MOO; o que significa
que, durante um curto período de tempo, perto do final da fase descendente,
ambos os músculos estão inativos. Além disso, forças passivas geradas pela
estrutura tarsoligamentar atuam no movimento palpebral descendente. Uma
vez que o movimento de descida é interrompido, o MOO retoma sua atividade
tónica e o MEPS contrai, elevando a pálpebra. A fase ascendente deve-se à
força ativa gerada pela contração do MEPS. A figura 13 ilustra as fontes de
forças ativas e passivas envolvidas no movimento da pálpebra superior durante
um pestanejo.
24
Figura 13 - Forças ativas e passivas envolvidas no movimento da pálpebra superior durante o pestanejo espontâneo
(Cruz, Garcia, Pinto and Cechetti 2011). Os dois primeiros traçados representam registos de eletromiografia do
músculo elevador da pálpebra superior (MEPS) e do músculo orbicular do olho (MOO). A terceira curva representa a
variação da energia potencial (EP) armazenada pelos componentes elásticos da pálpebra superior. O último traçado
ilustra o movimento da pálpebra superior. Os números 1 e 3 indicam os pontos de velocidade máxima da fase
descendente e ascendente, respetivamente. O número 2 indica o ponto de amplitude máxima do movimento, que
ocorre quando a velocidade é nula.
A fase ascendente do sacádico é semelhante à fase ascendente do
pestanejo; o sistema nervoso parece produzir um padrão semelhante de
atividade para o MEPS nestes dois movimentos (Becker and Fuchs 1988;
Evinger, Manning and Sibony 1991; Guitton, Simard and Codere 1991). Nesta
25
fase, ocorre apenas contração do MEPS. O sacádico descendente é muito
diferente da fase descendente do pestanejo. No primeiro, acontece o
relaxamento do MEPS, que associado a forças elásticas passivas palpebrais
(estruturas tarsoligamentares) e ao fenómeno gravitacional, levam a pálpebra
superior a descer (Evinger, Manning and Sibony 1991). Na fase descendente
do pestanejo a atividade elétrica do MEPS é nula e existe um aumento de
atividade do MOO (Fuchs, Becker, Ling, Langer and Kaneko 1992; Guitton,
Simard and Codere 1991).
1.4.2. Parâmetros de avaliação cinética
1.4.2.1. Amplitude e velocidade máxima
Embora possa parecer natural considerar a amplitude da fase
descendente e da fase ascendente essencialmente idênticas, é consensual que
é mais fácil determinar o final da fase de descida (Malbouisson, Messias,
Garcia, Cechetti, Barbosa and Cruz 2010; VanderWerf, Brassinga, Reits,
Aramideh and Ongerboer de Visser 2003). A fase ascendente tem uma
natureza oscilatória, e nem sempre é fácil identificar quando termina o
movimento (Cruz, Garcia, Pinto and Cechetti 2011; VanderWerf, Brassinga,
Reits, Aramideh and Ongerboer de Visser 2003). Assim passaremos a
considerar a expressão "amplitude do pestanejo" como referente à amplitude
de descida. Por outro lado, o movimento da margem da pálpebra superior
durante os pestanejos não é representado somente por uma translação vertical
(Evinger, Manning and Sibony 1991). Quando a pálpebra desce, o seu bordo
gira sobre a superfície curva da córnea. Assim, a amplitude é melhor
26
representada em graus do que em milímetros (Evinger, Manning and Sibony
1991; VanderWerf, Brassinga, Reits, Aramideh and Ongerboer de Visser 2003).
A variação da amplitude do pestanejo situa-se entre 10 e 60º. Por seu
turno, a amplitude média mantém-se semelhante nas diferentes faixas etárias,
observando-se uma pequena diminuição em indivíduos dos 80 aos 89 anos
(28,4º ± 2,5 Erro padrão) quando comparada com indivíduos dos 40 aos 49
anos (37,8º ± 4,6 Erro padrão) (Sun, Baker, Chuke, Rouholiman, Hasan, Gaza,
Stava and Porter 1997). Isto não significa que há alteração nos mecanismos
centrais de controle da amplitude do pestanejo. A razão mais plausível prendese com a posição da pálpebra superior que é mais baixa nos idosos (Cruz,
Garcia, Pinto and Cechetti 2011).
Em relação à cinética do movimento e concretamente em relação à
sua velocidade máxima, esta é sempre alcançada durante a fase descendente,
face à cessação da atividade muscular do MEPS, da força exercida pela
contração do MOO e das forças passivas. Por seu turno a fase ascendente é
mais lenta, já que resulta apenas da contração do MEPS (Evinger, Manning
and Sibony 1991; Guitton, Simard and Codere 1991). A ação do MOO não
ocorre durante toda a fase descendente. Em termos cinéticos, há um momento
em
que,
na
fase
descendente,
a
velocidade
da
pálpebra
diminui
progressivamente alcançando a sua amplitude máxima e iniciando a fase
ascendente. Neste contexto, a velocidade máxima é atingida aproximadamente
aos 70% de excursão da fase descendente (Malbouisson, Messias, Garcia,
Cechetti, Barbosa and Cruz 2010).
27
1.4.2.2. Main sequence: relação entre amplitude, velocidade máxima
e duração
A relação entre a amplitude e o pico de velocidade é considerada linear
(Evinger, Manning and Sibony 1991; Garcia, Messias, Costa, Pinto, Barbosa
and Cruz ; Sun, Baker, Chuke, Rouholiman, Hasan, Gaza, Stava and Porter
1997). Esta característica é conhecida como main sequence (um termo oriundo
da astronomia).
Figura 14 - Registo num indivíduo normal, mostrando a relação entre amplitude e velocidade máxima do pestanejo
espontâneo (Cruz, Garcia, Pinto and Cechetti 2011).
Originalmente, main sequence designava a relação entre o brilho de
uma estrela e a sua temperatura. A literatura sobre a main sequence do PE é
escassa. Em estudos da cinética do movimento dos músculos extraoculares,
esta expressão designa a relação entre o pico de velocidade e a amplitude dos
movimentos sacádicos oculares (Bahill, Clark and Stark 1975). Por analogia, o
28
conceito foi utilizado na caracterização dos movimentos palpebrais para
expressar a relação entre a amplitude e a velocidade dos mesmos. A inclinação
desta relação, designada main sequence é indicativa da atividade motora
neuronal do MOO (Hasan, Baker, Sun, Rouholiman, Chuke, Cowen and Porter
1997). Dependendo da magnitude da inclinação da main sequence da fase
descendente, a duração das fases de subida e descida irá aumentar
moderadamente com a amplitude (Cruz, Garcia, Pinto and Cechetti 2011;
Evinger, Manning and Sibony 1991; Guitton, Simard and Codere 1991).
1.4.2.3. Taxa de pestanejo espontâneo
A relação entre o número de pestanejos realizado num determinado
período de tempo designa-se taxa de pestanejo espontâneo (TPE). Para a
avaliar
solicitamos
ao
observador
para
fixar
determinado
objeto
e
contabilizamos o número total de pestanejos, o qual é dividido pelo tempo de
observação em minutos. A TPE é assim expressa como uma taxa média de
pestanejos/minuto.
Desde 1927, após a sua descrição por Ponder e Kennedy (Ponder and
Kennedy 1928), a determinação da TPE "normal" tem sido objeto de várias
abordagens, em diferentes áreas de investigação. Assim, o PE já ocorre na
vida intrauterina (Petrikovsky, Kaplan and Holsten 2003). A TPE aumenta na
infância (Lavezzo, Schellini, Padovani and Hirai 2008) e estabiliza na vida
adulta (10 a 20 pestanejos/minuto) (Bacher and Allen 2009; Bacher and
Smotherman 2004; Bacher and Smotherman 2004; Bentivoglio, Bressman,
Cassetta, Carretta, Tonali and Albanese 1997; Petrikovsky, Kaplan and Holsten
2003). Para além disso, situações que interferem no estado mental do indivíduo
29
alteram a taxa normal do pestanejo. Assim, situações de stress como falar em
público (Mori, Egami, Nakamori, Ohtsuki, Aikawa, Shintani, Matsumoto, Goto
and Tsubota 2008), estado de vigília prolongada (Barbato, De Padova, Paolillo,
Arpaia, Russo and Ficca 2007; Barbato, Ficca, Muscettola, Fichele, Beatrice
and Rinaldi 2000; Crevits, Simons and Wildenbeest 2003; De Padova, Barbato,
Conte and Ficca 2009) ou estados de ansiedade (Karson 1983; Kojima, Shioiri,
Hosoki, Sakai, Bando and Someya 2002) podem condicionar um aumento da
frequência do pestanejo. Já as situações que exijam atenção do indivíduo
como ler um livro, realização de atividades manuais ou ver um filme
condicionam diminuição da frequência do pestanejo (Bentivoglio, Bressman,
Cassetta, Carretta, Tonali and Albanese 1997; De Jong and Merckelbach 1990;
Freudenthaler, Neuf, Kadner and Schlote 2003; Kaneko and Sakamoto 2001;
Schaefer, Schaefer, Abib and Jose 2009; Schlote, Kadner and Freudenthaler
2004; Tsubota 1998; Tsubota and Nakamori 1993).
Admite-se que os distúrbios psiquiátricos, neurológicos e o consumo de
drogas que atuam sobre a TPE, sejam decorrentes de alterações no sistema
dopaminérgico central. Assim, o PE é usado como um marcador não invasivo
da atividade de circuitos cerebrais dopaminérgicos (Karson 1983). Foi
observada uma correlação positiva entre a TPE e a transmissão da dopamina
numa variedade de estudos clínicos de doentes com patologias relacionadas
com disfunção desse neurotransmissor. Assim, verificou-se uma diminuição da
TPE em pacientes com doença de Parkinson (Agostino, Bologna, Dinapoli,
Gregori, Fabbrini, Accornero and Berardelli 2008; Karson, LeWitt, Calne and
Wyatt 1982; Korosec, Zidar, Reits, Evinger and Vanderwerf 2006), com atraso
mental, com distúrbios de comportamento repetitivos (Bodfish, Powell, Golden
30
and Lewis 1995; Goldberg, Maltz, Bow, Karson and Leleszi 1987), paralisia
supranuclear progressiva (Bologna, Agostino, Gregori, Belvisi, Ottaviani,
Colosimo, Fabbrini and Berardelli 2009; Esteban, Traba and Prieto 2004),
abuso de álcool (Ponder and Kennedy 1928) e
doentes consumidores de
cocaína (Colzato, Van den Wildenberg and Hommel 2008). Pelo contrário, nos
distúrbios que cursam com atividade aumentada da dopamina, há um
significativo aumento da TPE. Os exemplos são numerosos e incluem a
esquizofrenia (Chen, Lam, Chen and Nguyen 1996; Mackert, Woyth, Flechtner
and Volz 1990; Stevens 1978), a doença de Huntington (Esteban, Traba and
Prieto 2004; Karson, Burns, LeWitt, Foster and Newman 1984), a distonia focal
(Esteban, Traba and Prieto 2004), o autismo (Goldberg, Maltz, Bow, Karson
and Leleszi 1987), o síndrome de Prader-Willi (Holsen and Thompson 2004), o
déficit de atenção/hiperatividade (Fukui, Svenningsson, Matsuishi, Higashi,
Nairn, Greengard and Nishi 2003; Konrad, Gauggel and Schurek 2003), a
depressão (Mackintosh, Kumar and Kitamura 1983), a psicose (Karson,
Goldberg and Leleszi 1986; Lovestone 1992), o transtorno do pânico (Kojima,
Shioiri, Hosoki, Sakai, Bando and Someya 2002) e o síndrome do X frágil
(Roberts, Symons, Johnson, Hatton and Boccia 2005).
Em oftalmologia, tem-se estudado, prioritariamente, a relação entre o
pestanejo e a superfície ocular. Foi demonstrado que fatores locais
da
superfície ocular modulam a TPE. É exemplo de diminuição da frequência do
pestanejo, a anestesia tópica da córnea (Freudenthaler, Neuf, Kadner and
Schlote 2003; Garcia, Messias, Costa, Pinto, Barbosa and Cruz ; Naase,
Doughty and Button 2005; Nakamori, Odawara, Nakajima, Mizutani and
Tsubota 1997). Por seu turno, os portadores de lente de contato (York, Ong
31
and Robbins 1971) e os doentes com olho seco (Cruz, Garcia, Pinto and
Cechetti 2011; Nakamori, Odawara, Nakajima, Mizutani and Tsubota 1997)
apresentam um aumento da TPE.
1.4.2.4. Distribuição dos intervalos de tempo entre pestanejos
Para além da amplitude e da TPE, o pestanejo também é caracterizado
pelo intervalo de tempo entre pestanejos (ITP). Ponder e Kennedy
demonstraram que o ITP, considerando pestanejos consecutivos não é fixo
(Ponder and Kennedy 1928). Isso significa que indivíduos com a mesma TPE
podem pestanejar de formas diferentes. Estes autores foram, provavelmente,
os primeiros a constatar que os intervalos variam bastante entre indivíduos
(Ponder and Kennedy 1928) e no mesmo indivíduo (Garcia, Pinto, Barbosa and
Cruz 2011).
Trabalhos de investigação subsequentes apresentam resultados pouco
concordantes. No geral, há um problema de amostragem nestes estudos
destinados a estabelecer padrões de distribuição ITP. Todos esses estudos
foram realizados com análise de vídeo, sendo os tempos de observação muito
curtos (geralmente 3 a 5 minutos). Se considerarmos que um indivíduo normal
pestaneja mais de 1000 vezes por hora, amostras formadas pelos pestanejos
que ocorrem em 3 a 5 minutos, tornam-se extremamente pequenas e variáveis
(Cruz, Garcia, Pinto and Cechetti 2011).
32
1.5. Orbitopatia de Graves
Orbitopatia de Graves (OG) é o nome dado à doença autoimune orbitária
caracterizada pela presença de retração palpebral associada à proptose,
estrabismo restritivo ou neuropatia ótica (Bartley and Gorman 1995; Burch and
Wartofsky 1993).
Figura 15 - Caso clínico de orbitopatia de Graves. Doente de 16 anos de idade, com bócio (hipertiroidismo) e
orbitopatia (proptose e retração palpebral).
A grande maioria dos doentes apresenta algum grau de disfunção
tiroideia, com destaque para o hipertiroidismo ou doença de Graves, que está
presente em 90% dos casos (Bartley, Fatourechi, Kadrmas, Jacobsen, Ilstrup,
Garrity and Gorman 1996) (figura 15). É de salientar que há doentes
33
eutiroideus e hipotiroideus com OG (Burch and Wartofsky 1993). A razão para
este achado é que quer a órbita quer a tiróide são órgãos-alvo deste processo
autoimune. Assim os doentes portadores de doença orbitária podem não
apresentar o quadro endocrinológico. Posteriormente o desenvolvimento da
doença orbitária é independente dos níveis séricos de hormonas tiroideias
(Bahn 2010; Waller 1982).
Em termos fisiopatológicos, a OG é um fenómeno autoimune devido à
interação entre os autoanticorpos anti-recetor da hormona estimulante da
tiróide (TRAb) e os fibroblastos orbitários. Estes são considerados as principais
células efetoras da OG (figura 16), devido à sua capacidade de resposta a
algumas citocinas e à interação com os autoanticorpos deste processo
autoimune. Estudos recentes têm demonstrado que a ativação do recetor da
hormona estimulante da tiróide (TSH) dos fibroblastos orbitários aumenta a
síntese de ácido hialurónico e a adipogénese, provocando espessamento dos
músculos extraoculares e aumento do componente adiposo orbitário (Bahn
2010; Iyer and Bahn 2012; Smith, Tsai, Shih, Tsui, Chen, Han, Naik, King,
Press, Kamat, Goldberg, Phipps, Douglas and Gianoukakis 2008).
A deteção dos níveis de TRAb é muito útil no diagnóstico (Jang, Shin,
Lee, Choi, Lee and Yoon 2013; Michalek, Morshed, Latif and Davies 2009),
follow up(Maugendre and Massart 2001; Tada, Mizuta, Takano, Tatsumi, Izumi,
Hidaka and Amino 2003), monitorização do tratamento (Jang, Shin, Lee, Choi,
Lee and Yoon 2013; Tada, Mizuta, Takano, Tatsumi, Izumi, Hidaka and Amino
2003) e prognóstico (Maugendre and Massart 2001) de doentes com OG.
Alguns trabalhos demonstraram a existência de uma correlação direta dos
níveis de TRAb com a prevalência de OG (Khoo, Ho, Seah, Fong, Tai, Chee,
34
Eng, Aw and Fok 1999), assim como com o grau de atividade (Gerding, van der
Meer, Broenink, Bakker, Wiersinga and Prummel 2000; Wakelkamp, Bakker,
Baldeschi, Wiersinga and Prummel 2003) e gravidade (Eckstein, Plicht, Lax,
Neuhauser, Mann, Lederbogen, Heckmann, Esser and Morgenthaler 2006;
Morris, Hay, Nelson and Jiang 1998) da doença. Existe uma relação direta
entre níveis de TRAb e prognóstico tanto da OG como do hipertiroidismo
(Eckstein, Lax, Losch, Glowacka, Plicht, Mann, Esser and Morgenthaler 2007).
De salientar que foi demonstrada uma relação direta entre os níveis de TRAb e
o grau de proptose (Gerding, van der Meer, Broenink, Bakker, Wiersinga and
Prummel 2000).
Figura 16 - Mecanismos moleculares da orbitopatia de Graves (Bahn 2010). IGF-I: fator de crescimento semelhante
à insulina tipo 1; TNF: fator de necrose tumoral; TGF-β: fator de transformação de crescimento beta.
35
Clinicamente, o atingimento do tecido adiposo e muscular da órbita pode
variar. Nunery classificou a OG em dois subtipos clínicos (Nunery 1991). A
orbitopatia subtipo 1 (lipogénica) caracteriza-se pelo aumento da gordura
orbitária, com pouco ou nenhum aumento muscular. Os pacientes com subtipo
1 de OG são, na maioria, do sexo feminino (relação feminino/masculino 8:1) e
costumam
apresentar
motilidade
ocular
normal,
ausência
de
sinais
inflamatórios, exoftalmias simétricas e evolução geralmente benigna. A
orbitopatia subtipo 2 (miogénica) é caracterizada pelo comprometimento
predominantemente muscular. Como consequência, pacientes com este
subtipo apresentam maior predisposição para desenvolver diplopia, proptose
assimétrica,
processos
inflamatórios
e
neuropatia
ótica
compressiva.
Geralmente o subtipo miogénico inicia-se em idades mais avançadas e
apresenta menor relação feminino/masculino (2:1) (Nunery 1991).
A
B
C
Figura 17 - Doente com subtipo lipogénico de orbitopatia de Graves. A e B: aspeto facial. C: tomografia
computorizada (corte axial) mostra exoftalmia simétrica com aumento do compartimento adiposo.
A
B
C
Figura 18 - Doente com subtipo miogénico de orbitopatia de Graves: estrabismo restritivo e diplopia. A: aspeto
facial. Tomografia computorizada (B: corte coronal; C: corte axial): espessamento dos músculos extraoculares.
36
Os critérios diagnósticos para OG foram definidos em 1995 por Bartley e
Gorman (Bartley and Gorman 1995). A OG deve ser considerada quando há
presença da retração palpebral associada a pelo menos um dos seguintes
sinais: disfunção tiroideia, proptose, neuropatia ótica e/ou atingimento dos
músculos extraoculares. Na ausência de retração palpebral, o diagnóstico é
estabelecido diante da disfunção tiroideia com proptose, neuropatia ótica e/ou
envolvimento dos músculos extraoculares.
A retração palpebral superior é a característica mais frequente da OG,
descrita em uma série de casos em cerca de 90% dos pacientes (Day 1959).
Apesar de a retração das pálpebras superiores ser o achado clínico mais
comum na OG, as pálpebras inferiores também estão comprometidas em
aproximadamente 25% dos pacientes (Bartley, Fatourechi, Kadrmas, Jacobsen,
Ilstrup, Garrity and Gorman 1996).
Figura 19 - Doente de 10 anos de idade, com retração palpebral superior e inferior por orbitopatia de Graves.
A proptose ocular (ou exoftalmo) ocorre em, aproximadamente, 60% dos
doentes com OG, estando relacionada com o aumento dos tecidos muscular e
37
adiposo orbitários (Bartley, Fatourechi, Kadrmas, Jacobsen, Ilstrup, Garrity and
Gorman 1996). A análise da evolução temporal da exoftalmometria mostra que
72 a 80% dos casos permanecem estáveis, 16 a 23% sofrem aumento maior
que 2 mm e 5% podem diminuir espontaneamente (Bartley, Fatourechi,
Kadrmas, Jacobsen, Ilstrup, Garrity and Gorman 1996). A protrusão ocular nos
pacientes com OG geralmente é simétrica, porém pode haver assimetria em
9% dos pacientes (Soroudi, Goldberg and McCann 2004).
O grau de protrusão ocular é medido pela exoftalmometria. Em 1904
Hertel (Hertel 1905; Hertel and Simonsz 2008) apresentou um instrumento para
obtenção de valores do posicionamento anteroposterior do olho: tomando como
base o rebordo orbitário lateral e com o auxílio de espelhos pode ser obtida a
distância até o ápice da córnea. Posteriormente surgiram críticas em relação à
precisão do aparelho desenhado por Hertel (Frueh and Frueh 2007; Vardizer,
Berendschot and Mourits 2005) e novas formas de efetuar essa medição
(Luedde 1938; Naugle and Couvillion 1992). No entanto até hoje nenhum é
consensual, pelo que o exoftalmómetro de Hertel continua a ser o instrumento
utilizado com maior frequência na prática clínica.
