Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging

doi:10.1016/S0002-9394(02)01695-1

American Journal of Ophthalmology

Volume 134, Issue 6, December 2002, Pages 872-878

https://doi.org/10.1016/S0002-9394(02)01695-1 Get rights and content

Abstract

PURPOSE: To compare normal functional anatomy of rectus extraocular muscles (EOMs) and pulleys in normal older humans with previously reported findings in younger subjects.

DESIGN: Experimental study of the orbits of normal healthy older volunteers by magnetic resonance imaging (MRI).

METHODS: In planes perpendicular to the orbital axis, contiguous MRI images spanned the anteroposterior extents of 22 orbits in 12 older adults with an average age of 65.2 years (range, 56–74). Images were obtained in central gaze in all subjects and repeated in supraduction, infraduction, abduction, and adduction in some subjects. Mean EOM cross-sectional area centroids were normalized to an oculocentric coordinate system and plotted over the length of each EOM to determine paths.

RESULTS: Compared with images obtained using identical technique in 12 younger subjects (average age, 28.5 years, range 21–33), the horizontal rectus EOMs in the 12 older subjects were significantly displaced inferiorly throughout the anteroposterior extent of the orbit. The vertical rectus EOM was positioned identically to those of younger subjects. Inflections in EOM paths produced by the connective tissue pulleys could not be determined in most older subjects, because of difficulties in maintaining extreme eccentric gaze. For one subject who was able to do this, the anteroposterior location of the medial rectus pulley inferred from path inflection was similar to that of younger subjects.

CONCLUSIONS: The horizontal rectus EOMs are displaced inferiorly in the elderly relative to the globe center. This displacement presumably reflects an inferior location of the corresponding pulleys, partially converting horizontal rectus EOM force to depression. This may contribute to the observed impairment of elevation in older people and predispose them to a characteristic pattern of incomitant strabismus.

Section snippets

Methods

Twelve older adult volunteers were recruited by advertisement and examined to verify normal ocular motility. After obtaining written informed consent according to a protocol conforming to the Declaration of Helsinki and approved by the Human Subject Protection Committee at the University of California, Los Angeles, each subject underwent high-resolution, T₁-weighted MRI using a 1.5-T General Electric Signa (Milwaukee, Wisconsin, USA) scanner.

The technique used to acquire and analyze the images

Results

The 12 subjects ranged in age from 56 to 74 years (average, 65.2 years). Based on the change in position of the globe-optic nerve junction, average elevation (16.3 degrees) and depression (16.4 degrees) were nearly identical, with slightly more adduction (25.1 degrees) than abduction (21.2 degrees). All values except abduction were at least 5 degrees less than achieved by younger subjects in a previously published study using identical techniques,14 although only the difference in depression

Discussion

This study demonstrates significant changes in the functional anatomy of the horizontal rectus EOMs of older people. Analogous to the age-related degenerative changes in the tarsal insertion of the levator palpebrae superioris leading to blepharoptosis, the MR and LR follow paths relatively more inferior to globe center than in younger subjects. Recent evidence indicates that rectus EOM paths reflect the locations of the guiding pulleys through which the EOMs pass before inserting on the sclera.