As medidas exoftalmométricas refletem a interação entre o continente
ósseo da órbita e seu conteúdo. A cavidade óssea orbitária circunda
completamente os tecidos moles orbitários, com exceção da porção anterior,
fazendo com que a posição do globo em relação à órbita seja um indicador de
alterações orbitárias (Vardizer, Berendschot and Mourits 2005). O grau de
protrusão ocular pode ser bem quantificado por meio da exoftalmometria
clínica. No entanto o interior da órbita contém várias estruturas, e medidas
relacionadas às estruturas intraorbitárias não são passíveis de serem
38
adquiridas clinicamente. Assim as medições exatas do interior da órbita só se
tornam possíveis por meio de amostragem cirúrgica (Rogers and Bojovic 2010),
estudos em cadáveres (Shams, Abed, Shen, Adds and Uddin 2012) e, mais
recentemente, com os exames de imagem. Desde a descoberta da radiação
ionizante (raio-X) no final do século XIX, os métodos de imagem na área
médica evoluíram substancialmente. Inicialmente a radiografia simples era a
técnica mais utilizada para avaliação das doenças de órbita; no entanto, com o
aparecimento de técnicas de imagem mais modernas e que permitem um
estudo mais rigoroso e detalhado da órbita, esta foi substituída principalmente
pela tomografia computadorizada e a ressonância nuclear magnética (Dutton
2010).
Figura 20 - Doente com 14 anos de idade com retração palpebral e proptose grave por orbitopatia de Graves.
O aumento da musculatura ocular externa na OG acontece em
aproximadamente 55% dos pacientes (Bartley, Fatourechi, Kadrmas, Jacobsen,
Ilstrup, Garrity and Gorman 1996), podendo variar desde um incremento
discreto de alguns músculos até o alargamento de todos os músculos
(principalmente os músculos reto medial e reto inferior) (Burch and Wartofsky
39
1993). Uma característica marcante da OG é o aumento dos músculos
extraoculares, poupando as inserções musculares tendinosas (Trokel and
Jakobiec 1981). Este fenómeno condiciona o desenvolvimento de estrabismo
restritivo em 43% dos doentes (figura 20), enquanto 6% evoluem para
neuropatia ótica. Esta deve-se a compressão do nervo ótico no ápice da órbita
(Bartley, Fatourechi, Kadrmas, Jacobsen, Ilstrup, Garrity and Gorman 1996).
A
B
Figura 21 - Doentes com orbitopatia de Graves, com estrabismo restritivo (A: hipotropia; B: endotropia).
A neuropatia ótica é considerada a complicação mais grave e a causa
mais frequente de perda de acuidade visual irreversível. Afeta 3 a 8% dos
doentes com OG (Wiersinga and Bartalena 2002). É um quadro clínico com
enorme variabilidade de apresentação devido à sua etiologia multifatorial. O
principal mecanismo proposto para a perda visual na OG é a compressão do
nervo ótico no ápice da órbita pelo aumento dos músculos extraoculares
(“apical crowding”) (Jorge, Scott, Akaishi, Cruz and Flynn 2003; Kennerdell,
Rosenbaum and El-Hoshy 1981; Neigel, Rootman, Belkin, Nugent, Drance,
Beattie and Spinelli 1988). Existem, no entanto, outros mecanismos que
poderão estar também na origem da neuropatia ótica associada à OG:
compressão da vascularização (originando estase venosa e/ou neuropatia
40
isquémica); em doentes com proptose marcada, o alongamento do nervo ótico
(pode provocar fenómenos isquémicos); em doentes com proptose mínima, a
rigidez do septo orbitário pode originar maior compressão no ápice da órbita
(Saavedra and Fernández 2011).
Os principais fatores de risco orbitários para o desenvolvimento de
neuropatia ótica são a restrição da motilidade ocular (especialmente
supradução menor que 30º) e o grau de aumento do volume dos músculos
extraoculares (Feldon, Muramatsu and Weiner 1984; McKeag, Lane, Lazarus,
Baldeschi, Boboridis, Dickinson, Hullo, Kahaly, Krassas, Marcocci, Marino,
Mourits, Nardi, Neoh, Orgiazzi, Perros, Pinchera, Pitz, Prummel, Sartini and
Wiersinga 2007). Os principais fatores de risco sistémicos são a diabetes
(Kalmann and Mourits 1999) e o tabagismo (Prummel and Wiersinga 1993).
Dado tratar-se de uma entidade frequentemente subdiagnosticada é de
salientar a importância de uma anamnese e uma avaliação oftalmológica
completa em todos os doentes com OG. Uma acuidade visual normal não
exclui o diagnóstico; os exames auxiliares de diagnóstico, nomeadamente teste
de sensibilidade cromática, perimetria computorizada, tomografia de coerência
ótica, estudo eletrofisiológico e exames de imagem (tomografia computorizada
e ressonância magnética nuclear) têm um papel importante no diagnóstico
desta patologia. Relativamente ao tratamento, o uso de corticóides como
tratamento inicial é universalmente aceite (Saavedra and Fernández 2011). Em
casos com contraindicação para o uso de corticóides ou em que estes não
foram eficazes, a radioterapia orbitária poderá estar indicada (Stiebel-Kalish,
Robenshtok,
Hasanreisoglu,
Ezrachi,
Shimon
and
Leibovici
2009).
A
descompressão orbitária com o objetivo de expansão cirúrgica do ápice da
41
órbita está especialmente indicada em casos que não respondem aos
imunossupressores e/ou à radioterapia; deve ser feita de forma urgente e
associada a pulsos de corticoterapia endovenosos, se a perda visual é rápida
(menos de 1 semana) e grave (acuidade visual menor que 20/200) (StiebelKalish, Robenshtok, Hasanreisoglu, Ezrachi, Shimon and Leibovici 2009).
A
B
Figura 22 - Doente com neuropatia ótica por compressão do nervo ótico no ápice da órbita devido ao espessamento
exuberante dos músculos extraoculares (A: aspeto facial; B: tomografia computorizada, corte axial).
1.5.1 Retração palpebral superior
A retração da pálpebra superior é o sinal mais comum e característico da
OG (Day 1959; Lebensohn 1964; Scott and Siatkowski 1999). Apesar de ser
bem reconhecida desde o século XIX, é ainda alvo de grande controvérsia. Foi
efetuada uma revisão extensa, incluindo aspetos históricos, etiologia,
diagnóstico e tratamento médico e cirúrgico. Os mecanismos responsáveis pela
retração palpebral são ainda tema de discussão. Apesar de ser uma patologia
com etiologia multifatorial, ainda não foram descritos subtipos de retração
palpebral superior. Os inúmeros procedimentos cirúrgicos descritos para a sua
correção, mostram que não há consenso entre os cirurgiões sobre qual o
melhor método a ser utilizado.
42
SURVEY OF OPHTHALMOLOGY
VOLUME 58 NUMBER 1 JANUARY–FEBRUARY 2013
MAJOR REVIEW
Graves Upper Eyelid Retraction
Antonio Augusto Velasco Cruz, MD,1 Sara F.T. Ribeiro, MD,2 Denny M. Garcia, BSc,1
Patricia Mitiko Akaishi, MD,1 and Carolina T. Pinto, MD1
1
Department of Ophthalmology, Otorhinolaryngology, and Head and Neck Surgery, School of Medicine of Ribeirão Preto,
University of São Paulo, Brazil; and 2Hospital de São João, School of Medicine, University of Oporto, Portugal
Abstract. Graves upper eyelid retraction (GUER) is the most common and characteristic sign of
Graves orbitopathy. Despite being well recognized since the 19th century, GUER is still a subject of
controversy. We review GUER, including historical aspects, diagnosis, methods of measurements,
ocular surface abnormalities, etiology, and medical and surgical treatments. There is no consensus
about the mechanisms of its etiology or the best surgical correction. There is a need for quantitative
studies on the effects of GUER on lid movements. (Surv Ophthalmol 58:63--76, 2013. Ó 2013
Elsevier Inc. All rights reserved.)
Key words.
Graves disease
eyelid movements
I. Introduction
management
upper eyelid retraction
Although many patients similar to the women
examined by Graves and Von Basedow had existed
in antiquity,17,121 only within the last two centuries
has the position of the upper lids in Graves disease
became a specific subject in the medical literature.
In the Lancet in 1849, Cooper discussed a case of
a patient with exophthalmos and goiter. He alluded
to John Dalrymple’s explanation of the eye changes
in the following words:
A. HISTORICAL BACKGROUND
The eye changes associated with a disease that
combined palpitations and goiter described in 1786
by Parry120 were already well recognized by the 19th
century. Robert J. Graves, in his twelfth lecture
presented in 1835 at the Meath Hospital in Dublin,
described a woman who had findings that were
initially thought to be hysterical. He noticed that
‘‘the eyes assumed a singular appearance, for the
eyeballs were apparently enlarged, so that when she
slept or tried to shut her eyes, the lids were incapable
of closing. When the eyes were open, the white
sclerotic could be seen to a breadth of several lines, all
round the cornea.’’65 Five years later Von Basedow
published similar observations about a Mrs F, who was
one of his four patients. She was described as having
‘‘eyes so protruded that one could see the sclera above
and below the cornea. The eyelids were spread wide
apart and with much force she was unable to bring
them together, and slept with wide open eyes.’’43,158
Dalrymple relates a case of a gentleman whose
eyes were so protruded that they were nearly
denuded of the protection of the upper lid by
a constant and powerful spasm of the levator
palpebrae superioris, which drew the lids, so
far upwards and backwards, that much of the
sclera above the cornea was visible.30,87
The English ophthalmologist John Dalrymple
clearly identified the levator palpebrae superioris
muscle (LPS) as the source of the upper lid retraction.
He was the first to differentiate lid retraction from
63
Ó 2013 by Elsevier Inc.
All rights reserved.
0039-6257/$ - see front matter
doi:10.1016/j.survophthal.2012.02.007
43
64
Surv Ophthalmol 58 (1) January--February 2013
CRUZ ET AL
TABLE 1
Eponyms Associated with Upper Eyelid in Graves Disease
Eponym
Name
Sign
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Dalrymple
Boston
von Graeffe
Rosenbach
Stellwag
Kocher
Pochin
Mean
Joffroy
Sainton
Gellinek
Riesman
Enroth
Vigouroux
Gifford
Lid retraction
Jerky and uneven downward movement of the lid
Upper lid lag on downgaze
Tremor of gently closed lids
Incomplete and infrequent blinking
Retraction of the lid during fixation
Reduced amplitude of blinking
Increased superior scleral show on upgaze
On looking up the normal creases are absent from the forehead
The frontalis contracts only after the levator action has ceased
Abnormal pigmentation of the lid
Bruit over eyelid
Edematous swelling of the lids
Puffiness of the lids
Difficult eversion of the lid
exophthalmos, and his name passed to history as
a synonym of Graves upper eyelid retraction (GUER).
In the last years of the 19th century and the
beginning of the 20th century, several physicians
observed that, besides being retracted, the upper
eyelids of Graves patients had abnormalities that
became known as signs bearing their names. Table 1
summarizes 15 eponyms associated with GUER
abnormalities.23,36,96 Eponyms 11--15 refer to nonspecific structural abnormalities; the first 10 indicate
anomalies of lid function, a subject that will be
addressed later on.
II. Diagnosis
A. NORMAL RESTING UPPER EYELID POSITION
Retraction implies that the resting position of the
affected lid is abnormally high. This definition
requires a statistical knowledge of the distribution
of the lid position in the normal population. In the
past, the upper limbus was commonly used as
a reference for a qualitative assessment of lid
position.36,62 Although some lid surgeons adopted
the lower limbus as the reference for measurement
of upper lid position,105,133 most measurements now
use the center of the pupil.54 There are few
published data on the midpupil to upper lid margin
distance (MPLD) in large samples of normal
patients. In his thesis for the American Ophthalmological Society, Frueh was the first to provide
statistical parameters of MPLD distribution. He
measured 111 normal patients (64 women and
47 men; mean age, 42.7 years) and obtained a mean
value of 3.5 mm and a standard deviation (SD) of
0.9 mm. The maximum value observed was 6.0
mm.54 Frueh’s results were corroborated by another
44
study that analyzed the effect of age on palpebral
fissure morphology.159 In that study 320 patients
ranging in age from 10 to 89 years were divided into
eight age groups of 40 patients each (20 men and
20 women). Each age group had a bin width of
10 years. Although the results of the MPLD were
provided only in graphic form, using a digitization
process we estimate that the plotted means and
standard deviations varied across groups from 3.3-3.85 1.10--1.92 (SD) mm. These values were not
significantly different, and lid position remained
stable over the whole age period studied.159
Assuming that the published mean values and
standard deviation of MPLD derive from a normal
distribution, only 2.25% of normal patients have
upper lids higher than the mean þ 2 SD (3.5 þ 1.8),
or 5.3 mm, above the midpupil. Given that the
vertical corneal diameter is on average 11 mm, an
MPLD of 5.3 mm is approximately at the upper
limbus. So, it is acceptable to consider eyelids
resting at or above the limbus as retracted.5,7,143
The diagnosis of GUER cannot be based only on
a single measurement. MLPD asymmetries are also
important. A patient may present with both lids
within the normal range (OD 5 3.0 mm and OS, 5.0
mm) and yet have left lid retraction. Frueh
concluded that the lid position was highly correlated
between eyes (r 5 0.90), but did not provide any
distribution of MLPD differences between the eyes.
It seems reasonable to consider asymmetries greater
than 1.0 mm as not normal and if both eyelids are
within the normal, range (3.5--5.5 mm), the
differential diagnosis is between retraction of the
higher eyelid and ptosis of the lower eyelid. In this
situation, other signs such as variability of the lid
position and contour abnormalities are highly
indicative of GUER.
65
GRAVES UPPER EYELID RETRACTION
Fig. 1. Left: Clinical appearance of a patient with lateral lid flare sign. Right: The dashed line represents normal upper
eyelid contour. The solid line is the patient’s lid contour. The vertical bar indicates the midpupil lid distance (MPLD).
Notice that the retraction is more evident laterally than medially.
B. LATERAL LID FLARE SIGN
The importance of qualitative clinical judgment
in assessing GUER was well addressed by Waller, who
recognized that a single measurement of lid
position did not capture the high variability of
GUER. He also relied on the observation of the
lateral flare for the diagnosis of difficult cases.163
The description ‘‘lateral flare’’ denotes the enhanced retraction of the lateral aspect of the eyelid,
a feature that was recognized since the first
publications on surgical correction of GUER.
On two-dimensional images the lateral flare is seen
as an increase of the temporal area of the fissure33 and
a lateral displacement of the eyelid contour peak32
(Fig. 1). This phenomenon probably reflects a state of
LPS contraction because voluntary upper lid retraction in normal subjects induces a typical ‘‘flare sign’’.
where R is the radius of the globe assuming that the
eye is spherical. The length of the arc AB is always
greater than AC. The differences between curved and
linear measurements are small, and any increase in
the linear dimension reflects worsening of the
retraction.
C. METHODS OF MEASUREMENT
In clinical settings the lid position is usually
measured with a millimeter ruler as a linear distance
between the pupil center and the edge of the lid
margin at the twelve o’clock position.142 This
measurement is performed with the examiner sitting
at eye level relative to the patient, who is instructed to
fixate on a distant target.44 If a light reflex is used to
locate the pupillary axis, the measurement is referred
to as margin reflex distance (MRD). Sometimes
a subscript number is used to differentiate the upper
(MRD1) from the lower (MRD2) lid.22,50,97,104,129,133
Photographs of the palpebral fissure projected on
a grid159 or displayed as digital images on a computer
screen32,44 are also used to measure MRD or MPLD.
A linear measurement such as MRD or MPLD does
not represent the exact amount of the excursion
undergone by the retracted lid over the curved
surface of the eye. As shown in Fig. 2, the curved
excursion of the lid is related to the linear MPLD
AC
,
measurement by the expression AB5R arcsin
R
Fig. 2. Relationship between the position of the upper
eyelid measured as a linear distance AC from the pupillary
center (B) and the length of the arc AB. Assuming that
the eye is approximately
spherical with a radius R, then
AC
AB5R arcsin
.
R
45
66
CRUZ ET AL
III. Prevalence
Lid retraction is one of the most common signs of
Graves orbitopathy (GO) and a major diagnostic
criterion for the disease.5 In early case series lid
retraction was found in 94.0% of the patients.36
Population-based studies have yielded similar results. Bartley found that among incident cases of GO
in Olmsted County, Minnesota, eyelid retraction was
the most common ophthalmic feature of autoimmune thyroid disease, being present either unilaterally or bilaterally in more than 90% of patients.4
Fig. 4. Young adult man with bilateral upper scleral show.
This is a normal finding in a small portion of the
population.
IV. Differential Diagnosis
Although there is a long list of conditions that
elicit upper lid retraction,6 in the majority of cases
the correct diagnosis is usually straightforward and
easily made when the overall clinical picture of the
patient is considered, including a comprehensive
anamnesis, determination of thyrotropin receptor
antibodies, thyroid hormone levels, and orbital
imaging studies. In childhood, congenital upper
lid retraction may simulate Graves disease,28,136,149
but the condition does not change with time, and
thyroid hormones and orbital imaging studies are
normal. As congenital lid retractions do not respond
to topical guanethidine, they are thought to be
caused by intrinsic LPS muscle abnormalities.2 Fig. 3
shows a case of congenital upper eyelid retraction.
Notice that, instead of lid lateral flare, the contour is
abnormal on the nasal aspect of the eyelid.
Bilateral symmetric eyelids resting above the limbus
may be a normal finding. As mentioned before,
theoretically, the MRD1 of 2.25% of the population is
greater than 5.3 mm. The patient shown in Fig. 4 is
a normal young adult with bilateral upper scleral show.
The patient reported that several healthy members of
his family, including his mother, sister, and several
aunts and uncles, had a similar appearance.
Unilateral acquired ptosis may be confounded
with contralateral lid retraction (pseudoretraction).13,63,71,95,103,106,108,135 This type of lid retraction
is explained by the synergistic motor correspondence of the levator muscles (Hering’s law). A similar
mechanism explains the rare cases of lid retraction
occurring in the non-paretic eye in acquired
ophthalmoplegia.86 Collier’s sign is the term used
to describe the lid retraction that occurs in the dorsal
midbrain syndrome caused by several neurological
diseases such as pinealoma, hydrocephalus, subthalamic or midbrain arteriovenous malformations,
thalamic-mesencephalic infarction, disseminated
sclerosis, and encephalitis.6,57,58,61,91 Parinaud syndrome is the combination of lid retraction, paralysis
of the vertical gaze, convergence retraction nystagmus on attempted upgaze, and pupillary light-near
dissociation.130 Paradoxical lid retraction may also
occur in myasthenia gravis.89,124,146
Other situations that may be confounded with
GUER include high myopia,6 prominent glaucoma
filtering blebs,126 orbital floor fractures with entrapment of the inferior rectus muscle,6,127 orbital
neoplasms,6 contact lens use,6,164 and sympathomimetics.6 The Summerskill sign is upper lid retraction associated with hepatic cirrhosis;150 Bartley
points out, however, that the patients described in
Summerskill’s original paper most likely had Graves
disease,3 and the association is questionable.109
V. Upper Eyelid Movements and Ocular
Surface Changes
Fig. 3. A seven-year old boy with congenital asymmetric
upper eyelid retraction. Notice the peculiar notch on the
medial portion of both upper lids.
46
The upper eyelids are constantly in motion.
During the waking hours we spontaneously blink
10 to 30 times per minute34 and when we look down
or up the lids follow the eye movement. These lid
movements that follow rapid changes in vertical
gaze fixation are known as lid saccades.9 Spontaneous
blinks and lid saccades frequently overlap, but they
are studied separately because these movements
have different kinematic properties, and the forces
involved in their generation also differ.48
67
Downward lid saccades are passive movements
that are generated by the relaxation of the stretched
elastic components of the lid (tarsal plate, medial
and lateral tendons, and Whitnall ligament). Upward saccades, on the contrary, are produced by the
active contraction of the levator muscle.48 Downward lid saccades are supposed to be abnormal in
GUER. The so-called ‘‘Boston sign’’ (jerky and
uneven downward movement of the lid) describes
an abnormality of the downward lid saccades.
The time-honored von Graefe sign also refers to
an abnormal function of the elastics components of
the upper lid.49 The exact meaning of this sign has
been a subject of controversy. For many the sign is
a synonymous with lid lag or, in other words,
a downward saccadic movement with reduced
amplitude.24,36,96 Harvey and Anderson do not
agree with this interpretation. They noticed that
a specific phrase of the original von Graefe’s paper
(‘‘aufgehobnen Consensus zwischen Lidbewegung
und Hebung und Senkung der Visirebene’’) referred to an abolishment of the lid eye coordination
rather than a true lid lag. Or, in other words, the
sign is a dynamic abnormality of the downward lid
saccades (velocity) instead of a static phenomenon
(lid lag).75 This point of view was adopted in a recent
work that assessed the frequency of von Graefe sign
and lid lag as distinct signs.56 From a historical point
of view, the distinction between reduced amplitude
(lid lag) and a slower rate of downward lid saccade is
untenable. In the original paper the phrase quoted
by Harvey and Anderson is followed by a paragraph
that can be translated as: When we, healthy people, move
the eyegaze up and downwards the upper lid follows this
movement. In Basedow’s patients the lid movement is
absent or reduced to a minimum. It is clear that von
Graefe did not consider loss of lid eye coordination
and reduced amplitude of the lid movement as
different signs.
In any case, there is a surprising paucity of
quantitative investigations on the effect of GUER
on the upper eyelid dynamics. The von Graefe sign
and/or lid lag are simply recorded qualitatively as
absent or present.36,56 Falcão et al measured with
a video technique upper lid saccades in a small
sample of 15 patients with GUER with a mean MRD1
of 6.6 mm. The lid saccades appeared to be grossly
normal, but their amplitudes were reduced compared to a control group.49 Considering that the
upper lid retractors are not always thickened in
GUER, further studies are necessary to establish the
real impact of the disease on lid saccades. Data on
simultaneous lid and eye saccadic recording
with magnetic search coils167 are still lacking in
GUER.
The rate and amplitude of spontaneous blinks are
supposed to be abnormal in GUER. The Stwellwag
sign refers to a marked increase in the blinking
rate134 and the Pochin sign describes the opposite.
We have documented both (Fig. 5). Because
spontaneous blinking activity distributes the tear
film over the ocular surface, its normal function is
essential for the clarity of vision and the maintenance of corneal transparency.34 We are aware of
Fig. 5. High and low spontaneous blinking rate in selected patients with lid retraction. Top: Stellwag sign (frequent
blinking). The blinking rate of this patient was estimated as 155.2 blinks/min. Bottom: Pochin sign (infrequent blinking).
This patient blinked only 2.9 blinks/min.
47
68
just one study that measured several blink parameters such as the rate (blinks/min), amplitude
(degree), maximum velocity (degrees/sec), and
duration (msec) in GUER. The blink rate in patients
with GO was variable, but the mean value (blinks/
min) tended to be lower than in normal patients.
The absolute amplitude of the movements measured in degrees was similar to that of controls;
when the amplitudes were converted to linear
measurement and divided by MRD1, however, the
blinks in GUER had smaller amplitudes compared
to controls. The relationship between maximum
velocity and amplitude, a characteristic known as
main sequence,1 suggested that the blinks of Graves
patients are slower than controls and consequently
have longer durations.59
Although a clear picture of the effect of GUER on
lid physiology is still lacking, patients with Graves
orbitopathy show a constellation of ocular changes
including superficial punctate keratitis, dry eyes,
nocturnal lagophthalmos, superior limbic keratitis,
and corneal ulcers.4,148,161 In the past all of these
changes were attributed to a mechanical effect
resulting from the combination of proptosis and
lid retraction.16,80 In fact, lid retraction increases the
palpebral fissure area, leading to an augmentation
of tear evaporation and tear film hyperosmolarity.84
More recent studies have shown that some of the
ocular surface changes are related to other causes
such as lacrimal gland impairment41 and inflammatory disease.70,162,168
VI. Etiology
Upper eyelid retraction is one of the most
intriguing and disputed clinical manifestations of
GO. Since Dalrymple made his observations on the
LPS ‘‘spasm’’30 in the 19th century, several mechanisms have been proposed to account for upper
eyelid retraction. A systematic review of the literature reveals three different mechanisms that are not
mutually exclusive.
A. MUSCLE HYPERACTION
Hyperaction of the LPS was one of the first
theories proposed to explain GUER and is still
frequently found in the literature.26,47,64,68,69,73,
74,76,78,79,88,101,110,116,122,125,137,145
Dalrymple used
the term ‘‘spasm’’ to express this idea. Small
examined 10 specimens of LPS proximal to the
Whitnall ligament and demonstrated that the
muscle fibers were enlarged compared with the
controls, with minimal signs of fibrosis.144 Innervational influences can also lead to LPS hyperaction.
LPS action is normally linked to that of the superior
48
CRUZ ET AL
rectus. In the setting of inferior rectus restriction,
any effort to maintain vertical eye alignment results
in an increased innervation to both the superior
rectus and LPS. This mechanism has been known
since the last century123 and receives frequent
mention in the literature.21,22,26,27,47,53,55,66,69,73,74,
76,79,107,111,112,118,128,137,140,145,165
Finally, it was
shown that hyperthyroidism in rabbits leads to
a reduced number of palpebral orbicularis oculi
muscle fibers.74 If such an effect exists in humans,
a reduced tonus of the orbicularis muscle would be
accompanied by levator muscle overaction, a finding
commonly seen in Bell palsy.
Since the classical paper by Pochin,123 Müller
muscle hyperactivity has been frequently cited to
account for GUER10,21,22,27,37,46,47,53,55,64,66--69,72--74,76,
78,79,88,101,107,112,115,116,118,122,125,128,137,140,145,147,165
and appears to be the cause of the temporary lid
retraction seen in the early phases of Graves
disease that spontaneously disappears with medical control of hyperthyroidism.35 The basis for
this explanation is the well-known sympathetic
activity of thyroid hormones and the correction
of small amounts of GUER by topical administration of sympathicolytic agents such as
guanethidine.20
B. THE CICATRICIAL OR RESTRICTIVE THEORY
GUER is frequently seen as a restrictive problem.
Similarly to the effects of Graves disease on the
oculorotary muscles, the elastic components of the
upper lid retractors may also become inflamed, with
subsequent fibrosis (intrinsic abnormalities).64 This
oft-cited11,37,67,78,80,125,143,145,147 theory has been
corroborated by a few radiological studies that,
using sagittal slices of magnetic resonance, have
demonstrated that the LPS muscle is frequently
thickened in patients with GUER.83,116
The involvement of Müller muscle in the cicatricial process induced by Graves orbitopathy is
a subject open to debate. Rootman et al did not
find any morphological or immunohistochemical
changes in the Müller muscles of a sample of 32
patients who had undergone müllerectomy.132
In contrast, more recent studies have found
compelling evidence that the Müller muscle is
involved in the inflammation and fibrosis of Graves
orbitopathy.26,140
The occurrence of anomalous cicatricial bands
between the LPS and surrounding tissues such as
the orbicularis oculi muscle and orbital septum was
first proposed by Groove in 198168 and is mentioned
by a number of lid surgeons.26,37,51,66,67,73,74,79,112,145
Such bands have not been observed by the vast
majority of those who have surgically corrected
69
GUER (Table 2). Modern magnetic resonance
imaging of the lids also fails to show this type of
abnormal tissue. Feldon and Levin postulated the
existence of such bands when they noticed that the
dimensions of the superior complex on computed
tomography scans did not correlate with the amount
of lid retraction,51 but this conclusion was not
supported by their data. The superior rectus was
included in the measurements.
C. MECHANICAL FACTORS
Although the occurrence of lid retraction in the
absence of exophthalmos has long been recognized,42,123 extreme degrees of proptosis exacerbate
the retraction mechanically.98 In fact, if the position
of the eye within the orbit is too anterior, the upper
lid margin cannot cover the cornea and tends to rest
on the globe equator. Although clearly a minor
point in the etiology of GUER, this factor is cited in
a number of publications.21,27,55,72,79,118,145
ocular irritation and discomfort.19 The drug, useful
only in the mild forms of GUER, was poorly
tolerated and is no longer administered.16,39,76
Botulinum toxin type A offers a different approach to the medical treatment of GUER. The
drug acts on the neuromuscular junction, blocking
acetylcholine release. With respect to GUER, its
action is directed to the LPS muscle, provoking
a temporary weakness. This type of chemodenervation is a good option for patients who cannot
undergo or do not desire surgical treatment12,31,119,138,139,157 and can also be used as
a temporary treatment for exposure keratitis and
conjunctivitis during the active phase of the disease.
The effect lasts 3--4 months, and there is a risk of
diplopia and ptosis.40,153
Finally, in the early inflammatory phase of the
orbitopathy, subconjunctival injection of triamcinolone has been reported to have reduced the
retraction. The mechanism of this effect is probably
the triamcinolone’s anti-inflammantory and antifibrotic actions.25
D. SUMMARY
The large body of clinical observations supporting
different mechanisms is strong evidence that GUER
is multifactorial. Small and temporary lid retractions
observed in the early phases of Graves disease are
probably due to the sympathetic effects of hyperthyroidism. As the orbitopathy progresses, the
inflammatory process involves both the levator and
Müller muscles. Muscle overaction can be the result
of such process or results from inferior rectus
restriction. Lid retractions that are variable160 and
do not show any evidence of lid lag56,69 may be
explained by muscle overaction.
A restrictive pattern of retraction can be explained by tissue changes and fibrosis in the lid
retractors. It is unlikely that abnormal cicatricial
bands play a role in the etiology of lid retraction.
The mechanical influence of large amounts of
proptosis is also a minor effect. Patients with GUER
are often not proptotic.21,79,163 Although lid retraction may be improved after orbital decompression, this surgery does not fully correct lid
retraction.76,82,163
VII. Management
A. MEDICAL TREATMENT
The first attempts to control GUER medically
were during the 1960s, when it was demonstrated
that topical administration of adrenergic blocking
agents such as guanethidine reduced retraction.20,60
This treatment had limited success because of drug
side effects such as vasodilatation, irritation, and
B. SURGICAL CORRECTION
The early attempts to alleviate GUER consisted of
cervical sympathectomy, tarsorrhaphy, and blepharorrhaphy.62,80 The history of the surgical techniques
(Table 2) specifically aimed to debilitate the upper
eyelid retractors in GUER8,10,11,14--16,18,21,22,27,29,37-39,45,52,53,55,62,66,67,76--78,80--82,85,90,92--94,99,100,102,104,105,
107,110,111,113--115,117,118,122,125,128,129,131,137,141,143,145,147,
151,152,154--156,163,166
started in 1934 when Goldstein
published his posterior approach to recess the LPS
aponeurosis.62 Moran was probably the first to
address the LPS muscle by an anterior approach
and to pay attention to the contour abnormalities.110 He performed LPS disinsertion at the tarsal
border and noticed that in some cases there was
a residual lateral retraction. In order to manage this
problem, he advocated myotomy, more intense on
the lateral aspect of the muscle. The need to
increase the debilitation of the retractors laterally
was accepted as a key step in surgical procedures.16,22,27,29,38,45,52,76,77,81,82,92,100,102,107,110,114,117,
129,151,166
Baylis8 and Meltzer107 subsequently used
an anterior approach but it was only when Harvey
and Anderson76 detailed the advantages of the wide
exposure obtained by the anterior approach that
this technique became a standard option for GUER
correction.
In 1965, Henderson described the combination of
müllerectomy and graded recession of the LPS by
a posterior approach.80 At the same time, Callahan
introduced the use of an absorbable spacer to
lengthen the LPS.18 Meltzer replaced this alloplastic
49
50
Müller’s muscle recession þ LPS recession
Müller’s muscle recession þ LPS recession þ spacer
Müllerectomy þ LPS recession
LPS marginal myotomy
LPS recession þ Spacer
Müller’s muscle recession þ LPS marginal myotomy
LPS recession þ spacer
Müllerectomy
Müllerectomy þ LPS recession þ lateral tarsorrhaphy
LPS recession þ Müller’s muscle recession þ tarsal
pedicle rotational flaps
Müllerectomy þ LPS recession þ tarsal fracture þ spacer
Cross-face free muscle--tendon graft
lateral tarsorrhaphy
Müllerectomy
Müllerectomy (2)
Müllerectomy þ LPS tenotomies (11)
Müllerectomy þ LPS recession (28)
LPS recession
LPS recession
LPS recession
LPS recession þ hang loose sutures
LPS recession/myotomy
LPS recession þ spacer
Transverse tarsotomy
Müller’s muscle recession þ LPS recession þ conjunctiva
recession
Müllerectomy
Müllerectomy þ LPS partial tenotomy
Müllerectomy
Müllerectomy þ LPS recession þ spacer
Technique
Posterior
Posterior
Anterior
Anterior
Posterior
Anterior
Anterior
Posterior
Posterior
Posterior
Anterior
Posterior
Anterior
Anterior
Anterior
Posterior
Anterior
Anterior
Anterior
Posterior
Anterior
Posterior
Anterior
Anterior
Posterior
Anterior
Posterior
Posterior
Posterior
Anterior
Posterior
Posterior
Posterior
Anterior
Posterior
Anterior
Posterior
Posterior
Approach
No
Sclera
No
No
No
No
Sclera
No
No
No
No
No
Fascia lata, nasal
cartilage, Sclera
No
No
No
No
No
Sclera, collagen film,
dura-mater
not stated
Sclera
No
No
Sclera
No
No
No
No
Sclera
No
No
No
No
No
No
Collagen film
No
No
Spacer
Not stated
Not stated
1/2
Not stated
Not stated
Not stated
Not stated
Not stated/2
Not stated/11
Not stated/28
Not stated/50
Not stated/17
Not stated/6
Not stated
Not stated
40/61
4/5
7/Not stated
14/24
32/53
Not stated
Not stated
Not stated
12/22
Not stated/114
1/2
1/2
2/4
1/1
2/3
Not stated
Not stated
5/8
12/21
27/41
Not stated
10/20
17/29
Patients/Lids
Shorr (1986)141
Hedin (1985)78
Nicolai (1983)115
Leone (1984)99
Hurwitz (1983)82
Dixon (1982)37
Waller (1982)163
Kohn (1983)94
Chalfin (1979)22
Grove (1980)67
Doxanas (1981)39
Harvey (1981)76
Putterman (1981)128
Smith (1981)145
Meltzer (1978)107
Buffam (1978)16
Baylis (1976)8
Putterman (1972)125
Goldstein (1934))
Moran (1956)110
Henderson (1965)80
Callahan (1965)18
Schimek (1972)137
62
70
Author (Year)
Surgical Techniques for Graves Upper Eyelid Retraction Correction
TABLE 2
CRUZ ET AL
LPS/Müller’s muscle transposition
LPS division þ hang-back sutures
Blepharotomy þ central suture placement
Blepharotomy with intact conjunctival central bridge
Blepharotomy
Blepharotomy
Müller’s muscle recession
LPS recession
LPS recession
Myotomy
Müllerectomy/LPS recession
LPS recession þ adjustable suture
LPS recession
LPS recession þ Müller’s muscle recession
LPS lengthening
Müller’s muscle recession þ LPS recession with cautery
Müller’s muscle recession þ LPS recession þ myotomy
þ adjustable suture
Müller’s muscle recession
Müllerectomy
LPS recession
Müller’s muscle recession þ LPS 2--3 transverse incisions
Müller’s muscle recession þ LPS recession þ myotomy
þ adjustable suture
LPS castellated lengthening
Müller’s muscle recession þ LPS recession þ medial
transposition of lateral horn
Müller’s muscle recession þ LPS recession þ adjustable suture
Marginal myotomy þ lateral tarsorrhaphy
LPS recession/Müller’s muscle recession
LPS 5 levator palpebrae superioris muscle.
Khan (2002)92
McNab (2004)105
Elner (2004)44
Ben Simon (2005)10
Hintschich (2005)81
Ivekovic (2005)85
McCracken (2008)104
Kikkawa (2010)93
Woog (1996)166
Tremolada (1997)154
Mourits (1999)114
Fenton (2002)52
Piggot (1995)122
Ceisler (1995)21
Olver (1995)118
Roncevic (1995)131
Tucker (1995)155
Uccello (1994)156
Morax (1987)111
Small (1988)143
Beyer-Machule (1989)11
Downes (1989)38
Harvey (1991)77
Mourits (1991)113
Older (1991)117
Levine (1991)100
Soares (1991)147
Liu (1993)102
Colla (1993)27
Thornton (1994)152
Collin (1994)29
Putterman (1986)129
Bonavolontà (1986)14
Thaller (1987)151
Anterior
Anterior
Anterior
Posterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior/Posterior
Anterior
Anterior
Posterior
Posterior
Posterior
Posterior
Anterior
Posterior
Posterior
Posterior
Posterior
Posterior
Anterior
Anterior
Anterior
Anterior
Posterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior
Anterior/Posterior
Adjustable suture
No
No
Mersilene or
vycril meshes
No
Adjustable suture
No
No
No
No
No
No
No
No
No
No
No
No
No
Adjustable suture
No
No
No
No
Sclera
No
Sclera, Goretex
No
Sclera/fascia lata
Mersilene mesh
Adjustable suture
Sclera
No
No
No
No
No
No
No
10/12
21/38
32/50
78/107
41/60
4/5
7/13
20/20
9/12
16/32
50/78
41/45
4/6
37/72
29/Not stated
20/Not stated
11/Not stated
22/33
51/99
7/9
92/156
51/Not stated
11/Not stated
30/Not stated
13/Not stated
5/Not stated
10/17
14/25
Not stated
Not stated/4
12/22
47/78
15/22
15/30
10/15
9/9
11/15
Not stated
5/Not stated
71
51
72
material by fresh or banked sclera and provided
quantitative guidelines to fashion the spacer.107 The
use of sclera53 and other spacers such as autogenous
tarsus,15 goretex,111 and mersilene meshes38 on the
upper eyelid was continued until the late 1980s39,78
and then almost disappeared from the literature.
Putterman refined Henderson’s procedure using
local anesthesia to control the amount of correction
during surgery. The patient was placed in sitting
position several times during the operation in order
to observe lid’s position in different directions of
vertical gaze. He also pointed out that only a subset
of the patients needed LPS surgery after the
excision of Müller muscle.125 In a subsequent
publication he highlighted several important concepts: the surgery was mainly directed to the lateral
two-thirds of the lid, the aponeurosis was recessed in
a graded manner, and a sclera spacer was unnecessary.22 An interesting technical detail in the
posterior approach is the conjunctival closure. Since
Henderson’s original description, most who perform surgery by the posterior route closed the
conjunctiva at the end of the procedure. Bonavolontà was the first to point out that this step is
unnecessary.14 We concur and have never closed the
conjunctiva following any type of Müllerectomy.
Medial and lateral LPS myotomies advocated by
Grove66--68 is seldom mentioned by other authors.145
Small was the first to use an adjustable suture in
order to control the lid margin position during
surgery or in the early postoperative period,143
a theme that was readdressed by Collin and
Tucker.29,155 Adjustable sutures are not used by the
majority of surgeons probably because the final
results are seen only 4 or 6 weeks after surgery.
In summary, the plethora of technical variations
described for the correction of GUER strongly
suggests that the results are variable with any type
of surgery. The upper lid retractors (LPS and Müller
muscle) can be debilitated separately or in combination by an anterior or posterior approach. The
muscles can be recessed, partially resected, or
lengthened. Various materials have been tried as
spacers between the recessed retractors and the
upper tarsal border, but the results were not better
than those obtained by just weakening the retractors. Residual lateral retraction is a well-known
phenomenon, and most surgeons do more aggressive surgery laterally.
A through-and-through blepharotomy has been
tried as a quick and reliable method to lower the lid
margin. One advantage of blepharotomy is to
address a possible fibrosis of the conjunctival
substantia propria.90 Kikkawa, however, studied the
histopathology of the superior palpebral conjunctiva of 20 patients who had undergone surgical
52
CRUZ ET AL
correction of GUER and were in the quiescent
phase of the disease. All patients underwent surgery
by anterior approach through an upper lid incision.
After recession of both the LPS and Müller’s muscle
in a single complex, a specimen of central palpebral
conjunctiva just above the tarsus was obtained for
biopsy. The specimens were compared to a control
group of patients undergoing surgery for ptosis by
posterior approach. No statistical difference was
observed in fibrosis or quantitative fibroblast count
between the two groups.93
Occasionally, there are new and unusual approaches proposed. An example of this is the
technique of Nicolai and Cruysberg, two British plastic
surgeons who corrected GUER with cross-face free
muscle grafts.115 This involves denervation of the
extensor digitorum brevis muscle, a sub-periosteal
dissection along the lower orbital rim, and the
preparation of a tunnel through the bony nasal
skeleton using a Z-incision between the glabella and
the nasal bridge. Unsurprisingly given the technical
challenges involved, this procedure has not been
mentioned in the ophthalmic literature until now.
VIII. Conclusion
The mechanisms responsible for GUER are still
a subject of discussion. Although this lid positional
abnormality seems to be a multifactorial problem,
no subtypes of GUER have been distinguished. The
plethora of surgical techniques that have been
published for GUER correction suggests that there
is no consensus among surgeons. The effects of
GUER on lid saccades and spontaneous blinking
activity is still a subject of research.
IX. Method of Literature Search
The authors conducted a search of the Medline
database using the following key words: Graves
opthalmopathy, Graves orbitopathy, upper lid retraction,
Graves disease, and Basedow disease. In addition,
selected references cited in the articles found
through the literature search were also included.
Most articles cited were published in English. A few
historical articles in German were translated and
also included.
X. Disclosure
The authors report no proprietary or commercial
interest in any product mentioned or concept
discussed in this article.
73
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dysthyroid ophthalmopathy: long-term results. J Craniomaxillofac Surg. 1995;23:355--62
132. Rootman J, Patel S, Berry K, et al. Pathological and clinical
study of Muller’s muscle in Graves’ ophthalmopathy. Can J
Ophthalmol. 1987;22:32--6
133. Sarver B, Putterman A. Margin limbal distance to determine amount of levator resection. Arch Ophthalmol.
1985;103:354--6
134. Schaumberg DA, Dana R, Buring JE, et al. Prevalence of
dry eye disease among US men: estimates from the
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763--8
135. Schechter RJ. Ptosis with contralateral lid retraction due to
excessive innervation of the levator palpebrae superiorus.
Ann Ophthalmol. 1978;10:1324--8
136. Schellini SA, Manetti LD, Silva MRBdM. Eyelid retraction
during pregnancy. Case report. Arq Bras Oftal. 1998;61:
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137. Schimek RA. Surgical management of ocular complications
of Graves’ disease. Arch Ophthalmol. 1972;87:655--64
138. Scott AB. Injection treatment of endocrine orbital myopathy. Doc Ophthalmol. 1984;58:141--5
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140. Shih MJ, Liao SL, Kuo KT, et al. Molecular pathology of
Muller’s muscle in Graves’ ophthalmopathy. J Clin Endocrinol Metab. 2006;91:1159--67
141. Shorr N, Seiff SR. The four stages of surgical rehabilitation
of the patient with dysthyroid ophthalmopathy. Ophthalmology. 1986;93:476--83
142. Small R, Sabates N, Burrows D. The measurement and
definition of ptosis. Ophthalmic Plast Reconstr Surg. 1989;
5:171--5
143. Small RG. Upper eyelid retraction in Graves’ ophthalmopathy: a new surgical technique and a study of the
abnormal levator muscle. Trans Am Ophthalmol Soc. 1988;
86:725--93
144. Small RG. Enlargement of levator palpebrae superioris
muscle fibers in Graves’ ophthalmopathy. Ophthalmology.
1989;96:424--30
145. Smith B, Lisman RD. Cosmetic correction of eyelid
deformities associated with exophthalmos. Clin Plast Surg.
1981;8:777--92
146. Smith JL. Lid position in neuro-ophthalmology. J Clin
Neuro-ophthalmol. 1987;7:149--50
147. Soares EJC, França VP. Lengthening of the upper lid
retractors. Orbit. 1991;10:133--40
148. Sokol JA, Foulks GN, Haider A, et al. Ocular surface effects
of thyroid disease. Ocul Surf. 2010;8:29--39
149. Stout AU, Borchert M. Etiology of eyelid retraction in
children: a retrospective study. J Pediatr Ophthalmol
Strabismus. 1993;30:96--9
150. Summerskill WH, Molnar GD. Eye signs in hepatic
cirrhosis. N Engl J Med. 1962;266:1244--8
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152. Thornton WR. Combined approach to eyelid surgery in
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Reprint address: Dr. Antonio Augusto Velasco Cruz, MD,
Department of Ophthalmology, Otorhinolaryngology, and Head
and Neck Surgery, School of Medicine of Ribeirão Preto,
University of São Paulo, Avenida Bandeirantes 3900, 14049-900,
Ribeirão Preto, São Paulo, Brazil. e-mail: [email protected].