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Advancement of the muscle insertion toward the limbus as an alternative or adjunct to resection
2022, Journal of AAPOS
Citation Excerpt :
Our proposed technique of muscle advancement may be another alternative, and it has the advantage of being easy to perform and reversible when necessary. Acquired small-angle esodeviation for distance can be related to progressive changes in laxity of orbital connective tissues with age.9,10 This divergence insufficiency pattern11,12 can also rarely be associated with a neurological condition, such as a residual abducens nerve paresis.12
To describe the surgical outcomes of patients that underwent strabismus surgery involving advancement of the muscular insertion line toward the limbus.
The medical records of patients who underwent rectus muscle advancement surgery between January 2009 and June 2019 and had at least 1 year of follow-up were reviewed retrospectively. Patients were classified into one of four types of deviation: (1) convergence insufficiency, without distance deviation; (2) small-angle distance esotropia, with diplopia; (3) residual strabismus after previous surgery; and (4) large-angle exotropia. The first group underwent 2 mm advancement of the medial rectus insertion bilaterally; the second, 2–3 mm advancement of the lateral rectus muscle bilaterally; the third, 2–3 mm advancement of the lateral or medial rectus muscle, with or without simultaneous resection; and the fourth, 3 mm advancement of the medial rectus with simultaneous resection, with or after maximum recession of the lateral rectus, bilaterally or unilaterally.
A total of 25 patients were included (mean age, 28.76 ± 22.75 years): 4 with convergence insufficiency, 3 with small-angle distance esotropia and diplopia, 16 with residual strabismus, and 2 with large-angle exotropia. Mean postoperative follow-up was 4.76 ± 2.03 years. Surgery was successful in all patients at 1 year (residual deviation ≤10^Δ), and all but 1 at 5 years; 1 patient required reoperation.
Advancement of the muscle insertion proved successful as an alternative or adjunctive procedure to other forms of muscle tightening in the subtypes of patients evaluated in this study.
Prevalence of Sagging Eye Syndrome in Adults with Binocular Diplopia
2020, American Journal of Ophthalmology
Sagging eye syndrome (SES), horizontal and/or vertical strabismus caused by orbital connective tissue degeneration, was first defined 10 years ago. This study investigated SES and other causes of acquired binocular diplopia in adults presenting to a single institution since the description of SES.
Retrospective observational case series.
Medical records were reviewed of all new patients over the age of 40 who presented to the Stein Eye Institute with binocular diplopia between January 2015 and December 2018. Clinical causes of diplopia were tabulated in patients grouped by age and sex. In patients with SES, we tabulated binocular alignment, types of treatment, and surgical outcomes.
There were 945 patients of mean age 66.5 years, of whom 514 (54.4%) were female. The most common cause of diplopia was SES (31.4%). The 297 patients with SES were older at 71.2 years (P < 0.0001) and more predominantly female at 59.9% than other patients (52.0%; P = 0.023). The relative proportion of SES patients among all diplopic patients increased with age from 4.7% under age 50 years to 60.9% over the age of 90. Age-related distance esotropia was present in 35% and cyclovertical strabismus in 65% of cases of SES. Strabismus surgery was performed in 50% of cases of SES. Mean esotropia at distance decreased from 6.9 ± 0.7Δ preoperatively to 0.3 ± 0.3Δ postoperatively. Preoperative hypertropia decreased from 3.0 ± 0.3Δ to 0.7 ± 0.2Δ postoperatively. Surgery resolved diplopia in all cases.
It is important to recognize that SES is a very common cause of adult binocular diplopia.
Difference between vertical and horizontal saccades across the human lifespan
2019, Experimental Eye Research
The purpose of the study was to analyze vertical saccade parameters (latency, peak velocity, amplitude gain), and compare them to those of horizontal saccades in a cross-sectional study across the ages of the human lifespan. One hundred and thirty one participants (62 males) between the ages of 3 and 86 years made vertical prosaccades of 2–44° in response to a dot stimulus projected on a screen. A subset of participants also made horizontal prosaccades of 2–60° under the same conditions. The El-Mar (Downsview, Ontario, Canada) eye tracker was used to record binocular eye movements. Measures of saccadic latency, peak velocity and amplitude gain were calculated for each participant. Differences between saccade parameters for upward & downward saccades were calculated. Vertical saccade parameters were evaluated as a function of age and age related differences between vertical and horizontal saccade parameters were determined. There was no significant