Outline
I. Introduction
A. Historical background
II. Diagnosis
A. Normal resting upper eyelid position
B. Lateral lid flare sign
C. Methods of measurement
III. Prevalence
IV. Differential diagnosis
V. Upper eyelid movements and ocular surface
changes
56
VI. Etiology
A.
B.
C.
D.
Muscle hyperaction
The cicatricial or restrictive theory
Mechanical factors
Summary
VII. Management
A. Medical treatment
B. Surgical correction
VIII. Conclusion
IX. Method of literature search
X. Disclosure
OBJETIVOS
1. Analisar quantitativamente o contorno palpebral superior de um grupo
controle e de doentes com retração palpebral superior secundária à OG.
Determinar as anomalias de contorno induzidas pela retração palpebral
superior. Verificar qual o papel da magnitude da retração palpebral e da
exoftalmometria nas anomalias do contorno da pálpebra superior por
OG.
2. Validar um novo método para registar e medir os movimentos das
pálpebras, utilizando um sistema de vídeo. Comparação dos resultados
com os obtidos pelo magnetic search coil (método "gold standard") num
grupo de indivíduos normais.
3. Determinar o efeito da correção cirúrgica da retração palpebral superior
da OG no contorno palpebral. Efetuar a análise quantitativa do contorno
palpebral superior pré e pós-operatório numa amostra de doentes
submetidos a cirurgia de retração palpebral. Identificar as anomalias de
contorno induzidas pela cirurgia e determinar o seu efeito no mau
resultado estético e/ou funcional.
4. Determinar o efeito da correção cirúrgica da retração palpebral superior
da OG (por müllerectomia via posterior) na cinética palpebral.
57
Capítulo II
- Anomalias de contorno induzidas pela retração palpebral superior da orbitopatia de Graves
______________________________________________________________
Anomalias de contorno induzidas pela retração palpebral superior da
orbitopatia de Graves
Anomalias de contorno introduzidas pela retração palpebral superior da orbitopatia de Graves
ORIGINAL INVESTIGATION
Lateral and Medial Upper Eyelid Contour Abnormalities
in Graves Orbitopathy: The Influence of the Degree of
Retraction
Sara Filipa Teixeira Ribeiro, M.D.*, Gherusa Helena Milbratz, M.D.†, Denny Marcos Garcia, B.Sc.†,
Vitor Leal Fernandes, M.D.*, Amândio Rocha-Sousa, M.D.*, Fernando Manuel Falcão-Reis, M.D.*,
and Antonio Augusto Velasco Cruz, Ph.D.†
*
*Department
of Ophthalmology, Centro Hospitalar de São João EPE, School of Medicine of Porto, University of Porto,
Porto, Portugal; and †Department of Ophthalmology, Otorhinolaryngology and Head and Neck Surgery, Hospital das
Clínicas-Campus, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, São Paulo, Brazil
Purpose: To determine the location of contour abnormalities
in Graves upper eyelid retraction.
Methods: Multiple midpupil angular eyelid distances of 75
upper eyelids of 55 patients (mean age = 41.7 ± 13.3 SD years)
in the inactive phase of Graves orbitopathy were measured with
a recently developed custom-made software. Sixty eyelids of
60 normal subjects were also measured as a control group. A
contour peak was defined by the highest midpupil angular eyelid
distance normalized (divided) by the superior limit of normality
(mean + 2SD).
Results: In 45 eyelids (60%), the peaks were lateral between
120° and 150°. For high levels of retraction, the peaks tended
to be centrally located with a substantial number of medial
deformities (30 eyelids). Although the lateral and medial peaks
were not affected by exophthalmometry, there was a statistically
significant increase of medial peaks when midpupil eyelid
distance was greater than 6.75 mm (χ2 = 5.20, p = 0.02).
Conclusions: Lateral contour abnormalities are more
frequent than medial deformities. With minor degrees of
retraction, there is a predominance of lateral peaks. With higher
degrees of retraction, the number of medial abnormalities is
similar to the lateral ones.
(Ophthal Plast Reconstr Surg
g 2013;29:40–43)
U
pper eyelid retraction is the most common and characteristic sign of Graves orbitopathy (GO).1 The eyelids affected
by this disease, besides being retracted, often show contour
abnormalities. The most cited deformity is the enhanced
retraction of the lateral aspect of the eyelid described as lateral flare sign.2 Although the eyelid contour changes in GO are
well-known,2–4 the literature on the mechanisms implicated in
their etiology is quite sparse. In this article, a new quantitative
method5 was used to precisely determine the location of the
contour peaks in a large sample of eyelids with GO retraction.
The results show that a substantial number of eyelids display
Accepted for publication November 3, 2012.
The authors have no financial or conflict of interest to disclose.
Address correspondence and reprint requests to Antonio Augusto Velasco
Cruz, PhD, Department of Ophthalmology, Otorhinolaryngology and Head
and Neck Surgery, School of Medicine of Ribeirão Preto, University of
São Paulo, Ribeirão Preto, 14049-900 São Paulo, Brazil. E-mail: aavecruz.
[email protected]
DOI: 10.1097/IOP.0b013e3182747537
medial contour deformities. Moreover, the level of retraction
appears to be a key factor for the development of contour
anomalies.
METHODS
Subjects. In this study, a large sample of patients was included
in the inactive phase of GO examined either at Hospital das Clínicas
de Ribeirão Preto (São Paulo, Brazil) or at the Centro Hospitalar de
São João, EPE (Porto, Portugal). There were 75 eyes of 55 patients (46
women) ranging in age from 24 to 55 (mean = 41.7 ± 13.3 SD) years.
The control group comprises 60 eyes of 60 normal subjects (41 women)
ranging in age from 17 to 66 (mean = 40.1 ± 11.9 SD) years. No patient
had any disease or surgery that could affect eyelid contour or function.
For all patients, Hertel exophthalmometric readings and images
of their palpebral fissure in the primary position of gaze were obtained.
In cases of symmetrical eyelid retraction, the eye to be analyzed was
randomly chosen. If the retraction was asymmetric, OU were selected.
Patients with strabismus or with a history of orbital or eyelid surgery
were excluded.
Eyelid Contour Analysis. A custom-made software developed in
the Matlab (MathWorks, Natick, MA, U.S.A.) by 1 of the authors
(D.M.G.) was used to analyze the palpebral fissure images.5 After the
pupil center was arbitrarily defined, the software drew a vertical line
at the 12 o’clock position (90°) and 6 radial lines 15° apart from the
midline in the temporal (105°, 120°, 135°,150°, 165°, and 180°)
and nasal (75°, 60°, 45°, 30°, 15°, and 0°) sectors of the eyelid fissure. The only task of the observer was to mark the intersections of
the radial lines on the eyelid margin. The length of the line which intersects the eyelid margin at the 12 o’clock position (90°) is the conventional midpupil lid distance commonly used to record the height of
the upper eyelid with a millimeter ruler in clinical settings. The other
lines can be seen as radial midpupil lid distances. The lengths of all
lines were automatically calculated by the software and displayed on
a polar plot, which represented the quantification of the whole eyelid
contour (Fig. 1). A contour peak was defined by the highest midpupil
angular eyelid distance normalized (divided) by the superior limit of
normality (mean + 2SD).
Statistical Analysis. The chi-square test was used to determine the association between the occurrence of medial or lateral peaks with Hertel
readings and midpupil lid distance at 90°. The t test for independent
samples was used to compare exophthalmometry and midpupil eyelid
distance at 90° between Graves patients and controls.
Ophthal Plast Reconstr Surg,
g Vol. 29, No. 1, 2013
61
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Upper Eyelid Contour Abnormalities in Graves Eyelid Retraction
FIG. 1. Left, multiple midpupil eyelid lines equally angularly (15°). Right, polar plot of the angular distances between pupil center and
eyelid margin.
FIG. 2. Angular distribution of the contour peaks.
RESULTS
Figure 2 shows the angular distribution of the contour
peaks. In 45 eyelids (60%), the peaks were lateral. Medial peaks
were seen in 30 eyelids (40%). Age was not associated with
the distribution of lateral or medial peaks (χ2 = 0.32, p = 0.57).
Typical cases of lateral and medial contour anomalies are shown
in Figure 3.
As expected, the mean Hertel reading was different
(tt = 11.75, p < 0.001) between patients (20.8 mm) and controls
(15.7 mm). However, proptosis was neither correlated with the
level of retraction nor associated with the presence of lateral and
medial peaks (Fig. 4).
As shown in Figure 5, when the retraction was moderate, the contours peaks were predominantly found on the lateral
portion of the eyelid between 150° and 120°. When the magnitude of retraction increased, the peaks clearly tended to become
more central. For high degrees of retraction (midpupil lid distance 90° >6.75 mm), there were approximately equal numbers
of eyelids with lateral and medial peaks. This finding means that
the occurrence of medial peaks is significantly associated with
high degrees of retraction (χ2 = 5.20, p = 0.02).
DISCUSSION
Eyelid contour abnormalities in Graves upper eyelid
retraction have been discussed since the early 50s. Moran6 was
the first to notice that, after surgical correction of retraction, the
temporal side of some eyelids was too high and with a bizarre
appearance. This postoperative lateral deformity was soon recognized as a key element to be addressed during eyelid retraction surgery with a more aggressive dissection on the temporal
side of the eyelid.2,6–8 Despite the widespread awareness of the
importance of achieving a proper postoperative contour, several
surgeons have pointed out that contour abnormalities are a common complication of any surgical type of correction of Graves
eyelid retraction.
The main difficulty in analyzing contour deformities is
related to the methodological problem of how to express complex curved lines in a simple way. Until recently, eyelid contours
were evaluated subjectively and abnormalities were named as
gothic arches, notches, peaks, lateral flare, and so on.2,9–11 It
should be noted that the determination of the highest point
of the eyelid contour has not the same meaning as measuring
lateral or medial peaks. As elegantly shown by Flynn et al.,12
when a horizontal line is moved until it touches the eyelid, the
point of contact expresses the location of the contour where the
first derivative is equal to zero.13 The highest point of the contour is always near the center. A contour may have a medial or
lateral deformation and still the highest point of the contour will
be close to the center. When multiple midpupil eyelid distances
are represented graphically, contour deformities can be visualized and quantified at any location.5
There is no literature describing the spectrum of
lateral or medial contour abnormalities in Graves upper
eyelid retraction. The results confirm the old notion that
the degree of retraction is not correlated with proptosis.14
The data also concur with the time-honored concept that
lateral contour abnormalities are frequently found in eyelids
with retraction.2,6–10,15–18 The so-called lateral eyelid flare is
explained by the important lateral extensions of Müller’s
muscle19 or by the facts that the superolateral intermuscular
septum fibers are enlarged in GO20 and the lateral horn of
the levator palpebrae superioris muscle is stronger than the
medial horn.19,21 The measurements indicate that these lateral
deformations are located mainly between 120° and 150°.
However, for high levels of retraction, the lateral deformities
are found near the center at 105° and the number of medial
peaks increases. The occurrence of medial peaks is a new
finding, which has theoretical and practical relevance. From
a theoretical point of view, the findings might indicate that
the association of high degrees of retraction with peaks that
are located more centrally may be a reflex of the normal
force arrangement that set up the highest point of the eyelid
contour close to the center. Besides, Graves patients show
a large interindividual variability in the levator or Müller’s
© 2013 The American Society of Ophthalmic Plastic and Reconstructive Surgery, Inc.
62
g Vol. 29, No. 1, 2013
S. F. Teixeira Ribeiro et al.
FIG. 3. Left, clinical pictures of eyelid fissures from different patients with Graves orbitopathy. Middle, upper eyelid contours expressed
by multiple midpupil lid distances (MPLDs) (solid line).
e The dotted lines express the normal range (mean ± 2SD). Right, location of the
contour peaks. A, Typical example of well-known lateral eyelid flare. B, C, and D, Examples of medial peaks.
FIG. 4. Left, V
Variation of midpupil lid distance (MPLD) at 90° versus exophthalmometry. Right, lateral and medial peaks versus
exophthalmometry.
muscle distribution of forces along the eyelid margin. The
demonstration that there is a spectrum of eyelid deformation
in GO retraction has a clear surgical importance. To correct
the retraction, the surgeon has to lower the eyelid margin and
at the same time achieve a normal, smooth contour similar to
a second-degree function (parabola).5 A careful preoperative
contour evaluation is essential. The dissection on the lateral
aspect of the eyelid should not always be more important.
63
g Vol. 29, No. 1, 2013
FIG. 5. Lateral and medial peaks versus midpupil lid distance
(MPLD) at 90°.
The lack of a proper contour evaluation before surgery might
be a factor leading to the well-known postoperative contour
abnormalities.
ACKNOWLEDGMENTS
The authors thank Sociedade Portuguesa de Oftalmologia for providing general support. ARS was supported by Portuguese grants
from FCT (PTDC/SAU-ORG/110683/2009), through Unidade I &
D Cardiovascular (51/94-FCT).
REFERENCES
1. Lebensohn JE. The eye signs of Graves’ disease. Am J Ophthalmol
1964;57:680–1.
2. Waller RR. Eyelid malpositions in Graves’ ophthalmopathy. Trans
Am Ophthalmol Soc 1982;80:855–930.
3. Cruz AA, Akaishi PM, Coelho RP. Quantitative comparison between upper eyelid retraction induced voluntarily and by Graves
orbitopathy. Ophthal Plast Reconstr Surg
g 2003;19:212–5.
Upper Eyelid Contour Abnormalities in Graves Eyelid Retraction
4. Cruz AA, Coelho RP, Baccega A, et al. Digital image processing
measurement of the upper eyelid contour in Graves disease and
congenital blepharoptosis. Ophthalmology 1998;105:913–8.
5. Milbratz GH, Garcia DM, Guimarães FC, et al. Multiple radial
midpupil lid distances: A simple method for lid contour analysis.
Ophthalmology 2012;119:625–8.
6. Moran RE. The correction of exophthalmos and levator spasm.
Plast Reconstr Surg (1946) 1956;18:411–26.
7. Putterman AM, Urist M. Surgical treatment of upper eyelid retraction. Arch Ophthalmoll 1972;87:401–5.
8. Buffam FV, Rootman J. Lid retraction—its diagnosis and treatment.
Int Ophthalmol Clin 1978;18:75–86.
9. Harvey JT, Anderson RL. The aponeurotic approach to eyelid
retraction. Ophthalmology 1981;88:513–24.
10. Older JJ. Surgical treatment of eyelid retraction associated with thyroid
eye disease. Ophthalmic Surgg 1991;22:318–22; discussion 322–3.
11. Shore JW. Graves disease: correcting upper eyelid retraction
[letter]. Ophthalmology 1996;103:1713–4.
12. Flynn TH, Rose GE, Shah-Desai SD. Digital image analysis to
characterize the upper lid marginal peak after levator aponeurosis
repair. Ophthal Plast Reconstr Surg
g 2011;27:12–4.
13. Cruz AA, Garcia DM. Re: “Digital image analysis to characterize the
upper lid marginal peak after levator aponeurosis repair.” Ophthal
Plast Reconstr Surgg 2011;27:308–9; author reply 309.
14. Frueh BR. Graves’ eye disease: orbital compliance and other physical measurements. Trans Am Ophthalmol Soc 1984;82:492–598.
15. Levine MR, Chu A. Surgical treatment of thyroid-related lid retraction:
a new variation. Ophthalmic Surg
g 1991;22:90–4.
16. Liu D. Surgical correction of upper eyelid retraction. Ophthalmic
Surgg 1993;24:323–7.
17. Elner VM, Hassan AS, Frueh BR. Graded full-thickness anterior blepharotomy for upper eyelid retraction. Arch Ophthalmol
2004;122:55–60.
18. Ceisler EJ, Bilyk JR, Rubin PA, et al. Results of Müllerotomy and
levator aponeurosis transposition for the correction of upper eyelid
retraction in Graves disease. Ophthalmology 1995;102:483–92.
19. Morton AD, Elner VM, Lemke BN, et al. Lateral extensions of the
Müller muscle. Arch Ophthalmoll 1996;114:1486–8.
20. Goodall KL, Jackson A, Leatherbarrow B, et al. Enlargement of the
tensor intermuscularis muscle in Graves’ ophthalmopathy. A computed tomographic and magnetic resonance imaging study. Arch
Ophthalmoll 1995;113:1286–9.
21. Anderson RL, Beard C. The levator aponeurosis. Attachments and
their clinical significance. Arch Ophthalmoll 1977;95:1437–41.
64
Capítulo III
– Validação de um sistema de vídeo digital como método de registo e quantificação dos movimentos palpebrais
______________________________________________________________
Validação de um sistema de vídeo digital como método de registo e
quantificação dos movimentos palpebrais
Validação de um sistema de vídeo digital como método de registo e quantificação dos movimentos palpebrais
Two-Dimensional Video Analysis of the Upper Eyelid
Motion During Spontaneous Blinking
Sarah P. F. Wambier, M.D.*, Sara F. Ribeiro, M.D.†, Denny M. Garcia, B.Sc.*,
Rodrigo R. Brigato, M.D.*, Andre Messias, M.D.*, and Antonio A. V. Cruz, M.D.‡
* Department of Ophthalmology, Otorhinolaryngology and Head and Neck Surgery, School of Medicine of Ribeirão
Preto, University of São Paulo, Brazil; † Department of Senses Organs, Ophthalmology Unit, Faculty of Medicine,
University of Porto, Portugal; and ‡Department of Ophthalmology, Otorhinolaryngology and Head and Neck Surgery,
School of Medicine of Ribeirão Preto, University of São Paulo, Brazil
Purpose:: To validate and to report the results of a new
inexpensive video-based method to measure upper eyelid
motion during spontaneous blinks.
Methods:: Spontaneous blinks were simultaneously recorded
in 21 healthy adult subjects for 5 minutes with magnetic search
coil (MSC) and a portable video system (VDS) composed by a
commercial high-speed camera coupled to a laptop computer
and a blue light-emitting diode. Agreement between the 2
methods was assessed using qualitative comparison of the
eyelid motion traces and Bland-Altman plots.
Results:: The blink traces registered with both methods were
virtually identical. With the either method, the relationship
between amplitude and maximum velocity was well fitted
by linear regression with mean r values = 0.81 (MSC) and
0.85 (VDS). Bland-Altman plots showed good agreement
between methods. The mean ± SE differences of amplitude
(0.06 ± 0.17 mm) and maximum velocity (5.0 ± 3.4 mm/s) were
not significant. With the VDS, it was also possible to quantify the
horizontal component of the blink movements. The amplitude
of the horizontal shift of the eyelid during blinks was 40% of the
vertical downward phase of the movement.
Conclusions:: Blinking kinematics can be precisely measured
using a simple and inexpensive video system suitable for
clinical settings.
g 2014;30:146–151)
S
pontaneous blinking (SB) continuously spreads lacrimal
fluid over the cornea, maintaining the stability of the tear
film. Upper eyelid motion is thus essential for protecting the
eye surface and ensuring visual function..1Spontaneous blinks
are compromised in many disorders that are routinely operated
On leave of absence of Antonio A. V. Cruz, M.D., at the School of
Medicine of Ribeirão Preto and Craniofacial Research Support Center, he
can be contacted at King Khaled Eye Specialist Hospital, Riyadh, Saudi
Arabia, and Johns Hopkins University, Maryland, U.S.A.
Accepted for publication August 30, 2013.
The authors have no financial or conflicts of interest to disclose.
Supported by grants from the Brazilian Research Council (CNPq),
Brasília, Brazil, #301865/2009-4 and from the Craniofacial Research
Support Center of the University of São Paulo.
Address correspondence and reprint requests to Antonio A. V. Cruz, M.D.,
Department of Ophthalmology, Otorhinolaryngology, and Head and Neck
Surgery, School of Medicine of Ribeirão Preto, University of São Paulo, São
Paulo, Brazil. E-mail: [email protected]
DOI: 10.1097/IOP.0000000000000031
by oculoplastic surgeons such as ptosis, cicatricial ectropion,
eyelid retraction, and cicatricial or paralytic lagophthalmos.
However, as eyelid movements are usually measured in a laboratory setting only,2–4 there is an astonishing paucity of clinical
data on the effects of these interventions on SB.
The present study validates a new, inexpensive, and portable method to register and precisely measure blinking kinematics that can be easily used in daily clinical practice.
METHODS
This research adhered to the tenets of the Declaration of
Helsinki. The local Ethics Committee approved the study, and all subjects provided written informed consent.
Twenty-one healthy adult subjects (9 females) aging from 22 to 58
years (mean ± SD of 31.8 ± 8.9 years) were tested. None of the subjects had
eyelid disease or any neurologic or ophthalmic abnormalities. SB was registered simultaneously with a magnetic search coil (MSC) and video system
(VDS) during 5 minutes while the subjects watched a commercial movie.
MSC consisted of an oscillating magnetic field produced by a
cubic frame. A small coil (3.8 mm diameter, 30 turns, 30 mg, copper
wire 0.102 mm in diameter) is taped to the upper eyelid close to the
margin, above the pupil. Due to the flux generated by the magnetic field,
a current is induced inside the coil. This sign is proportional to the sine
of the angle between the coil and the magnetic field orientation. The
conversion of electronic signs to spatial position is possible because as
the eyelid rotates over the curved ocular surface, the angular shifts of the
coil are proportional to its position.5
The recordings were low-pass filtered at 10 kHz, amplified 20,000
times, digitized with 12-bit precision, and sampled at 200 Hz by a computed system (Remel Laboratories, San Antonio, TX, U.S.A.), providing
detection of eyelid rotations with a spatial resolution of 0.1° (equivalent
to a linear eyelid motion of 0.02 mm) at a temporal resolution of 200 Hz.
To simultaneously register eyelid movements with the MSC
and VDS, a small blue light-emitting diode (LED), measuring 2 × 1 ×
1 mm, brightness 100 mcd, was placed on the eyelids just below the
coil. An electronic circuit that permitted adjustment of brightness powered the LED. A commercially available high-speed camera (Point Grey
Research® Inc, model FL3-U3-13S2C-CS) was aligned with the small
LED in the subject’s primary position of gaze. Coupled to a laptop computer the camera was used to register the upper eyelid motion on both
eyes using red, green, and blue (RGB) color image, 800 × 350 pixels,
150 dpi resolution, at 120 frames/s. (Fig. 1)The method was developed
by 2 of the authors (D.M.G. and A.M.) (see Appendix).
Eyelid Kinematics Analysis. Initially, eyelid motion during SB registered with the 2 methods was compared graphically. Linear regression
was then used to fit the relationship between amplitude and maximum
Ophthal Plast Reconstr Surg, Vol. 30, No. 2, 2014
67
Video-analysis of Upper Eyelid Spontaneous Blink
FIG. 1. Small blue light-emitting diode (LED) fixed on the central part of the pretarsal portion of both upper eyelids. Spatial coordinates measured by the software during a spontaneous blink. The y coordinate indicates the amount of the vertical descent of the eyelid. The x changes are due to the horizontal movement of the eyelid during the blink.
velocity measured with both methods. This relationship is usually
named “main sequence” and believed to be an important parameter of
any eyelid movement.2 After converting blinking amplitude measured
in degrees with MSC to millimeters, Bland-Altman plots6 were used
to compare the agreement between methods. All calculations were performed with the JMP software version 10.0 (SAS Institute Inc., Cary,
NC, U.S.A.).
RESULTS
The mean blink rate of the subjects was 19.1 blinks/minute. The
traces of the eyelid motion registered with both methods were virtually
identical (Fig. 2).
Taking into consideration all blinks measured (n = 1976), the
amplitudes recorded with the 2 methods had similar distributions.
As shown in Fig. 3, the distributions were symmetrical with most
movements reaching the pupil center. Only few movements (<15° or
3.5 mm) did not reach the pupil or completely occluded the fissure
(>45° or 9.0 mm). The relationship between amplitude and maximum
velocity (main sequence) was extremely well fitted by linear regression with the data obtained by the 2 methods (Fig. 4). Table 1 lists the
mean values of the blink kinematic parameters (amplitude, maximum
velocity, and the main sequence slope) obtained for each subject with
both methods.
Figure 5 shows, for the whole sample, the Bland-Altman plots
for amplitude, maximum velocity, and main sequence determined with
VDS and MSC. To plot the graphs, amplitude and maximum velocity
data obtained with MSC were converted from degrees to millimeters.
This conversion was possible based on the formula: amplitude (mm) =
13 sin (angle [degrees]), assuming an eyeball with 11.5 mm of radius
and an eyelid thickness of 1.5 mm.
The mean differences of the values measured by the 2 methods were not significant: amplitude = 0.06 ± 0.17 mm, p = 0.724, and
maximum velocity = 5.0 ± 3.39 mm/s, p = 0.1595. The mean difference
between the main sequence values (0.11 ± 0.39·s−1) was not significant
either ((p =0.782).
68
S. P. F. Wambier et al.
diagonal fashion. In the up phase, the eyelid margin returns to its original position with a curvilinear motion (Fig. 6).
The medial translation of the eyelid margin is linearly correlated
to the magnitude of the amplitude the blink (the r values range from
0.70 to 0.96 with a mean = 0.86 ± 0.07 SD) (Fig. 7). The mean slope of
the relationship between vertical (x) and horizontal displacement (y)
was 0.39 ± 0.11 SD indicating that the horizontal movement is approximately 40% of the vertical component of the blink amplitude.
DISCUSSION
FIG. 2. Traces of eyelid motion during spontaneous blinks
from 1 subject. Movements registered with a magnetic search
coil (top) and with a video (bottom).
The horizontal component in the medial direction of the eyelid during SB was easily observed during VDS analysis. As the eyelid
closes down, the eyelid margin is displaced in the medial direction in a
FIG. 3.
The lack of clinical data on the effect of a variety eyelid
conditions on eyelid movement’s kinematics is definitely due to
a methodological problem. Although different techniques such
as electrooculography7–9 and electromyography10,11 have been
used to record blinks, MSC is considered to be the gold standard
method for studying eyelid movements.
The MSC technique was originally developed by
Robinson to measure rotational fast movements such as eye saccades5 because it allows a high spatial resolution (up to 0.1°
or 0.02 mm). As the upper eyelid displacements are rotational
movements, the technique was also used to record blinks and
eyelid saccades.12 Although extremely sensitive and precise, the
use of MSC presents some difficulties. The apparatus necessary
to generate the magnetic field is bulky and expensive. The technique cannot detect lower eyelid displacements and coil fixation
on the pretarsal area of the upper eyelid that may be difficult or
even impossible in oriental eyelids with faint or absent eyelid
creases. This technique is not applicable to daily clinical use.
The use of a VDS as an option to the MSC is not new.
Previously, classic data on eyelid physiology have been obtained
with high-speed cameras.13 However, in the precomputer era,
the amount of work necessary to process several hundred
images of the upper eyelid was a serious limitation.14 In addition, high-speed cameras were expensive and not practical for
clinical use. Some authors tried to overcome the drawbacks of
video analysis processing using a line image camera15 or using
softwares that detect specific marks on the eyelid.16 A variant
of this last method is the videonystagmography, which is basically a test that records eye movements by tracking the pupil
center. In a recent article, the authors drew a black spot 10 mm
in diameter on a piece of paper and attached this surrogate pupil
to an aluminum mask (20 × 20 mm) that was then fixed to the
free edge of the eyelid margin.17 However, the distance between
Amplitude distribution of all blinks registered with both methods. Left: magnetic search coil, right: video.
69
FIG. 4.
Relationship between amplitude and maximum velocity (main sequence) in 1 subject. Left: magnetic search coil, right: video.
the aluminum mask and the skin artificially increases the radius
of eyelid rotation, and the recorded movements are thus much
larger than the real eyelid motion, which poses a limitation of
the previous study.
Another interesting solution with the use of VDS is represented by the methods that compute differences in brightness
on the palpebral fissure images during the opening and closing phase of blinks.18 With this technique, the eye needs to be
illuminated with infrared light, and another device is required
to detect the light reflected back from the eye. Both the light
source and its detector are mounted on an eyeglass trial frame.
Eyelid kinematics is thus measured in an indirect fashion by
computing differences of the palpebral fissure area.
The authors believe that the method they have designed is
the simplest solution for measuring eyelid movements in clinical settings. Small LEDs are inexpensive, and their output can
be controlled by a customized power supply. They are smaller
than the coils, can be positioned close to the eyelid margin, and
do not induce any positional artifact. No specific apparatus is
necessary, and high-speed cameras with 120 Hz of temporal
resolution allowing a precision of 0.15 mm are inexpensive. To
quantify a large number of blinks, it is necessary to use a customized software to automatically identify the blinks and measure the amplitude and maximum velocity of each movement.
They do not have any commercial interest in the software, which
is available on request.
These results indicate that the eyelid motion recorded
with VDS is qualitatively identical to the traces obtained with
MSC. In addition, there is a high agreement between measurements obtained with the 2 methods.
An important characteristic of the VDS is that the horizontal and vertical components of the spontaneous blinks are
recorded separately. Although horizontal shifts of the eyelids
can, theoretically, be quantified with MSC, this type of measurement is not usually performed with coils. The medial shift
of the upper eyelid margin on eyelid closure19 and spontaneous blinks20 has been previously noticed. However, they are not
aware of any quantitative examination of the medial translation
of the upper eyelid margin during blinking. These results clearly
showed that the down phase of the blinks is not a pure vertical movement. As the eyelid closes, there is a horizontal shift
of the upper eyelid margin in the medial direction. This medial
shift has been documented many times for the lower eyelid. In
fact, Doane13 in his classic article showed that during the down
phase of blinks, the upper and lower puncta are compressed
and displaced medially. He measured the lower eyelid translation but did not quantify any upper eyelid horizontal movement
and found that only when there is a complete eyelid closure the
lower eyelid carries the upper eyelid along with it. These results
indicate that a horizontal upper eyelid movement occurs for
any magnitude of blink. This medial shift of the upper eyelid
margin is very similar to the eye motion in the nasal direction
FIG. 5. Agreement between MSC and video expressed by Bland-Altman plots for mean values of all subjects. In all plots, the difference on the y axes are MSC minus video. The dashed liness indicate 2 SD of the differences. MSC values of amplitude (left) and maximum velocity (middle) were converted from degrees to millimeters. Right, main sequence.
70
S. P. F. Wambier et al.
FIG. 6. Two-dimensional upper eyelid motion during 9 spontaneous blinks.
that occurs during blinks.21,22 The horizontal eyelid movement
appears to be dependent on the intensity of the orbicularis contraction and thus is not a passive translation provoked by the
contact between the upper and lower eyelids.
The quantification of eyelid kinematics may help clinicians evaluate important surgical treatments widely performed
in ophthalmology. For instance, in congenital ptosis, levator
palpebral superioris muscle is advanced or partially resected.
Some authors recommend large amounts of muscle resection
beyond Whitnall’s ligament as an option for frontalis suspension
in cases of poor Levator action.23–25 The effect of this type of
surgery on eyelid kinematics remains unknown.
The management of irreversible Bell’s palsy is another
topic that deserves to be quantitatively studied. Reanimation of
paralyzed upper eyelids with gold weight insertion is a popular
surgery, but they are aware of just 1 investigation of the benefits of this procedure on spontaneous blinks of 5 patients.26 The
results indicated a modest increase in blink amplitude (14%)
and no effect on the maximum velocity of the blinks. Palpebral
springs have been advocated as a better operation for the restoration of eyelid kinematics27–29 but, as far as they know, the effects
of this surgery on spontaneous blinks have never been quantified.
Eyelid kinematics deserves also to be quantified in
Graves upper eyelid retraction. There is a plethora of surgical techniques described to correct the eyelid margin position
of patients with Graves’ orbitopathy.30 Nevertheless, it is not
known if the alleviation of retraction is accompanied by a signiff
icant change in the amplitude or velocity of spontaneous blinks.
In conclusion, they believe that there is a need for objective characterization of eyelid kinematics in ophthalmology. A
simple video system is sufficient to fulfill this task.
FIG. 7. Relationship between vertical amplitude of spontaneous blinks and horizontal displacement of the eyelid margin on 4 subjects.
71
REFERENCES
1. Cruz AA, Garcia DM, Pinto CT, et al. Spontaneous eyeblink activity. Ocul Surff 2011;9:29–41.
2. Evinger C, Manning KA, Sibony PA. Eyelid movements.
Mechanisms and normal data. Invest Ophthalmol Vis Sci
1991;32:387–400.
3. Sibony PA, Evinger C, Manning KA. Eyelid movements in facial
paralysis. Arch Ophthalmoll 1991;109:1555–61.
4. Evinger C, Bao JB, Powers AS, et al. Dry eye, blinking, and blepharospasm. Mov Disordd 2002;17 Suppl 2:S75–8.
5. Robinson DA. A method of measuring eye movement using a
scleral search coil in a magnetic field. IEEE Trans Biomed Eng
1963;10:137–45.
6. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet
1986;1:307–10.
7. Mackert A, Woyth C, Flechtner KM, et al. Increased blink rate
in drug-naive acute schizophrenic patients. Biol Psychiatry
1990;27:1197–202.
8. Barbato G, De Padova V, Paolillo AR, et al. Increased spontaneous eye blink rate following prolonged wakefulness. Physiol Behav
2007;90:151–4.
9. Colzato LS, Slagter HA, Spapé MM, et al. Blinks of the eye predict
blinks of the mind. Neuropsychologia 2008;46:3179–83.
10. Holder DS, Scott A, Hannaford B, et al. High resolution electromyogram of the human eyeblink. Electromyogr Clin Neurophysiol
1987;27:481–8.
11. Van allen MW, Blodi FC. Electromyographic study of reciprocal
innervation in blinking. Neurology 1962;12:371–7.
12. Guitton D, Simard R, Codère F. Upper eyelid movements measured with a search coil during blinks and vertical saccades. Invest
Ophthalmol Vis Sci 1991;32:3298–305.
13. Doane MG. Interactions of eyelids and tears in corneal wetting and
the dynamics of the normal human eyeblink. Am J Ophthalmol
1980;89:507–16.
14. Hung G, Hsu F, Stark L. Dynamics of the human eyeblink. Am J
Optom Physiol Optt 1977;54:678–90.
15. Gittins J, Martin K, Sheldrick JH. A line imaging system for
measurement of eyelid movements. Physiol Meas 1995;16:
303–11.
APPENDIX
Using Matlab Image Processing Toolbox (MathWorks,
Natick, MA, U.S.A.), each frame of the tape was analyzed as
a separate image to track the blue LED displacement during
eyelids movement. The RGB color image is a 3 array color
pixel, where each color pixel is a triplet corresponding to red,
green, and blue components.The blue array of the image was
subtracted from its own gray component, highlighting the blue
elements. The blue light emitted by the LED was then isolated
16. Sforza C, Rango M, Galante D, et al. Spontaneous blinking
in healthy persons: an optoelectronic study of eyelid motion.
Ophthalmic Physiol Optt 2008;28:345–53.
17. Casse G, Sauvage JP, Adenis JP, et al. Videonystagmography to assess
blinking. Graefes Arch Clin Exp Ophthalmoll 2007;245:1789–96.
18. Caffier PP, Erdmann U, Ullsperger P. Experimental evaluation of
eye-blink parameters as a drowsiness measure. Eur J Appl Physiol
2003;89:319–25.
19. Frueh BR, Hassan AS, Musch DC. Horizontal eyelid movement on
eyelid closure. Ophthal Plast Reconstr Surg
g 2005;21:109–11.
20. Kennard DW, Glaser GH. An analysis of eyelid movements. J Nerv
Ment Dis 1964;139:31–48.
21. Bour LJ, Aramideh M, de Visser BW. Neurophysiological aspects of eye and eyelid movements during blinking in humans.
J Neurophysioll 2000;83:166–76.
22. VanderWerf F, Brassinga P, Reits D, et al. Eyelid movements: behavioral studies of blinking in humans under different stimulus conditions. J Neurophysioll 2003;89:2784–96.
23. Decock CE, Shah AD, Delaey C, et al. Increased levator
muscle function by supramaximal resection in patients with
blepharophimosis-ptosis-epicanthus inversus syndrome. Arch
Ophthalmoll 2011;129:1018–22.
24. Epstein GA, Putterman AM. Super-maximum levator resection
for severe unilateral congenital blepharoptosis. Ophthalmic Surg
1984;15:971–9.
25. Johnson CC. “Super-maximum levator resection for severe unilateral congenital blepharoptosis”. Ophthalmic Surg
g 1985;16:512–3.
26. Abell KM, Baker RS, Cowen DE, et al. Efficacy of gold weight
implants in facial nerve palsy: quantitative alterations in blinking.
Vision Res 1998;38:3019–23.
27. Levine RE, House WF, Hitselberger WE. Ocular complications of
seventh nerve paralysis and management with the palpebral spring.
Am J Ophthalmoll 1972;73:219–28.
28. Levine RE, Pulec JL. Eyelid reanimation with the palpebral spring
after facial nerve graft surgery: an interdisciplinary approach.
Ear Nose Throat J 1993;72:686–91.
29. Levine RE, Shapiro JP. Reanimation of the paralyzed eyelid with
the enhanced palpebral spring or the gold weight: modern replacements for tarsorrhaphy. Facial Plast Surgg 2000;16:325–36.
30. Cruz AA, Ribeiro SF, Garcia DM, et al. Graves upper eyelid retraction. Surv Ophthalmoll 2013;58:63–76.
by a threshold parameter allowing the LEDs to be detected and
spatially recorded (Fig. 1).
All coordinates in pixels were stored and converted to
millimeters using a reference mark placed in the image. A custom software based on the blink signal’s first derivative was
used to detect the blinks automatically and to determine the
beginning and end of a blink. In addition, the data retrieved
were checked manually to avoid mistakes. The software automatically calculated the variables amplitude and the maximum
velocity.
72
Capítulo IV
- Efeito da correção cirúrgica da retração palpebral superior no contorno palpebral
______________________________________________________________
Efeito da correção cirúrgica da retração palpebral superior no contorno
palpebral
Capítulo IV
- Efeito da correção cirúrgica da retração palpebral superior no contorno palpebral
Efeito da correção cirúrgica da retração palpebral superior no contorno palpebral
Pre- and Postoperative Quantitative Analysis of Contour
Abnormalities in Graves Upper Eyelid Retraction
Sara F. T. Ribeiro, M.D.*, Gherusa H. Milbratz, M.D.†, Denny M. Garcia, B.Cs.†, Martin Devoto, M.D.‡,
‡
Guilherme H. Neto, M.D.§, Ricardo Mörschbächer, M.D.‖,
‖ Filipe J. Pereira, M.D.¶,
and Antonio A. V. Cruz, M.D., Ph.D.†
*Hospital de São João, School of Medicine, University of Oporto, Oporto, Portugal; †School of Medicine of Ribeirão
Preto, Department of Ophthalmology, Otorhinolaryngology and Head and Neck Surgery, University of São Paulo, São
Paulo, Brazil; ‡Consultores Oftalmologicos, Buenos Aires, Argentina; §Department of Ophthalmology, Fluminense
School of Medicine, Fluminense Federal University, Niterói, Rio de Janeiro; ‖‖Health Sciences Federal University of
Porto Alegre, Porto Alegre; and ¶Clínica Catarinense de Pálpebras e Olhos, Florianópolis, Santa Catarina, Brazil
Purpose:: One of the most common problems of the surgical
management of Graves upper eyelid retraction is the occurrence
of eyelid contour abnormalities. In the present study, the
postoperative contour of a large sample of eyelids of patients
with Graves orbitopathy was measured.
Methods:: The postoperative upper eyelid contour of 62 eyes
of 43 patients with Graves orbitopathy was subjectively classified
by 3 experienced surgeons in 3 categories: poor, fair, and good.
The shape of the eyelid contours in each category was then
measured with a recently developed custom-made software by
measuring multiple midpupil eyelid distances each 15° along the
palpebral fissure. The upper eyelid contour of 60 normal subjects
was also quantified as a control group.
Results:: The mean ratio between the sum of the lateral and
medial midpupil eyelid distances (lateral/medial ratio) was 1.10 ±
0.11 standard deviation in controls and 1.15 ± 0.13 standard
deviation in patients. Postoperatively, the mean midpupil eyelid
distance at 90° was 4.16 ± 1.13 mm standard deviation . The
distribution lateral/medial ratios of the eyelids judged as having
good contours was similar to the distribution of the controls with
a modal value centered on the interval between 1.0 and 1.10. The
distribution of lateral/medial ratios of the eyelids judged as having
poor contour was bimodal, with eyelids with low and high lateral/
medial ratios. Low lateral/medial ratios occurred when there was
a lateral overcorrection, giving the eyelid a flat or a medial ptosis
appearance. High lateral/medial ratios were due to a central or
medial overcorrection or a lateral peak maintenance.
Conclusions:: Postoperative upper eyelid contour abnormalities
can be quantified by comparing the sum of multiple midpupil
eyelid distances of the lateral and medial sectors of the eyelid.
Low and high lateral/medial ratios are anomalous and judged as
unpleasant.
T
he most common and characteristic sign of Graves orbitopathy is upper eyelid retraction.1 Most of the affected patients
are women who usually have serious concerns about their
appearance and in severe cases suffer from dry eye and keratitis.2 Although the retracted upper eyelid can be temporarily
lowered with medical treatment such as guanethidine eyedrops3
and botulinum toxin type A injection,4 a permanent correction is
obtained only with surgery. All techniques published to correct
upper eyelid retraction are minor variations of weakening of the
levator palpebrae superioris (LPS) and Müller’s muscle.5–10
One of the most important problems of any procedure
aimed to correct upper eyelid retraction is how to avoid postoperative contour abnormalities. Although well-known in the oculoplastic literature,5,11 these contour abnormalities have never been
analyzed in a quantitative manner. In the present study, a new
method was used to measure eyelid contour12 to analyze the shape
of the upper eyelid in a series of patients with Graves orbitopathy
who had undergone surgery for eyelid retraction correction.
METHODS
Subjects. The control group comprises images of the OD or OS of 60 norr
mal subjects (41 women and 19 men) ranging in age from 17 to 66 years,
with no pathology or surgery that could affect eyelid shape or function. The
Graves group consisted of 62 palpebral fissure images of 43 patients with
Graves orbitopathy derived from the private practice of 4 different surgeons
in Brazil and 1 in Argentina. The Table lists the sample demographics and
the number of eyelids that were operated by anterior or posterior approach.
Surgery by anterior approach was performed in 90% of the eyelids as described by Harvey and Anderson.5 Briefly, using an eyelid crease incision,
the orbital septum was identified and incised exposing the preaponeurotic
fat and the underlying LPS aponeurosis. Then, LPS aponeurosis was care-
g 2012;28:429–433)
Sex, age, number of eyelids, and surgical approach
used in the patients
Accepted for publication July 3, 2012.
The authors have no financial or conflict of interest to disclose.
Address correspondence and reprint requests to Antonio A. V. Cruz, M.D.,
Ph.D., Department of Ophthalmology, Otorhinolaryngology and Head and
Neck Surgery of the School of Medicine of Ribeirão Preto, University of
São Paulo, São Paulo, Brazil. Av. Bandeirantes, 3900, 14049–900 – Ribeirão
Preto, São Paulo, Brazil. E-mail: [email protected]
DOI: 10.1097/IOP.0b013e3182696532
No. subjects
Age range (years)
Orbital decompression
No. eyelids
Surgical approach
Anterior
Posterior
Patients
Controls
43 (33 F/10 M)
24–55
24
62
60 (41 F/19 M)
17–66
—
60
56
6
—
—
75
S. F. T. Ribeiro et al.
FIG. 1. Method for quantification of the upper eyelid contour. Left, Radial drawn by the software from the pupil center. Right,
Graphic representation of the eyelid contour. The line that represents the contour is obtained when the observer marks the intersections between the radial lines and the eyelid margin.
fully dissected from the lateral to the medial aspect of the eyelid. The lateral
horn of the LPS was cut or not depending on the amount of lateral preoperative retraction. Finally, the exposed Müller’s muscle was undermined and
excised. In all patients, the LPS recession and Müller’s muscle extirpation
were gradually reduced as the surgery progressed toward the medial portion
of the eyelid. In the remaining 10% of surgeries, the posterior approach was
used.13 In this case, the eyelid was everted over a Desmarres retractor exposing the palpebral conjunctiva. The conjunctiva was ballooned with a local
FIG. 2. Distribution of the lateral/medial (LM) ratio in the controls and patients with Graves orbitopathy.
anesthetic, incised at the level of the superior tarsal border, and dissected
from the underlying Müller’s muscle with Westcott scissors. This muscle
was next extirpated from the lateral to the medial direction. If necessary, the
lateral horn of the LPS was cut and recessed.