difference between upward and downward saccades and no effect of age for either latency or peak velocity. Downward saccades had significantly higher gains than upward saccades (p = 0.0001) and this difference increased significantly with age (p = 0.001). Vertical saccadic latency initially decreased from about 400 ms at 4 years of age, remained stable for a period of time and then increases again in later life. The lowest peak velocities were found in participants under 20 and over 70 years of age, while the highest peak velocities were seen in participants between 20 and 60 years of age. The majority of vertical saccades were hypometric. Saccadic amplitude gains varied depending on both the stimulus size (p = 0.0001) and age (p = 0.0001) of participants. Vertical saccades are most accurate for small amplitudes and for participants between 20 and 30 years of age. Vertical saccades had significantly longer latencies than horizontal saccades (p = 0.0001) but there was no significant effect of age. Vertical saccades had lower peak velocities than horizontal saccades in very young children but this difference decreased with age (p = 0.0015). Large vertical saccades were more hypometric than their horizontal counterparts across all ages. The observed differences in saccadic parameters could be related to the different areas in the brain used for saccadic generation, different periods and/or mechanisms of development and senescence within the visual system and brain and/or the effects of differential use.
Rectus Extraocular Muscle Paths and Staphylomata in High Myopia
2019, American Journal of Ophthalmology
To investigate the relationship between displacement of extraocular muscles (EOMs) and staphyloma in high myopia using magnetic resonance imaging (MRI).
Retrospective case-control study.
Setting: Institutional study. Population: Twenty-nine highly myopic patients (46 eyes), 11 age-matched healthy control subjects (21 eyes), and 34 patients (66 eyes) with sagging eye syndrome. Procedures: MRI was analyzed for aspect ratio (AR) of the ocular cross section, locations of staphylomata and EOMs, and status of superior rectus to lateral rectus (SR-LR) band ligament. Main Outcome Measures: Association between staphylomata with EOM paths and the LR-SR band.
Several associations of staphylomata were statistically significant (P < .05). Most staphylomata were superotemporal. Myopic patients with staphyloma had larger ARs in quasi-coronal images than in myopic subjects without staphyloma or normal controls. Compared to patients with high myopia without staphyloma and normal controls, when staphyloma was present, there was more inferior LR displacement, larger LR-globe angle, and larger SR-LR displacement angle than in myopic subjects without staphyloma. Staphyloma in the superotemporal quadrant was associated with greater SR-LR angle than in other quadrants. There were significantly more ruptures of SR-LR band ligament in highly myopic patients with staphyloma than in those without staphyloma.
Local staphylomata in high myopia reflect ocular asphericity and correlate with EOM paths. Myopic staphylomata are associated with inferior displacement of LR path and defect of the LR-SR band ligament.
Long-term evolution of age-related distance esotropia
2018, Journal of AAPOS
Citation Excerpt :
They also observed that the mean heterophoria value for distance fixation was exophoric except in their 71- to 80-year-old group, which was esophoric. Although the etiology of ARDET is still not clear, it is likely secondary to involutional changes within the orbit14; most notably, sagging and inferior displacement of the lateral rectus muscles and its pulleys, caused by tendon laxity due to degeneration.5-15 Recent studies of Chaudhuri and Demer16-18 have shown that sagging and bilaterally symmetrical downward displacement of the lateral rectus pulleys may symmetrically reduce supraduction and may cause esodeviation and horizontal diplopia at distance.
To evaluate the evolution of horizontal deviation and fusional amplitudes both at distance and at near in patients with age-related distance esotropia (ARDET).
The medical records of consecutive patients diagnosed with ARDET between January 2008 and March 2016 were reviewed retrospectively. Patients with at least 60 months’ follow-up were eligible for inclusion. Horizontal deviation, fusional convergence amplitude, and fusional divergence amplitude both at distance and at near were compared.
Of 131 cases reviewed, 31 patients were identified for inclusion. Median age at diagnosis was 73 years. Median distance esodeviation was 6^Δ esotropia at initial examination (range, 2^Δ-12^Δ esotropia) and 8^Δ eostropia at final examination (range, 2^Δ-25^Δ esotropia). Median near deviation was orthophoria at initial examination (range, 10^Δ exophoria to 8^Δ esophoria) and 4^Δ esophoria at final examination (range, 4^Δ exophoria to 14^Δ esophoria). Median fusional divergence amplitude at distance was 4^Δ at initial and at final examinations. At near, median fusional divergence amplitude was 8^Δ at initial and at final examinations. Median fusional convergence amplitude at distance was 14^Δ at initial examination and 12^Δ at final examination. At near, median fusional convergence amplitude was 26^Δ at initial and at final examinations. Base-out prisms were prescribed in all patients. In 23 patients the prism correction gradually increased. Strabismus surgery was performed in 3 patients.