Eyelid Contour Analysis. First, 3 physicians (a general plastic surgeon,
an oculoplastic specialist, and an ophthalmologist) who were not aware
of the preoperative appearance of the palpebral fissure of the patients
FIG. 3. Distribution of the quantitative contour analysis with
good (upper), fair (middle) and poor (bottom) postoperative
results. LM, lateral/medial.
76
Contour Abnormalities in Graves Upper Eyelid Retraction
FIG. 4. Contour abnormalities in the poor category. Left, Preoperative retraction. Right, Postoperative appearance. From above, Flat
shape, lateral ptosis, lateral peak, and medial ptosis.
subjectively graded the postoperative upper eyelid contour in 3 categories: poor, fair, and good. All patients had at least more than 6 months
of follow up after surgery. A contour was classified only when 2 of the
judges agreed on their judgment
Following the subjective classification, the pre- and postoperative contours of all eyelids were measured with the assistance of a
custom-made software recently developed in the Matlab MathWorks.12
First, the user arbitrarily defines the pupil center, then the software
draws a vertical line at the noon position (90°) and 6 radial lines 15°
apart from the midline in the temporal (105°, 120°, 135°,150°, 165°,
and 180°) and nasal (75°, 60°, 45°, 30°, 15°, and 0°) sectors of the eyelid
fissure. The only task of the user is to mark the intersections of the radial
lines on the eyelid margin edge. The length of the line which intersected
the eyelid margin at the noon position (90°) is the conventional midpupil
lid distance (MPLD) commonly used to record the height of the upper
eyelid with a millimeter ruler in clinical settings.14,15 The other lines can
be seen as radial MPLDs. The lengths of all lines are automatically calculated by the software and displayed on a polar plot, which represented
the quantification of the whole eyelid contour (Fig. 1).
Eyelid contour was expressed as the ratio between the sum of the
lateral (165°, 150°, 135°, 120°, and 105°) and medial (15°, 30°, 45°, 60°,
and 75°) MPLDs (lateral/medial ratio). Contour asymmetry was defined
by any lateral/medial ratio different from 1.0.
Statistical Analysis. All statistical analyses were performed using the
SAS system. Data are reported as means ± standard deviation. Compari-
sons regarding the parameters of the MPLDs at 90° between groups and
judgments were performed by 1-way analysis of variance and the t test.
RESULTS
The mean and standard deviation of MPLD at 90° was 4.07 ±
0.73 mm for the control group. These figures concur well with previous studies that define upper eyelid retraction as any eyelid that is 5.5
mm or more above the pupil center.16,17 Preoperatively, all eyelids of
the patients were outside the normal range. The mean midpupil eyelid
distance at 90° was 7.65 ± 1.20 mm. Figure 2 displays the distribution
of lateral/medial ratios for the controls and patients with Graves orbitopathy. The mean lateral/medial ratio of the control group was 1.10 ±
0.11. Among the patients with Graves orbitopathy, this lateral asymmetry increased significantly (mean lateral/medial ratio = 1.15 ± 013;
t = 2.38; p = 0.02).
Postoperatively, the mean midpupil eyelid distance at 90° was
4.16 ± 1.13 mm. The surgeons agreed on the classification of 54 of the
62 eyelids evaluated. A total of 23 contours were classified as good, 16
as fair, and 15 as poor. The mean MPLD at 90° of the contours judged
as poor (3.51 ± 1.34 mm) was significantly lower than that of the eyelids
with good (4.45 ± 0.85 mm) and fair (4.49 ± 1.22 mm) contours (F =
4.01; p = 0.024). The mean lateral/medial ratio of the 3 subjective categories was similar (good: 1.10 ± 0.10; fair: 1.09 ± 0.16; poor: 1.20 ±
0.24; F = 2.05; p = 0.139). However, as shown in Figure 3, the shapes
of the distributions differed between categories. The distribution of the
eyelids judged as having good contours was similar to the distribution
of the controls with a modal value centered on the interval between 1.0
and 1.10. The distribution of the eyelids judged as having poor contour
77
S. F. T. Ribeiro et al.
was bimodal with eyelids with low and high lateral/medial ratios. The
graphic analysis of these eyelids revealed that low lateral/medial ratios
had a lateral or central overcorrection, giving the eyelid a flat or a lateral
ptosis appearance. Eyelids with high lateral/medial ratios showed either
a lateral undercorrection or a medial overcorrection (Fig. 4).
decision on the extent of lateral dissection. The results suggest
that aggressive lateral debilitations carry the risk of central and
medial overcorrection with unfavorable results. They also show
that a small lateral asymmetry is a normal finding, and the optimal goal is to be achieved by many patients.
DISCUSSION
REFERENCES
There is a large body of technical variations published
for the surgical correction of eyelid retraction in Graves orbitopathy. The LPS and Müller’s muscle can be weakened in combination or separately by anterior5 or posterior13 approach. The
process of muscle debilitation also varies. Both muscles can be
lengthened,18 resected, or recessed with19,20 or without spacers.5
Whatever the technique used, there is general agreement that
the effect of the procedures is variable, and most authors try
to perform the surgery under local anesthesia in a graded and
controlled fashion.
Although several authors have reported their results in
terms of symmetry of eyelid height21,22 or reduction of retraction
at the central portion of the eyelid,7,23,24 postoperative contour
anomalies are well-known and cited in many articles as a possible
complication of any surgery for eyelid retraction correction.11,25
This point was specifically addressed by Shore26 who criticized the
strict adherence to the symmetry or position of the central portion
of the upper eyelid as a gold standard by which postoperative
results are evaluated.
Eyelid contour has always been analyzed subjectively
because until recently there was no way to quantify any type of
upper eyelid deformation in a simple manner. The method used
is an extension of the time-honored measurement of the eyelid
margin height at the noon position. Instead of just using 1 linear
determination, it is easy to establish the position of the upper
eyelid margin in multiple angles with a special software.12
It is agreed that some patients sought treatment for
preoperative contour anomalies. The most cited anomaly is
the so-called lateral eyelid flare sign,27 a term used to name
an enhanced lateral retraction. This type of retraction may be
caused by a state of LPS overcontraction, because voluntary
eyelid retraction in normal subjects induces a typical lateral
contour deformation.27 Another explanation for the lateral flare
is the involvement of Müller’s muscle, which has an important
lateral extension.28,29
The normal upper eyelid contour is smooth and follows
a second-degree function (parabola).30 Mathematically, this
shape can be explained by the fact that the eyelid rests on the
anterior portion of a spherical boy, the eyeball.31 Contour deformities, on the contrary, do not follow any geometric pattern.
The results confirm earlier subjective assessments showing that
the retracted eyelids of patients with Graves orbitopathy often
have a lateral deformation. This lateral contour asymmetry was
detected in a large number of the patients operated on. It is thus
clear that for a large number of patients, the surgeon’s task when
operating an eyelid with retraction is not just a matter of lowering the eyelid margin. Besides correcting the eyelid height,
the surgeon should achieve a lateral/medial contour balance.
To address the enhanced lateral retraction, it is recommended
a more aggressive muscle debilitation on the lateral aspect of
the eyelid.5,6 However, in doing so, there is a risk to overcorrect the lateral or central portions of the eyelid. The quantitative
analysis of the eyelids subjectively judged with unsatisfactory
results indicated that most had a central and medial overcorrection. These eyelids have an unpleasant appearance because
the preoperative lateral slant was transformed to a contour that
was flat or with medial ptosis. It is clear that during the process
of weakening the eyelid retractors, the surgeon faces a critical
1. Lebensohn JE. The eye signs of Graves’ disease. Am J Ophthalmol
1964;57:680–1.
2. Sokol JA, Foulks GN, Haider A, et al. Ocular surface effects of
thyroid disease. Ocul Surff 2010;8:29–39.
3. Gay AJ, Wolkstein MA. Topical guanethidine therapy for endocrine
lid retraction. Arch Ophthalmoll 1966;76:364–7.
4. Costa PG, Saraiva FP, Pereira IC, et al. Comparative study of Botox
injection treatment for upper eyelid retraction with 6-month followup in patients with thyroid eye disease in the congestive or fibrotic
stage. Eye (Lond) 2009;23:767–73.
5. Harvey JT, Anderson RL. The aponeurotic approach to eyelid retraction. Ophthalmology 1981;88:513–24.
6. Putterman AM, Fett DR. Müller’s muscle in the treatment of upper
eyelid retraction: a 12-year study. Ophthalmic Surg
g 1986;17:361–7.
7. Dixon R. The surgical management of thyroid-related upper eyelid
retraction. Ophthalmology 1982;89:52–7.
8. Thaller VT, Kaden K, Lane CM, et al. Thyroid lid surgery. Eye
(Lond) 1987;1 (Pt 5):609–14.
9. Older JJ. Surgical treatment of eyelid retraction associated with
thyroid eye disease. Ophthalmic Surg
g 1991;22:318–22; discussion
322–3.
10. Hurwitz JJ, Rodgers KJ. Prevention and management of postoperative lateral upper-lid retraction in Graves’ disease. Can J Ophthalmol
1983;18:329–32.
11. Ceisler EJ, Bilyk JR, Rubin PA, et al. Results of Müllerotomy and
levator aponeurosis transposition for the correction of upper eyelid
retraction in Graves disease. Ophthalmology 1995;102:483–92.
12. Milbratz GH, Garcia DM, Guimarães FC, et al. Multiple radial
midpupil lid distances: a simple method for lid contour analysis.
13. Putterman AM. Surgical treatment of thyroid-related upper eyelid
retraction. Graded Müller’s muscle excision and levator recession.
14. Frueh BR. Graves’ eye disease: orbital compliance and other physical measurements. Trans Am Ophthalmol Soc 1984;82:492–598.
15. Edwards DT, Bartley GB, Hodge DO, et al. Eyelid position measurement in Graves’ ophthalmopathy: reliability of a photographic
technique and comparison with a clinical technique. Ophthalmology
2004;111:1029–34.
16. Bartley GB, Fatourechi V, Kadrmas EF, et al. Chronology of
Graves’ ophthalmopathy in an incidence cohort. Am J Ophthalmol
1996;121:426–34.
17. Bartley GB, Gorman CA. Diagnostic criteria for Graves’
ophthalmopathy. Am J Ophthalmoll 1995;119:792–5.
18. Grove AS Jr. Levator lengthening by marginal myotomy. Arch
Ophthalmoll 1980;98:1433–8.
19. Meltzer MA. Surgery for lid retraction. Ann Ophthalmol
1978;10:102–6.
20. Flanagan JC. Retraction of the eyelids secondary to thyroid ophthalmopathy–its surgical correction with sclera and the fate of the
graft. Trans Am Ophthalmol Soc 1980;78:657–85.
21. Chalfin J, Putterman AM. Müller’s muscle excision and levator recession in retracted upper lid. Treatment of thyroid-related retraction. Arch Ophthalmoll 1979;97:1487–91.
22. Levine MR, Chu A. Surgical treatment of thyroid-related lid retraction: a new variation. Ophthalmic Surg
g 1991;22:90–4.
23. Small RG. Upper eyelid retraction in Graves’ ophthalmopathy: a
new surgical technique and a study of the abnormal levator muscle.
Trans Am Ophthalmol Soc 1988;86:725–93.
24. Khan JA, Garden V, Faghihi M, et al. Surgical method and results
of levator aponeurosis transposition for Graves’ eyelid retraction.
Ophthalmic Surg Lasers 2002;33:79–82.
25. Liu D. Surgical correction of upper eyelid retraction. Ophthalmic
Surgg 1993;24:323–7.
78
26. Shore JW. Graves disease: correcting upper eyelid retraction [letter]. Ophthalmology 1996;103:1713–4.
27. Cruz AA, Akaishi PM, Coelho RP. Quantitative comparison between upper eyelid retraction induced voluntarily and
by Graves orbitopathy. Ophthal Plast Reconstr Surg
g 2003;19:
212–5.
28. Morton AD, Elner VM, Lemke BN, et al. Lateral extensions of the
Müller muscle. Arch Ophthalmoll 1996;114:1486–8.
Contour Abnormalities in Graves Upper Eyelid Retraction
29. Kakizaki H, Takahashi Y, Nakano T, et al. Müller’s muscle: a component of the peribulbar smooth muscle network. Ophthalmology
2010;117:2229–32.
30. Cruz AA, Coelho RP, Baccega A, et al. Digital image processing
measurement of the upper eyelid contour in Graves disease and
congenital blepharoptosis. Ophthalmology 1998;105:913–8.
31. Malbouisson JM, Baccega A, Cruz AA. The geometrical basis of
the eyelid contour. Ophthal Plast Reconstr Surg
g 2000;16:427–31.
79
Capítulo V
______________________________________________________________
Efeito da correção cirúrgica da retração palpebral superior (por müllerectomia
via posterior) na cinética palpebral
Capítulo V - Efeito da correção cirúrgica da retração palpebral superior (por mullerectomia via posterior) na cinética palpebral
Efeito da correção cirúrgica da retração palpebral superior (por müllerectomia via posterior) na cinética palpebral
"Graded Müllerectomy for Correction of Graves Upper Eyelid Retraction:
Effect onEyelid Movements."
Sara Ribeiro MD; Denny Garcia BSc; Vítor Leal MD; Faria-Correia MD; Amândio Rocha-Sousa
MD, PhD; Fernando Falcão-Reis MD, PhD; Antonio Augusto Velasco e Cruz MD, PhD.
Ophthal Plast Reconstr Surg 2014; Apr 25 [Epub ahead of print].
83
Graded Müllerectomy for Correction of Graves Upper
Eyelid Retraction: Effect on Eyelid Movements
Sara Filipa Teixeira Ribeiro, M.D.*, Denny M. Garcia, B.Sc.†, Vítor Leal, M.D.*,
Fernando Faria-Correia, M.D.*, Amândio Rocha-Sousa, M.D., Ph.D.*,
Fernando Falcão-Reis, M.D., Ph.D.*, and Antonio Augusto Velasco e Cruz, M.D., Ph.D.†
*Ophthalmology Unit, Department of Senses Organs, Faculty of Medicine, University of Porto, Porto, Portugal;
†Department of Ophthalmology, Otorhinolaryngology, and Head and Neck Surgery, School of Medicine of
Ribeirão Preto; ‡School of Medicine of Ribeirão Preto and Craniofacial Research Support Center, University of
São Paulo, São Paulo, Brazil; §King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia;
and ║Johns Hopkins University, Baltimore, Maryland, U.S.A.
Purpose:: To measure the effect of müllerectomy from
posterior approach on the amplitudes of spontaneous blinking
and downward eyelid saccades.
Methods:: Spontaneous blinks and downward upper eyelid
saccadic movements of 16 patients (23 eyelids) with Graves
orbitopathy were measured before and after müllerectomy
from posterior approach. A new video system was used to
continuously register the blinking activity while subjects viewed
a commercial movie for 5 minutes. Downward eyelid saccades
(30° of downgaze) were also measured with the video system.
Results:: Müllerectomy had no effect on the amplitude of
the blink. However, as the eyelid margins were significantly
lowered by the surgery, the amplitude of the blink movements
relative to the pupil center increased substantially. The number
of movements occluding the pupil center increased from 0%
to 13%. Due to the increased efficiency of blinking, the blink
rate decreased. Surgery induced a mean increase of 1.1 mm of
downward saccades.
Conclusions:: The effects of müllerectomy on the blinks are
indirect and related to correction of eyelid retraction. The relative
amplitude of blink movements increases and blink rate decreases.
Müllerectomy does affect the downward eyelid saccades
increasing the ability of the upper eyelid to relax on downgaze.
g 2014;XX:00–00)
U
pper eyelid retraction (UER) is the most common manifestation of Graves orbitopathy (GO), and since the nineteenth century, a vast amount of literature has been published
on this topic.1 The observation that movements of the retracted
eyelids seem to be abnormal in some GO patients has been well
documented. A typical example is the eyelid lag of the upper
Accepted for publication December 25, 2013.
Supported by grants from the Sociedade Portuguesa de Oftalmologia and
from the Craniofacial Research Support Center of the University of São
Paulo.
The authors have no financial or conflicts of interest to disclose.
Address correspondence and reprint requests to Antonio Augusto Velasco
e Cruz, Department of Ophthalmology, Otorhinolaryngology, and Head and
Neck Surgery, School of Medicine of Ribeirão Preto, University of São
Paulo, Av. Bandeirantes, 3900, 14049-900 Ribeirão Preto, São Paulo, Brazil.
E-mail: [email protected]
DOI: 10.1097/IOP.0000000000000116
eyelid on downgaze as described by Von Graeffe in 1864.2
Spontaneous blinks are also believed to be somewhat abnormal
in GO. Reduced blinking amplitude and low blink rate are signs
of GO that have been previously described.3
Although there are numerous surgical techniques for the
correction of Graves UER,1 the authors are not aware of any
study that investigates the effect of different surgical modalities
on eyelid function. In the present study, they used a novel clinical method to record spontaneous blinks and eyelid saccades in
a series of patients who underwent graded müllerectomy.
METHODS
This research adhered to the tenets of the Declaration of Helsinki
and was approved by the Ethics Committee of the Hospital das Clínicas
of the School of Medicine of Ribeirão Preto, University of São Paulo.
Subjects. Twenty-three upper eyelids of 16 patients with GO (12
women; GO group), ranging in age from 19 to 74 years (mean age ±
SD, 48.4 ± 11.9 years), underwent eyelid retraction surgery (7 bilateral
procedures) for cosmetic reasons. At the time of the study, 12 patients
were euthyroid and 4 had hypothyroidism. Nine patients used topical
lubricants regularly, but none had any signs of superficial keratopathy.
Orbital imaging was performed in all patients with CT (n = 20) or MRI
(n = 3). Qualitative analysis of the images indicated that the superior
complex was not significantly enlarged in any patient. The upper margin
reflex distance (MRD1) of the sample ranged from 4.0 to 8.0 mm (mean
± SD, 5.7 ± 1.1 mm). Five eyelids with MRD1 between 4 and 5 mm underwent surgery to correct eyelid height asymmetry mainly due to unilateral eyelid flare.
For comparison, a control group was enrolled, comprising 24
normal subjects (18 women) ranging in age from 24 to 73 years (mean
± SD, 41.4 ± 11.4 years). No subject in the control group had any pathology or surgery that could affect eyelid shape or function. The MRD1
(OD or OS) ranged from 3.0 to 3.5 mm (mean ± SD, 4.0 ± 0.7 mm).
Surgery. All surgeries were performed by a single surgeon (V.L.)
through the posterior approach as described by Putterman and Fett.4
Briefly, the eyelid was everted over a Desmarres retractor exposing
the palpebral conjunctiva. The conjunctiva was ballooned with a local
anesthetic, incised at the level of the superior tarsal border, and dissected from the underlying Müller’s muscle with Westcott scissors. This
muscle was next extirpated in a graded fashion in a lateral-to-medial
direction. If necessary, a limited incision of the lateral horn of the levator palpebral superioris (LPS) was performed to correct any residual
flare (11 eyelids).
Ophthal Plast Reconstr Surg, Vol. XX, No. XX, 2014
85
Eyelid Movements. The amplitude of spontaneous blinks and downward
eyelid saccades were registered with a portable video system.5 To record
the eyelid movements, a small blue light-emitting diode (LED), measuring 2 × 1 × 1 mm, brightness 100 mcd, was placed just above the eyelashes of the eyelid on pretarsal area (Fig. 1). A commercial high-speed
camera was aligned with a small LED in the subject’s primary position
of gaze. Controlled by a laptop computer, the camera registered the upper eyelid motion on OU using RGB color image, 800 × 350 pixels, 150
dpi resolution, at 120 Hz (120 frames/s). The LEDs were detected, and
their coordinates precisely measured with customized software. The
spontaneous blink rate was estimated after 5 minutes of continuous registration, while the subjects watched a commercial movie.
Eyelid saccades were measured when the eye rotated from the
primary position of gaze to 30° downward. The mean of 3 consecutive
movements was taken as the movement value.
All preoperative measurements were performed 2 to 4 weeks preoperatively. Postoperatively, patients were measured after the symptoms and
signs of inflammation had disappeared, typically at 4 weeks after surgery.
Statistical Analysis. Paired t tests were used to compare the movements
of the eyelids before and after surgery. Comparisons of these values
with those of the control group were performed with the independent
t test. A p value less than 0.05 was considered statistically significant.
RESULTS
The mean preoperative MRD1 of the GO group (5.7 mm) was statistically significantly higher than the control group (4.0 mm; p < 0.001).
Postoperatively, the mean MRD1 dropped to 3.7 ± 0.66 mm (standard error
[SE]), which was similar to the control group (p
( = 0.36). Figure 2 shows
typical examples of the effect of the surgery on eyelid position and contour.
FIG. 1. Small blue light-emitting diode fixed on the central part of the pretarsal portion of both upper eyelids. The Y coordinate indicates the amount of the vertical descent of the eyelid. The X changes are due to the horizontal movement of the eyelid during the blink.
FIG. 2. Top, Preoperative Graves upper eyelid retraction. Bottom, Postoperative results. Notice the correction of the eyelid flare sign
on the left and a discrete lowering of the eyelid margin on the right.
86
Effect of Müllerectomy on Eyelid Movements
Values (mean ± standard error) of parameters of upper eyelid movements of the controls and patients before (preop)
V
and after (postop) surgery
Spontaneous blinks
Downward saccades
Subjects Amplitude (mm) Maximum velocity (mm/s) Amplitude/MPLD Rate (blinks/min) Amplitude (mm) Maximum velocity (mm/s)
Patients
Preop
Postop
Controls
7.9 ± 0.47
7.4 ± 0.46
6.7 ± 0.43
160.7 ± 11.21
150.2 ± 12.86
154.11
1.5 ± 0.11
2.0 ± 0.15
1.72 ± 0.12
18 ± 2.2
14 ± 1.8
16 ± 1.9
7.1 ± 0.20
8.2 ± 0.20*
7.1 ± 0.22
112.7 ± 4.24
125.2 ± 5.05**
100.0 ± 4.31
Postop, postoperative; preop, preoperative. *p < 0.001; **p = 0.002.
The Table presents the mean values ± SE of spontaneous blinks
parameters and the saccadic amplitude for the control group and GO
group before and after surgery. There was no statistical difference between groups in the mean preoperative blink parameters (amplitude,
t = 1.92, p = 0.06; rate, t = 0.60, p = 0.55; relative amplitude, t = 1.58,
p = 0.12). The mean preoperative amplitude of the saccadic movements
was not statistically significantly different between groups (t = 0.007;
p = 0.99).
The blink amplitude was not significantly different postoperatively compared with preoperatively (t = 1.60; p = 0.12; Fig. 3). However,
because the eyelid margin was lowered after surgery, the relative amplitude of the blinks relative to the pupil center increased significantly. The
number of blinks not reaching the pupil center (values < 1) decreased
from 17.4% to 4.3%, and the number of movements completely occluding the fissure (values > 3) increased from 0% to 13% (Fig. 4). Because
the efficacy of the blinking activity increased, the mean blink rate decreased statistically significantly (t = 2.1; p = 0.046).
The amplitude of downward saccadic movements increased significantly after müllerectomy (t = 5.61; p < 0.001; Fig. 5). The differences between the preoperative and postoperative measurements ranged
from 0 to 3.2 mm (mean ± SE, 1.1 ± 0.2 mm). No correlation was found
between the degree of eyelid lowering and the increment of saccade
amplitude. However, the increase on the amplitude tended to be related
to the magnitude lowering effect. For instance, the median increment of
the saccadic amplitude was 1.35 mm for the eyelids lowered more than
1.5 mm and only 0.5 mm for those lowered < 1.5 mm. However, due to
small size of each group, this difference failed to be significant.
DISCUSSION
The spontaneous blinking activity is generally considered abnormal in Graves UER; however, there is a relative paucity of studies corroborating this classic concept. The findings
observed on the current study concur well with a previous report
that the amplitude of the blinking movements of patients with
GO were similar to a control group of normal patients.6 The
authors believe that any research on blinking in GO needs to
be put in the context of the clinical characteristics of the samples studied. Specifically, one should consider the magnitude
of retraction and the radiologic evidence of LPS enlargement.
The retraction levels of the present sample were not high, no
patient had any signs of superficial keratopathy, and the LPS
did not seem especially enlarged. In addition, eyelid lag was
not also present, indicating that the elastic components of the
eyelids undergoing surgery were not seriously affected by the
disease. It is possible that the findings would differ in a sample
of patients with a predominance of eyelid lag on downgaze and
clear signs of LPS hypertrophy. Eye surface changes due to dry
FIG. 3. Spontaneous blinks before (top) and after (bottom) eyelid surgery. The mean amplitude of the blinks was not affected by
the surgery.
87
FIG. 5. Example of the effect of müllerectomy on downward
eyelid saccades.
FIG. 4. Distribution of the amplitude of blink movements
related to the pupil center, before (top) and after (bottom)
müllerectomy. V
Values < 1 indicate that the eyelid margin did not
reach the pupil center. V
Values > 3 indicate the fissure was completely occluded.
eye is another factor that may influence the blinking kinematics in GO. As the authors have mentioned, the ocular surface of
their patients were normal.
In this study group (GO group) with normal blinking
movements, müllerectomy did not affect the amplitude of the
blink. This result suggests that Müller’s muscle plays no role
in blink kinetics. However, because the eyelid margins are
lowered by surgery, there was a clear beneficial effect because
the relative amplitude of the blinks increased. After surgery,
a substantial number of movements occluded the fissure, and
only a few blinks did not reach the pupil center. The blink rate
diminished postoperatively, a finding that the authors believe
is associated to the increased efficacy of the blinks protecting
the cornea.
Although müllerectomy had no effect on blinking amplitude, the downward saccade movements increased significantly
after surgery. This is another clear beneficial effect of the surgery because it indicates that after surgery the passive forces of
the upper eyelid are dissipated with more efficiency on downgaze, increasing the ability of the eyelid to relax. From a therapeutic point of view, the increment on the downward saccades
prevent lagophthalmos during sleep.
In summary, müllerectomy from posterior approach acts
on spontaneous blinks primarily by the effect of lowering the
eyelid margin. The surgery does increase downward saccades.
REFERENCES
1. Cruz AA, Ribeiro SF, Garcia DM, et al. Graves upper eyelid retraction. Surv Ophthalmoll 2013;58:63–76.
2. Von Graefe HA. Vortrag Ueber die Basedowsche Krankheit.
Klinische Monatsblatter fur Augenheilkunde. 1864;2:183–5.
3. Lebensohn JE. The eye signs of graves’ disease. Am J Ophthalmol
1964;57:680–1.
4. Putterman AM, Fett DR. Müller’s muscle in the treatment of upper
eyelid retraction: a 12-year study. Ophthalmic Surg
g 1986;17:361–7.
5. Wambier SPF, Ribeiro SF, Garcia DM et al. Two dimensional video
analysis of the upper eyelid motion during spontaneous blinking.
Ophthal Plast Reconstr Surg. 2014 Jan 29 [Epub ahead of print].
6. Garcia DM, Messias A, Costa LO, et al. Spontaneous blinking
in patients with Graves’ upper eyelid retraction. Curr Eye Res
2010;35:459–65.
88
Capítulo VI
- Discussão Global e Conclusões
______________________________
Discussão Global e Conclusões
1. Anomalias de contorno induzidas pela retração palpebral
superior da OG
A retração da pálpebra superior é o sinal mais comum e característico da
OG (Lebensohn 1964). As pálpebras afetadas, além de retraídas, podem
apresentar anomalias de contorno. A deformidade de contorno mais descrita é
a retração mais acentuada da porção lateral da pálpebra, designada lateral
flare sign (Waller 1982).
Apesar das anomalias de contorno da OG serem bem conhecidas (Cruz,
Akaishi and Coelho 2003; Cruz, Coelho, Baccega, Lucchezi, Souza and Ruiz
1998; Waller 1982), a literatura sobre a sua etiologia é bastante escassa. Neste
trabalho, foi usado um novo método de avaliação quantitativa do contorno
(Milbratz, Garcia, Guimaraes and Cruz 2012) para determinar com precisão a
localização dos picos de contorno de uma amostra de pálpebras com retração
por OG. O método consiste na utilização de um software para análise da
imagem da fenda palpebral. O princípio é o mesmo da distância entre o centro
da pupila e a margem palpebral. Porém, além de fornecer a medida central, na
posição das 12 horas, o uso do software fornece múltiplas DMCP radiais,
partindo do centro da pupila e intervaladas entre si de 15º. A intersecção
destes raios com a margem palpebral fornece os valores angulares de DMCP,
o que permite a análise quantitativa do contorno palpebral.
Este trabalho demonstrou que uma pequena assimetria lateral é um
achado normal. Pretendeu-se avaliar a simetria dos setores lateral e medial das
pálpebras superiores. Para isso, foi realizada a soma das DMCPs em cada
setor, e o valor obtido no setor lateral foi dividido pelo valor obtido no setor
91
medial. Assim, os valores maiores do que a unidade identificaram as
assimetrias laterais, e os valores menores identificaram as assimetrias mediais.
Esta constatação já é conhecida na literatura (Cruz, Akaishi and Coelho 2003;
Lemke 1991) e justificada pelo fato de que o globo ocular, em posição primária
do olhar, está medial ao eixo da órbita, fazendo com que uma parte maior de
esclera temporal seja naturalmente exposta (Lemke 1991).
Os nossos resultados mostraram também que um número substancial
de pálpebras apresentava deformidades de contorno medial. Além disso, o
nível de retração parece ser um fator importante no desenvolvimento de
anomalias do contorno.
As anomalias do contorno palpebral na retração da pálpebra superior por
OG têm sido discutidas desde o início dos anos 50. Moran (Moran 1956) foi o
primeiro a notar que, após a correção cirúrgica da retração, o lado temporal de
algumas pálpebras se mantinha muito alto e com uma aparência bizarra. Esta
deformidade lateral no pós-operatório foi reconhecida como um elemento
chave a ter em conta no decurso da cirurgia da retração palpebral. Para evitar
procede-se a uma disseção mais agressiva da porção temporal da pálpebra
(Buffam and Rootman 1978; Moran 1956; Putterman and Urist 1972; Waller
1982). Estranhamente e apesar da noção da importância de alcançar um
contorno pós-operatório adequado, vários cirurgiões têm considerado as
deformidades do contorno como uma complicação comum de qualquer tipo de
cirurgia de correção da retração palpebral por OG.
A principal dificuldade na análise das deformidades de contorno está
relacionada com um problema metodológico: como expressar linhas curvas
complexas de uma forma simples. Até recentemente, os contornos das
92
pálpebras eram avaliados subjetivamente e as anomalias descritas como arcos
góticos, entalhes, picos, lateral flare, etc. (Harvey and Anderson 1981; Older
1991; Shore 1996; Waller 1982). Deve-se salientar que a determinação do pico
do contorno não tem o mesmo significado que medição dos picos medial e
lateral. Como foi demonstrado por Flynn et al. (Flynn, Rose and Shah-Desai
2011), quando uma linha horizontal se move até tocar na pálpebra, o seu ponto
de contato expressa o local do contorno onde a primeira derivada é igual a zero
(Cruz and Garcia 2011). O ponto mais alto do contorno é sempre perto do
centro. O contorno pode ter uma deformação medial ou lateral, no entanto, o
ponto mais alto do contorno localizar-se-á perto do centro. A representação
gráfica das distâncias pálpebra-centro da pupila permite visualizar e quantificar
as deformidades de contorno em qualquer localização (Milbratz, Garcia,
Guimaraes and Cruz 2012).
Não existe na literatura a descrição do espectro de anomalias de
contorno lateral e medial na retração palpebral por OG. Na nossa casuística
verificamos que o grau de retração não está correlacionada com o grau de
proptose, noção já adiantada anteriormente (Frueh 1984). A proptose é um
sinal característico da doença, presente em aproximadamente 60% dos
doentes com OG (Bartley, Fatourechi, Kadrmas, Jacobsen, Ilstrup, Garrity and
Gorman 1996). A ocorrência de retração palpebral na ausência de exoftalmia é
bem reconhecida (Eden and Trotter 1942; Pochin 1939), contudo também é
reconhecido que grandes proptoses podem exacerbar a retração palpebral
mecanicamente: se a posição do globo ocular é muito anterior em relação à
órbita, a pálpebra superior pode não cobrir a córnea e tende a repousar sobre o
equador do globo ocular (Lemke 1991).
93
O conceito de que o grau de proptose ocular não é necessariamente
correlacionado à magnitude da retração palpebral superior é tradicional na
literatura oculoplástica (Frueh 1984). Recentemente, Cho et al estudou o efeito
da descompressão de órbita na retração palpebral de doentes com OG. Não
encontraram correlação entre mudanças nos valores de exoftalmometria e na
posição da pálpebra superior após a cirurgia (Cho, Elner, Nelson and Frueh
2011).
Verificamos ainda que os nossos resultados são concordantes com o
conceito instituído de que as anomalias de contorno lateral são frequentes na
retração da pálpebra superior por OG (Buffam and Rootman 1978; Ceisler,
Bilyk, Rubin, Burks and Shore 1995; Elner, Hassan and Frueh 2004; Levine and
Chu 1991; Liu 1993; Moran 1956; Older 1991; Putterman and Urist 1972; Shore
1996; Waller 1982). Estas anomalias, nomeadamente o sinal do "flare lateral"
pode ser explicado pelas extensões laterais importantes do MM (Morton, Elner,
Lemke and White 1996) ou pelo facto das fibras superolaterais do septo
intermuscular estarem aumentadas na OG (Goodall, Jackson, Leatherbarrow
and Whitehouse 1995) e pelo corno lateral do MEPS ser mais forte que o
medial (Anderson and Beard 1977; Morton, Elner, Lemke and White 1996).
As nossas medições indicaram que as deformidades laterais estão
localizadas sobretudo entre 120 e 150 graus. Estas anomalias deslocam-se
para mais perto do centro, a 105º, quando temos níveis elevados de retração.
Nesta situação, o número de picos mediais aumenta, sendo este um achado
novo com relevância teórica e prática.
Do ponto de vista teórico estes resultados podem indicar que a
associação de elevados graus de retração com picos do contorno localizados
94
mais centralmente, pode ser um reflexo do arranjo normal das forças que
deslocam o ponto mais alto do contorno da pálpebra para perto do centro. Além
disso,
os
pacientes
com
OG
apresentam
uma
grande
variabilidade
interindividual na distribuição das forças do MEPS e MM ao longo da margem
palpebral.
A demonstração de que existe um espectro de deformidades palpebrais
nos doentes com retração palpebral por OG tem uma grande importância na
correção cirúrgica desta retração. Como consequência desta análise é
aconselhável, durante a correção da retração, baixar a margem da pálpebra e
ao mesmo tempo atingir um contorno normal, semelhante a uma função de
segundo grau (parábola) (Milbratz, Garcia, Guimaraes and Cruz 2012). Assim
uma avaliação pré-operatória do contorno é essencial enquanto que o
enfraquecimento na porção lateral da pálpebra não é sempre o procedimento
mais importante.
2. Validação de um sistema de vídeo digital como método de registo
e quantificação dos movimentos palpebrais
O PE é responsável pela distribuição contínua e estabilidade do filme
lacrimal sobre a córnea. O movimento da pálpebra superior é essencial para
proteger a superfície ocular e assegurar a função visual (Cruz, Garcia, Pinto
and Cechetti 2011). O PE está comprometido em várias patologias que afetam
a pálpebra superior, nomeadamente, ectrópio cicatricial, retração palpebral,
lagoftalmo paralítico e cicatricial, etc. A perda de função da pálpebra superior
nestas patologias, contribui para a proteção inadequada da superfície ocular, o
95
que aumenta o risco de complicações oculares graves devido a exposição
corneana. Estas patologias são frequentemente tratadas cirurgicamente. As
cirurgias visam restaurar o pestanejo e diminuir a exposição corneana. No
entanto, a literatura oftalmológica é surpreendentemente escassa de dados
quantitativos relativos aos movimentos da pálpebra superior. Os poucos
estudos sobre cinética palpebral foram realizados em laboratório, utilizando o
magnetic search coil (Evinger, Bao, Powers, Kassem, Schicatano, Henriquez
and Peshori 2002; Evinger, Manning and Sibony 1991; Sibony, Evinger and
Manning), técnica que não se pode utilizar na prática clínica diária. O princípio
básico
da
técnica
consiste
na
obtenção
de
variações
de
sinais
eletromagnéticos que ocorrem devido a mudanças na inclinação de uma
bobina colocada num campo eletromagnético. Além do espaço necessário,
este método exige um sistema de calibração rigoroso e um software de análise
específico. Um dos trabalhos desenvolvidos teve como objetivo validar um
novo método de registo e medição precisa dos movimentos das pálpebras, que
pode ser facilmente utilizado na clínica.
A falta de dados clínicos sobre o efeito na cinética palpebral das
diferentes patologias que afetam a pálpebra superior deve-se a problemas
metodológicos. Por outro lado, não é fácil medir movimentos tão rápidos como
os movimentos de PE. Face a isto a cinética palpebral tem sido quantificada
apenas em laboratórios especializados (Evinger, Manning and Sibony 1991;
Sibony, Evinger and Manning).
Apesar de diferentes técnicas, tais como electro-oculografia dinâmica
(Barbato, De Padova, Paolillo, Arpaia, Russo and Ficca 2007; Colzato, Van den
Wildenberg and Hommel 2008; Mackert, Woyth, Flechtner and Volz 1990) e
96
eletromiografia (Holder, Scott, Hannaford and Stark 1987; Van Allen and Blodi
1962) terem sido utilizadas para gravar os pestanejos, o magnetic search coil é
considerado o melhor método para os estudar.
O magnetic search coil foi originalmente desenvolvido por Robinson para
medir movimentos rotacionais rápidos, como os sacádicos oculares (Robinson
1963). Este método permite uma alta resolução espacial (até 0,1 graus ou 0,02
milímetros). Como os deslocamentos da pálpebra superior são movimentos
rotacionais, a técnica foi utilizada para gravar o pestanejo e os movimentos
sacádicos palpebrais (Guitton, Simard and Codere 1991). Embora seja um
método extremamente sensível e preciso, a utilização do magnetic search coil
apresenta algumas dificuldades. O equipamento que gera o campo magnético
é volumoso e caro. A técnica não consegue detetar deslocamentos da pálpebra
inferior. Por fim, a fixação da bobina na área de pré-tarsal da pálpebra superior
pode ser difícil ou mesmo impossível nas pálpebras orientais com sulcos
baixos ou ausentes. Por tudo isto, esta técnica não se aplica à prática clínica
diária.
Outro método de avaliação do pestanejo é a utilização do vídeo. Este
tem sido usado como uma alternativa ao magnetic search coil desde há algum
tempo. No passado, dados clássicos sobre a fisiologia palpebral, foram obtidos
com câmaras de alta velocidade (Doane 1980). No entanto, na era précomputador, o trabalho necessário para processar várias centenas de imagens
da pálpebra superior foi uma limitação importante (Hung, Hsu and Stark 1977).
Além disso, as câmaras de alta velocidade eram caras e não eram práticas
para o uso clínico. Alguns autores tentaram superar essas limitações usando
uma câmara (proparoxítana) que processava somente linhas verticais (Gittins,
97
Martin and Sheldrick 1995). Outra opção é o uso de software que deteta
marcas específicas colocadas na pálpebra (Sforza, Rango, Galante, Bresolin
and Ferrario 2008).
Uma variante deste último método é a videonistagmografia. Esta
consiste no registo dos movimentos oculares, acompanhando o centro da
pupila. Num artigo recente, os autores desenharam num papel uma mancha
preta de 10 mm de diâmetro e anexaram a esta uma máscara de alumínio (20 x
20 mm), fixada seguidamente na extremidade livre da margem palpebral
(Casse, Sauvage, Adenis and Robert 2007). Este método tem como limitação o
facto de se verificar que a distância entre a máscara de alumínio e a pele
aumentar artificialmente o raio de rotação da pálpebra. Consequentemente, os
movimentos registados são muito maiores do que o movimento real, o que
constitui uma limitação clara deste método.
Outra técnica interessante usando o vídeo são os métodos baseados na
deteção de diferenças de brilho nas imagens da fenda palpebral durante a fase
descendente e ascendente do movimento de pestanejo (Caffier, Erdmann and
P. 2003). Com esta técnica, o olho é iluminado com uma luz infravermelha,
sendo necessário um dispositivo que deteta a sua luz refletida. Tanto a fonte de
luz como o seu detetor são montados sobre uma armação de prova. A cinética
palpebral é, portanto, medida de uma forma indireta, pelo cálculo das
diferenças de área da fenda palpebral.
O uso deste novo método aqui aplicado parece ser a solução mais
simples para medir os movimentos das pálpebras em ambientes clínicos. Este
método usa pequenos LEDs colocados sobre a pálpebra. Estes LEDs são
baratos e a intensidade do seu brilho pode ser controlada por uma fonte de
98
alimentação personalizada. Os LEDs são mais pequenos que as bobinas,
podem ser posicionados perto da margem palpebral e não provocam qualquer
artefacto posicional. Não é necessário equipamento específico e uma câmara
de alta velocidade com 120 hertz de resolução temporal, que permite uma
precisão de 0,15 mm, é bastante acessível. Com o objetivo de quantificar uma
grande quantidade de movimentos é necessário usar um software adequado
para identificar automaticamente os pestanejos e medir a amplitude e a
velocidade máxima de cada movimento. Este software está disponível e pode
ser solicitado on-line. Os nossos resultados indicam que os movimentos
palpebrais gravados com este sistema de vídeo são qualitativamente idênticos
aos obtidos com magnetic search coil. Observamos uma alta correlação entre
as medidas obtidas com os dois métodos.
Uma característica importante do vídeo é que os componentes horizontal
e vertical dos PE são registados separadamente. Embora deslocamentos
horizontais das pálpebras possam, teoricamente, ser quantificados com o
magnetic search coil, este tipo de medição não é normalmente realizada com
bobinas. O deslocamento medial da margem palpebral superior durante o
encerramento palpebral (Frueh, Hassan and Musch 2005) e o PE (Kennard and
Glaser 1964) foi previamente descrito. No entanto, não está descrita a análise
quantitativa desse deslocamento durante o pestanejo. Os nossos resultados
mostram claramente que a fase descendente do pestanejo não é um
movimento vertical puro. À medida que a pálpebra desce, há um deslocamento
horizontal da margem palpebral superior no sentido medial. Este deslocamento
medial tem sido descrito diversas vezes para pálpebra inferior. Doane (Doane
1980) no seu artigo clássico mostrou que durante a fase descendente do
99
pestanejo os pontos lacrimais superior e inferior são compactados e
deslocados medialmente. Ele mediu o deslocamento da pálpebra inferior mas
não o da pálpebra superior. Apenas descreveu que quando há um
encerramento completo da pálpebra inferior, esta é acompanhada pela
pálpebra superior. Os nossos resultados indicam que um movimento horizontal
da pálpebra superior ocorre independentemente da amplitude de pestanejo.
Este deslocamento medial da margem palpebral superior é muito semelhante
ao do movimento do globo ocular em direção nasal, que ocorre durante o
pestanejo (Bour, Aramideh and de Visser 2000; VanderWerf, Brassinga, Reits,
Aramideh and Ongerboer de Visser 2003). O movimento horizontal da pálpebra
parece ser dependente da intensidade da contração do músculo orbicular e,
portanto, não sendo um deslocamento passivo provocado pelo contacto entre
as pálpebras superiores e inferiores.
A quantificação da cinética palpebral pode ajudar na avaliação do efeito
de alguns tratamentos cirúrgicos amplamente realizados em oculoplástica. Por
exemplo, na ptose congénita a quantidade de recessão do MEPS é variável.
Alguns autores recomendam grandes quantidades de resseção do músculo
além do LW como uma opção para suspensão frontal em casos de ação pobre
do MEPS (Decock, Shah, Delaey, Forsyth, Bauters, Kestelyn, De Baere and
Claerhout 2011; Epstein and Putterman 1984; Johnson 1985). O efeito deste
tipo de cirurgia na cinética palpebral é em grande parte desconhecido. A
abordagem da paralisia de Bell irreversível é outro tema que merece ser
estudado quantitativamente. Reabilitação de pálpebras superiores paralisadas,
com inserção peso de ouro (Abell, Baker, Cowen and Porter 1998) é uma
100
cirurgia popular, mas estamos conscientes que se torna necessário caracterizar
os benefícios deste procedimento no PE.