Our patients with ARDET experienced a slight increase in distance esodeviation (P < 0.001), whereas no significant change in fusional amplitudes was observed over time (P ≥ 0.05).
Orbital magnetic resonance imaging is useful in age-related distance esotropia
2018, Journal of Optometry
To describe findings for orbital magnetic resonance imaging (MRI) in patients with age-related distance esotropia (ARDE).
We compared 31 orbital MRI from patients with ARDE (77 ± 7 SD years) with 2 control groups: 32 orbits from individuals aged 18–50 years (33 ± 8 SD years) and 16 orbits from individuals aged >60 years (77 ± 7 SD years). MRI scans were acquired using 3D fast field echo in T1 sequence without fat saturation. Exclusion criteria for all groups were neurological or thyroid disease and a relevant ophthalmological history (e.g., high myopia, diplopia from another etiology, complicated cataract surgery, etc.). Muscle displacement and characteristics of the lateral rectus–superior rectus (LR–SR) intermuscular band were analyzed.
The analysis of the muscles and angles revealed a series of statistically significant differences (p < 0.07) between the groups. Subjects with ARDE had LR pulley positions 1.32 ± 0.19 mm lower than in younger controls, and the medial rectus (MR) pulley positions were 0.68 ± 0.19 mm lower than in younger. Older controls had LR and MR pulley positions 0.85 ± 0.20 mm and 0.49 ± 0.23 mm lower than in younger. ARDE subjects had LR pulley positions 0.46 ± 0.26 mm lower than in older control group. The LR–SR band was absent in 35.5% of ARDE patients and in 12.5% of older control group (p = 0.168).
MRI showed that displacements of LR and LR–SR band degeneration could facilitate the diagnosis of patients with ARDE.
Describir los hallazgos encontrados en la resonancia magnética orbitaria (RMN) en pacientes con esotropía asociada a la edad (ETAE).
Comparamos 31 RMN orbitarias de pacientes con ETAE (77 ± 7 DE años) con 2 grupos control: 32 órbitas de individuos con edades comprendidas entre 18 y 50 años (33 ± 8 DE años) y 16 órbitas de individuos con edades >60 años (77 ± 7 DE años). Las RMN se adquirieron utilizando eco de campo rápido 3D en secuencia T1 sin saturación de grasa. Los criterios de exclusión para todos los grupos fueron enfermedad neurológica o tiroidea y antecedentes oftalmológicos relevantes (ej.: alta miopía, diplopía de otra etiología, cirugía complicada de cataratas …). Se analizaron el desplazamiento muscular y las características de la banda intermuscular recto lateral-recto superior (RL-RS).
El análisis de los músculos y ángulos reveló una serie de diferencias estadísticamente significativas (p < 0,07) entre los grupos. Los sujetos con ETAE presentaban la polea del RL 1,32 ± 0,19 mm inferior a los controles jóvenes y la polea del recto medial (RM) 0,68 ± 0,19 mm inferior a los sujetos jóvenes. Los controles de mayor edad tenían las poleas del RL y del RM posicionadas 0,85 ± 0,2 mm y 0,49 ± 0,23 mm inferiores a los jóvenes. Los sujetos con ETAE tenían la polea del RL 0,46 ± 0,26 mm inferior a la del grupo control de mayor edad. La banda RL-RS estaba ausente en el 35,5% de los pacientes con ETAE y en el 12,5% del grupo control de mayor edad (p = 0,168).
La RMN reflejó que los desplazamientos del RL y la degeneración de la banda RL-RS podrían facilitar el diagnóstico de los pacientes con ETAE.

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^☆: This work was supported by NEI grant EY-08313. Joseph L. Demer received an unrestricted award from Research to Prevent Blindness and is Laraine and David Gerber Professor of Ophthalmology.

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Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging☆

Abstract

Section snippets

Methods

Results

Discussion

Surv Ophthalmol

Vision Res

J. AAPOS

J Am Assoc Ped Ophthalmol Strabismus

Am J Ophthalmol

J AAPOS

Am J Ophthalmol

Details of the orbital connective tissue system in the adult

Acta Morphol Neerl Scand

The first results of a new anatomical method of approach to the human orbit following a clinical enquiry

Acta Morphol Neerl Scand

Traite d’anatomie descriptive avec figures intercalees dans le texte

Structural organization of the extraocular muscles

Sideways displacement and curved path of recti eye muscles

Arch Ophthalmol

Location and stability of rectus muscle pulleys inferred from muscle paths

Invest Ophthalmol Vis Sci

Displacement of the medial rectus pulley in superior oblique palsy

Invest Ophthalmol Vis Sci