A cinética palpebral merece também ser quantificada em situações de
retração da pálpebra superior por OG. Há uma infinidade de técnicas cirúrgicas
descritas para corrigir a posição da margem palpebral nestes doentes (Cruz,
Ribeiro, Garcia, Akaishi and Pinto 2013). No entanto, não se sabe se a redução
da retração é acompanhada por uma mudança significativa na amplitude ou na
velocidade do PE; este facto levou-nos a estudar o efeito da müllerectomia na
cinética palpebral, utilizando este método.
Em conclusão, acreditamos que é essencial a caracterização objetiva da
cinética palpebral em oftalmologia. Este sistema de vídeo simples é suficiente
para cumprir este objetivo.
3. Efeito da correção cirúrgica da retração palpebral superior no
contorno palpebral
Um dos pontos mais importantes para qualquer procedimento destinado
a corrigir a retração da pálpebra superior é evitar as anomalias de contorno
pós-operatórias. Apesar de bem conhecidas na literatura oculoplástica (Ceisler,
Bilyk, Rubin, Burks and Shore 1995; Harvey and Anderson 1981), estas
deformidades do contorno nunca foram analisadas de uma forma quantitativa.
No nosso estudo, foi utilizado o novo método atrás descrito de avaliação
quantitativa do contorno palpebral (Milbratz, Garcia, Guimaraes and Cruz 2012)
numa série de pacientes com OG submetidos a cirurgia para correção da
retração palpebral superior.
101
Há uma grande variedade de opções técnicas publicadas para a correção
cirúrgica da retração palpebral na OG. O MEPS e MM podem ser
enfraquecidos em combinação ou separadamente por via anterior (Harvey and
Anderson
1981)
ou
posterior
(Putterman
1981).
O
processo
de
enfraquecimento muscular também varia. Ambos os músculos podem ser
alongados (Grove 1980), ressecados ou recuados com (Flanagan 1980;
Meltzer 1978) ou sem uso de spacers (Harvey and Anderson 1981). Seja qual
for a técnica utilizada, há um consenso geral de que o efeito dos procedimentos
é incerto, e a maioria dos autores tentam realizar a cirurgia sob anestesia local,
de forma gradual e controlada.
Embora vários autores tenham descrito os resultados em termos de
simetria da altura da pálpebra (Chalfin and Putterman 1979; Levine and Chu
1991) ou redução da retração na porção central da pálpebra (Dixon 1982;
Khan, Garden, Faghihi and Parvin 2002; Small 1988), as anomalias de
contorno pós-operatórias são bem conhecidas e citadas como uma possível
complicação da cirurgia de correção da retração palpebral (Ceisler, Bilyk,
Rubin, Burks and Shore 1995; Liu 1993). Este ponto foi especificamente
abordado por Shore (Shore 1996) que defendeu ser insuficiente considerar
apenas a simetria ou a posição da porção central da pálpebra superior na
avaliação dos resultados pós-operatórios.
O contorno palpebral tem sido sempre analisado subjetivamente, porque,
até recentemente, não havia nenhuma forma simples de quantificar qualquer
tipo de deformação da pálpebra superior. O método utilizado é uma extensão
da medida comummente usada da altura margem palpebral ás 12 horas. Em
vez de usar apenas uma determinação linear, é fácil estabelecer a posição da
102
margem da pálpebra superior em vários ângulos com recurso a um software
específico (Milbratz, Garcia, Guimaraes and Cruz 2012).
Alguns dos nossos doentes procuraram tratamento devido a anomalias de
contorno pré-operatórias. A assimetria de contorno lateral foi detetada num
grande número de doentes operados. Ficou assim claro que, para um grande
número de pacientes, a cirurgia de uma pálpebra com retração não é apenas
para baixar a margem palpebral. O cirurgião deve alcançar o equilíbrio de
contorno lateral/ medial. Para abordar a retração lateral, é recomendável um
enfraquecimento muscular mais agressivo no setor lateral da pálpebra (Harvey
and Anderson 1981; Putterman and Fett 1986). No entanto, este procedimento
tem um risco aumentado de hipercorreção das porções lateral e central da
pálpebra. A análise quantitativa das pálpebras avaliadas subjetivamente com
resultados insatisfatórios indicaram que a maioria teve uma hipercorreção
central e medial. Estas pálpebras têm uma aparência desagradável porque a
inclinação lateral pré-operatória foi transformada num contorno plano ou com
ptose medial.
Durante o processo de enfraquecimento dos retratores da pálpebra, o
cirurgião enfrenta uma decisão crítica sobre a extensão lateral da dissecção.
Os resultados sugerem que cirurgias laterais agressivas aumentam o risco de
hipercorreção central e medial, com resultados desfavoráveis. Como já foi
referido, uma pequena assimetria lateral é um achado normal, sendo o objetivo
a ser atingido em muitos doentes (Ribeiro, Milbratz, Garcia, Fernandes, RochaSousa, Falcao-Reis and Cruz 2013).
103
4. Efeito da correção cirúrgica da retração palpebral superior (por
mullerectomia via posterior) na cinética palpebral
Como já referido, a retração da pálpebra superior é a manifestação mais
comum da OG (Cruz, Ribeiro, Garcia, Akaishi and Pinto 2013). Sabe-se que
em alguns doentes com OG, as pálpebras retraídas apresentam movimentos
anormais (Garcia, Pinto, Barbosa and Cruz 2011). Um exemplo típico é o
atraso na descida da pálpebra superior no olhar para baixo bem descrita por
Von Graefe em 1864 (Von Graefe 1864), que ficou conhecido por sinal de Von
Graefe. Acredita-se que o PE esteja anormal na OG. A diminuição da taxa e
amplitude do pestanejo são também sinais da OG descritos no passado
(Lebensohn 1964).
Embora existam inúmeras técnicas cirúrgicas para correção da retração
palpebral da OG, não temos conhecimento de qualquer estudo sobre o efeito
das diferentes modalidades cirúrgicas na função da pálpebra. Neste estudo,
utilizamos um novo método clínico de registo dos movimentos palpebrais para
medir, numa série de doentes com OG, os efeitos da müllerectomia graduada
por via posterior no PE e na amplitude dos movimentos sacádicos palpebrais.
Pensa-se que a atividade de PE seja anormal na retração palpebral
superior da OG, no entanto há poucos estudos a validar este conceito clássico.
Os resultados observados na nossa casuística confirmam, como observado
anteriormente, que a amplitude dos movimentos de PE em pacientes com OG
foi semelhante aos controlos (Garcia, Messias, Costa, Pinto, Barbosa and
Cruz). Acreditamos que qualquer investigação sobre pestanejo em OG deve
considerar as características clínicas da amostra estudada. Especificamente,
104
deve considerar-se a magnitude da retração palpebral e a evidência radiológica
de espessamento do MEPS. Na amostra que estudamos, os níveis de retração
não eram altos. Nesta nenhum doente revelava sinais de ceratopatia superficial
e o MEPS não se apresentava espessado. Além disso, o atraso do movimento
da pálpebra na infradução (lid lag) não estava presente, indicando que os
componentes elásticos das pálpebras operadas não foram seriamente afetados
pela doença. É possível que os resultados fossem diferentes numa amostra
com predomínio de pálpebras com lid lag e com clara hipertrofia do MEPS.
Mesmo na nossa amostra, com movimentos de pestanejo normais, a
müllerectomia não afetou a amplitude do PE. Este resultado sugere que o
músculo de Müller não desempenha nenhum papel na cinética do pestanejo.
No entanto, como a altura da margem palpebral diminuiu com a cirurgia, houve
um efeito benéfico evidente porque a amplitude relativa do pestanejo
aumentou. Após a cirurgia, um número substancial de movimentos encerra a
fenda palpebral enquanto uma pequena percentagem dos movimentos de
pestanejo não atinge o centro da pupila. Por outro lado este procedimento
diminui a taxa de PE. Este achado está associado ao aumento da eficácia dos
movimentos de pestanejo na proteção da córnea.
Embora a müllerectomia não tenha tido efeito na amplitude do pestanejo,
os movimentos sacádicos descendentes aumentaram significativamente após a
cirurgia. Este é outro efeito benéfico da cirurgia já que as forças passivas da
pálpebra superior são dissipadas com mais eficácia durante a infradução
aumentando consequentemente a capacidade da pálpebra relaxar. Do ponto
de vista terapêutico, o aumento dos sacádicos descendentes previne o
lagoftalmo noturno.
105
Em resumo, a müllerectomia por via posterior atua primariamente no PE
principalmente pelo seu efeito na descida da margem palpebral superior. A
cirurgia
aumenta
descendentes.
106
a
amplitude
dos
movimentos
sacádicos
palpebrais
CONCLUSÕES
A discussão que acabámos de efetuar permite-nos apresentar as
seguintes conclusões:
1. Anomalias de contorno induzidas pela retração palpebral superior da
OG:
x
O contorno palpebral superior apresenta assimetria lateral nos sujeitos
do grupo controle.
x
Na retração palpebral superior secundária à OG, a assimetria lateral do
contorno tende a ser maior se comparada com o grupo controle. Nesta
situação a maior parte dos picos de contorno encontra-se no setor lateral
da fenda. As nossas determinações objetivas indicaram que as
deformidades laterais estão localizadas sobretudo entre 120 e 150
graus.
x
Para níveis elevados de retração, as anomalias laterais localizam-se
mais centralmente, aos 105 graus, e o número de picos mediais
aumenta.
x
Os valores de exoftalmometria não apresentam correlação com a
magnitude da retração palpebral superior.
2. Validação de um sistema de vídeo digital como método de registo e
quantificação dos movimentos palpebrais:
x
A cinética palpebral pode ser medida com precisão com um sistema de
vídeo associado a LEDs, adequado à prática clínica.
x
Os nossos resultados indicam que os movimentos palpebrais gravados
com o sistema de vídeo são qualitativamente idênticos aos obtidos com
107
o magnetic search coil. Além disso, as medidas obtidas com os dois
métodos estão altamente correlacionadas.
x
Uma característica importante do nosso sistema de vídeo é que os
componentes horizontal e vertical dos pestanejos espontâneos são
registados separadamente.
x
Os nossos resultados mostram claramente que a fase descendente do
pestanejo não é um movimento vertical puro. À medida que a pálpebra
desce, há um deslocamento horizontal da margem palpebral superior no
sentido medial. Um movimento horizontal da pálpebra superior ocorre
para qualquer amplitude de pestanejo.
3. Efeito da correção cirúrgica da retração palpebral superior no contorno
palpebral:
x
Na correção cirúrgica da pálpebra superior pretende-se corrigir a
altura da pálpebra e alcançar um equilíbrio contorno lateral/
medial.
x
A análise quantitativa das pálpebras operadas e avaliadas
subjetivamente com resultados insatisfatórios indicaram que a
maioria teve uma hipercorreção central e medial. Estas pálpebras
têm uma aparência desagradável porque a inclinação lateral préoperatória foi transformada num contorno plano ou com ptose
medial.
108
x
Os resultados sugerem que debilitações laterais agressivas
aumentam o risco de hipercorreção central e medial, com
resultados desfavoráveis
x
Uma pequena assimetria lateral é um achado normal, sendo o
objetivo a ser atingido na maioria dos doentes.
4. Efeito da correção cirúrgica da retração palpebral superior (por
müllerectomia via posterior) na cinética palpebral:
x
Na nossa amostra, com movimentos de pestanejo normais, a
müllerectomia não afetou a amplitude do PE. Este resultado
sugere que o MM não desempenha nenhum papel na cinética do
pestanejo.
x
A müllerectomia por via posterior atua primariamente no PE
principalmente pelo seu efeito na descida da margem palpebral
superior. Após a cirurgia, um número substancial de movimentos
encerram a fenda palpebral e apenas uma pequena percentagem
dos movimentos de pestanejo não atinge o centro da pupila.
x
A taxa de PE diminuiu após a cirurgia, um achado que
consideramos estar associado ao aumento da eficácia dos
movimentos de pestanejo na proteção da córnea.
x
Embora a müllerectomia não tenha tido efeito na amplitude do
pestanejo, os movimentos sacádicos descendentes aumentaram
109
significativamente após a cirurgia. Do ponto de vista terapêutico,
o aumento dos movimentos sacádicos descendentes previne o
lagoftalmo noturno.
110
Capítulo VII
- Resumo
______________________________
Resumo
Resumo
RIBEIRO, SFT. Efeito da correção cirúrgica da retração palpebral superior
da orbitopatia de Graves no contorno e cinética palpebrais. Dissertação de
Doutoramento. Faculdade de Medicina da Universidade do Porto, 2014.
A retração palpebral superior é o sinal mais comum de orbitopatia de
Graves. Associa-se a um amplo e variável espectro de anomalias do contorno
e cinética palpebrais.
O trabalho de investigação descrito nesta dissertação tem como objetivo
pesquisar as repercussões morfológicas e funcionais da correção cirúrgica da
retração da pálpebra superior. Uma extensa revisão da literatura sobre o tema
revelou uma carência de dados funcionais das inúmeras técnicas descritas
para a correção deste tipo de retração. Verificou-se também que as
deformações da margem palpebral induzidas pela retração nunca tinham sido
objeto de cuidadoso estudo quantitativo.
A nossa investigação pode dividir-se nos seguintes objetivos: i) análise
quantitativa do contorno palpebral em doentes com retração palpebral superior
secundária à orbitopatia de Graves; determinação das anomalias de contorno
induzidas pela retração palpebral e verificação do papel da magnitude da
retração palpebral e da exoftalmometria nas anomalias do contorno; ii)
validação de um novo método que permite registar e medir os movimentos das
pálpebras (sistema baseado na análise digital de imagens de vídeo); iii)
avaliação do efeito da correção cirúrgica da retração palpebral superior no
contorno palpebral e identificação das anomalias de contorno induzidas pela
cirurgia (determinantes de mau resultado estético e/ou funcional); iiii) medição
do efeito da müllerectomia via posterior na amplitude do pestanejo espontâneo
e dos movimentos sacádicos palpebrais descendentes.
Os estudos desenvolvidos nesta dissertação conduziram aos seguintes
resultados: i) o contorno palpebral superior apresenta assimetria lateral nos
sujeitos do grupo controle; na retração palpebral superior, a assimetria lateral
do contorno tende a ser maior se comparada com o grupo controle; em 60%
das pálpebras com retração estudadas, o pico de contorno encontrava-se no
setor lateral da pálpebra (sobretudo entre os 120 e os 150 graus); para níveis
elevados de retração, as anomalias laterais localizam-se mais centralmente,
aos 105 graus, e o número de picos mediais aumenta; os valores de
exoftalmometria não apresentam correlação com a magnitude da retração
palpebral superior; ii) os traçados do pestanejo registados com o magnetic
search coil e o novo sistema de vídeo foram praticamente idênticos; a
distribuição da amplitude dos pestanejos foi idêntica; a relação entre a
amplitude e a velocidade máxima (main sequence) foi comparada por meio de
regressão linear com valores médios de r = 0,81 (magnetic search coil) e 0,85
(vídeo); os gráficos de Bland-Altmann mostraram boa concordância entre os
métodos para os valores médios de todos os sujeitos; um movimento horizontal
da pálpebra superior ocorre para qualquer amplitude de pestanejo; a amplitude
do deslocamento horizontal da pálpebra superior durante o pestanejo foi 40%
113
Resumo
do movimento vertical da fase descendente do pestanejo; iii) a análise
quantitativa das pálpebras operadas e avaliadas subjetivamente com
resultados insatisfatórios indicaram que a maioria teve uma hipercorreção
central e medial (contorno plano ou ptose medial); cirurgias laterais agressivas
aumentam o risco de hipercorreção central e medial, com resultados
desfavoráveis; uma pequena assimetria lateral é um achado normal, sendo o
objetivo a ser atingido na maioria dos doentes; iiii) a müllerectomia reduz
significativamente a média da distância entre o centro da pupila e a margem
palpebral superior das pálpebras operadas (p<0,001); a amplitude dos
movimentos sacádicos palpebrais descendentes aumentou significativamente
com a müllerectomia (p<0,001); a cirurgia não modificou o valor absoluto da
amplitude (p=0,12) nem da velocidade máxima (p=0,14) dos pestanejos
espontâneos; a amplitude relativa do pestanejo espontâneo em relação ao
centro da pupila aumentou significativamente: o número de pestanejos que não
atingem o centro da pupila diminuiu de 17,4 para 4,3% e o número de
movimentos que encerram completamente a fenda palpebral aumentaram de 0
para 13%; como a eficácia do pestanejo aumentou, a taxa de pestanejo
espontâneo média diminuiu significativamente (p=0,046).
Os trabalhos realizados permitiram tirar as seguintes conclusões: i) as
anomalias de contorno laterais são mais frequentes que as mediais; nas
retrações de menor magnitude há predomínio de anomalias laterais; nas
grandes retrações, o número de deformações mediais iguala o das laterais; ii) a
cinética do pestanejo pode ser medida com precisão através de um sistema de
vídeo apropriado para ambientes clínicos; iii) a avaliação pré-operatória é
essencial para um bom resultado pós-operatório, evitando hiper ou
hipocorreções segmentares; maus resultados cirúrgicos são representados por
hipercorreções centrais e mediais ou hipocorreções laterais; uma pequena
assimetria lateral está presente em indivíduos normais e é frequentemente
avaliada como um bom resultado cirúrgico; iiii) a müllerectomia permite que as
forças passivas da pálpebra superior sejam dissipadas na infradução,
aumentando a capacidade da pálpebra relaxar e, assim, impedindo o
lagoftalmo noturno; o efeito sobre os pestanejos espontâneos é principalmente
devido à posição de repouso inferior da pálpebra após a cirurgia.
Este conjunto de trabalhos fornece vários dados novos sobre a retração
palpebral superior secundária à orbitopatia de Graves com implicações no seu
tratamento cirúrgico.
114
Capítulo VIII - Abstract
______________________________
Abstract
Abstract
RIBEIRO, SFT. Effect of surgical correction of Graves upper eyelid
retraction in eyelid contour and kinematics. Doctoral Dissertation.
Faculdade de Medicina da Universidade do Porto, 2014.
The upper eyelid retraction is the most common sign of Graves
orbitopathy. It is associated with a wide and variable spectrum of abnormalities
of the eyelid contour and kinetics.
The research described in this thesis aims to investigate the
morphological and functional effects of surgical correction of Graves upper
eyelid retraction. An extensive review of literature related to this topic revealed a
lack of functional data of the numerous techniques described for the correction
of this type of retraction. It was also found that the eyelid margin deformation
induced by retraction had never been the object of careful quantitative study.
Our research can be divided into the following objectives: i) quantitative
analysis of eyelid contour in patients with upper eyelid retraction secondary to
Graves' orbitopathy; determination of contour anomalies induced by eyelid
retraction and verification the role of the magnitude of eyelid retraction and
exophthalmometry in contour abnormalities; ii) validation of a new method to
measure and record the movements of the eyelids (system based on digital
analysis of video images); iii) to assess the effect of surgical correction of upper
eyelid retraction on eyelid contour and identification the eyelid contour
abnormalities induced by surgery (determinants of poor aesthetic and/or
functional result); iiii) to measure the effect of müllerectomy by posterior
approach in the amplitude of spontaneous blinking and downward eyelid
saccades.
The studies carried out in this thesis, led to the following results: i) the
upper eyelid contour features lateral asymmetry in the control group subjects; in
upper eyelid retraction, the lateral asymmetry of the contour tends to be greater
when compared with the control group; in 60% of the retracted eyelids studied,
the peak of contour was at the temporal section of the lid (in particular between
120 and 150 degrees); for high levels of retraction, the contour anomalies are
located more centrally and the number of medial peaks increases; the values of
exophthalmometry are not correlated with the magnitude of the upper eyelid
retraction; ii) blinking records registered with magnetic search coil and the new
vídeo system were virtually similar; the distribution of the blink amplitude was
identical; the relationship between amplitude and maximum velocity (main
sequence) was compared by linear regression with mean values of r=0.81
(magnetic search coil) and 0.85 (video); Bland–Altmann graphics showed good
agreement between the methods for the mean values of all subjects; a
horizontal movement of the upper eyelid occurs for any range of blinking; the
amplitude of the horizontal displacement of the upper eyelid during blinking was
40% of the vertical motion of the descending phase of blinking iii) the
quantitative analysis of the eyelids operated and evaluated subjectively as
unsatisfactory results indicated that most had a central and medial
117
Abstract
overcorrection (plan contour or medial ptosis); aggressive lateral surgeries
increase the risk of central and medial overcorrection, with poor results; a small
lateral asymmetry is a normal finding, and the goal to be achieved in most
patients; iiii) müllerectomy significantly reduces the mean distance between the
pupil center and the upper eyelid margin of the operated lids (p<0.001); the
amplitude of the downward eyelid saccades increased with müllerectomy
(p<0.001); surgery did not change the absolute value of the amplitude (p=0.12)
or maximum velocity (p=0.14) of spontaneous blinking; the relative amplitude of
spontaneous blinking in relation to the pupil center increased significantly: the
number of blinks not reaching the pupil center has decreased from 17.4 to 4.3%
and the number of movements that completely closes the eyelid fissure
increased from 0 to 13%; as the efficiency of the blink increased, the medium
rate of spontaneous blinking decreased significantly (p=0.046).
The research allowed the following conclusions: i) the lateral contour
anomalies are more frequent than the medial; in lower degrees of retraction
there is a predominance of lateral anomalies; in high levels of retraction, the
number of medial and lateral deformations is identical; ii) the kinetics of blinking
can be measured accurately using a digital video system suitable for clinical
settings; iii) the preoperative evaluation is essential for a good postoperative
result, avoiding segmental over or undercorrections; poor surgical results are
represented by central and medial overcorrections and by lateral
undercorrections; a small lateral asymmetry is present in normal individuals and
is often assessed as a good outcome; iiii) müllerectomy relieves the passive
forces of the upper eyelid, increasing the ability of the upper eyelid to relax in
downgaze, preventing nocturnal lagophthalmos; the effect on spontaneous
blinking is mainly due to the lower rest position of the eyelid after surgery.
These studies provide several new data on the upper eyelid retraction
secondary to Graves' orbitopathy with implications on surgical treatment.
118
Capítulo IX
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