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1.  Changes in Binocular Alignment after Surgery for Concomitant and Pattern Intermittent Exotropia* 
Strabismus  2008;16(2):57-63.
Although early post-surgical over-correction for exotropia is widely advised, post-operative drift has not been well quantified in concomitant exotropia, and has not been described specifically with A and V patterns. While such patterns have been proposed to result from abnormal locations of the rectus muscle pulleys, others have suggested that A and V patterns may result from the disruption of fusion arising from exotropia itself.
We prospectively performed Hess screen analysis in 20 exotropic patients (mean age 42 ± 16 yrs) before and two to six times after strabismus surgery, with a post-operative follow-up of 2–108 weeks. Primary surgery cases included medial rectus resection (2) and lateral rectus recession (10), combined resection/recession (6), and superior oblique tenectomy (2). Alignment trends in primary and secondary gazes were analyzed for concomitant, pattern, and re-operated subgroups. Results were also analyzed by type of surgery performed.
Mean pre-operative central gaze exotropia was 8.6 ± 7.1°. Twelve cases were concomitant, while 8 exhibited A or V patterns. Twelve cases were re-operations. In initial surgery for concomitant exotropia, there was a well-defined exotropic drift approaching 5° by 30 weeks post-operatively (linear regression, r = 0.43, p = 0.01). There was similar exo drift in re-operations. However, in pattern exotropia, post-operative drift was more variable, with mean esotropic drift of approximately 5° (r = 0.18, p = 0.43). For all patients, final post-operative central gaze exotropia was 1.9 ± 5.8°, with significant pattern collapse (p < 0.01).
Post-operative exo-shift of about 5° occurs in initial and re-operated concomitant exotropia. However, in A and V patterns, there is no definitive direction of post-operative drift, suggesting that pattern strabismus may be more likely due to mechanical factors in the orbit than to neural factors associated with fusion disruption.
Alignment following strabismus surgery differs in concomitant vs. pattern exotropia. Initial over-correction of about 5° is advisable for concomitant exotropia, but should be avoided in A and V patterns.
PMCID: PMC2796603  PMID: 19995177
Concomitant exotropia; pattern exotropia; strabismus surgery; postoperative drift; binocular alignment; over-correction
2.  Biomechanics of superior oblique Z-tenotomy 
A recent report suggests that 70%-80% Z-tenotomy of the superior oblique tendon is necessary to effectively treat A-pattern strabismus associated with over depression in adduction. To clarify the clinical effect, we compared the biomechanics of Z-tenotomy on the superior oblique tendon, superior rectus tendon, and isotropic latex material.
Fresh bovine superior oblique tendons were trimmed to 20 mm × 10 mm dimensions similar to human superior oblique tendon and clamped in a microtensile load cell under physiological conditions of temperature and humidity. Minimal preload was applied to avoid slackness. Tendons were elongated until failure following Z-tenotomies, made from opposite tendon sides, spaced 8 mm apart and each encompassing 0%, 20%, 40%, 50%, 60%, or 80% tendon width. Digitally sampled failure force was monitored using a precision strain gauge. Control experiments were performed in similar-sized specimens of bovine superior rectus tendon and isotropic latex.
Progressively increasing Z-tenotomy of latex caused a linearly graded reduction in force. In contrast, Z-tenotomy of up to 50% in superior oblique and superior rectus tendons caused nonlinear reduction in force transmission that reached a negligible value at 50% tenotomy and greater.
Z-tenotomy up to 50% progressively reduces extraocular tendon force transmission, but Z-tenotomy of ≥50% is biomechanically equivalent in vitro to complete tenotomy.
PMCID: PMC3858822  PMID: 24321425
3.  Traumatic longitudinal splitting of the inferior rectus muscle 
Orbital floor fractures and associated injuries can cause strabismus. We present the case of a 34-year-old man with incomitant strabismus following orbital reconstruction after a high-impact baseball injury. Multipositional, high-resolution magnetic resonance imaging (MRI) revealed extensive longitudinal splitting of the inferior rectus muscle by an orbital floor implant that separated its orbital and global layers.
PMCID: PMC3098934  PMID: 21463958
4.  Sagging Eye Syndrome 
JAMA ophthalmology  2013;131(5):619-625.
Recognition of sagging eye syndrome (SES) as the cause of chronic or acute acquired diplopia may avert neurologic evaluation and imaging in most cases.
To determine whether SES results from inferior shift of lateral rectus (LR) extraocular muscle (EOM) pulleys and to investigate anatomic correlates of strabismus in SES.
Design and Setting
We used magnetic resonance imaging to evaluate rectus EOMs, pulleys, and the LR– superior rectus (SR) band ligament at an eye institute.
Patients with acquired diplopia suspected of having SES. We studied 56 orbits of 11 men and 17 women (mean [SD] age of 69.4 [11.9] years) clinically diagnosed with SES. Data were obtained from 25 orbits of 14 control participants age-matched to SES and from 52 orbits of 28 younger controls (23[4.6] years).
Main Outcome Measures
Rectus pulley locations compared with age-matched norms and lengths of the LR-SR band ligament and rectus EOMs. Data were correlated with facial features, binocular alignment, and fundus torsion.
Patients with SES commonly exhibited blepharoptosis and superior sulcus defect. Significant infero-lateral LR pulley displacement was confirmed in SES, but the spectrum of abnormalities was extended to peripheral displacement of all other rectus pulleys and lateral displacement of the inferior rectus pulley, with elongation of rectus EOMs (P < .001). Symmetrical LR sag was associated with divergence paralysis esotropia and asymmetrical LR sag greater than 1mm with cyclovertical strabismus. The LR-SR band was ruptured in 91% of patients with SES.
Conclusions and Relevance
Widespread rectus pulley displacement and EOM elongation, associated with LR-SR band rupture, causes acquired vertical and horizontal strabismus. Small-angle esotropia or hypertropia may result from common involutional changes in EOMs and orbital connective tissues that may be suspected from features evident on external examination.
PMCID: PMC3999699  PMID: 23471194
5.  Long-Term Outcome of Medial Rectus Recession and Pulley Posterior Fixation in Esotropia With High AC/A Ratio 
Strabismus  2012;20(3):115-120.
Medial rectus (MR) recession with pulley posterior fixation (PF) can be used to treatesotropia (ET) with a high accommodative convergence to accommodation (AC/A) ratio as effectively in the short term as MR recession with scleral PF. This study provides a novel examination of the long-term results of MR recession with pulley PF (PPF).
In 21 children we performed bilateral MR recession and pulley PF for ET greater at near than distance (high AC/A). Mean follow-up was 3.5 ± 2.5 (standard deviation [SD]) years.
Mean age at presentation was 2.7 ± 1.8 and at surgery 4.3 ± 1.6 years. Fourteen (67%) children had amblyopia. Distance and near pre-operative ET averaged 19.6Δ ± 10.5Δ and 36.9Δ ± 18.9Δ, respectively. Mean near-distance (N-D) disparity was 16.4Δ ± 12.3Δ. The MR recession averaged 4.4 ± 0.9 mm. Early mean postoperative ET was 1.3 ± 3.3Δ at distance and 2.8Δ ± 5.2Δ at near. Mean late postoperative ET was 0.1Δ ± 5.8Δ and 1.0Δ ± 6.2Δ at distance and near, respectively. At the final postoperative examination, mean N-D disparity was reduced to 0.9Δ ± 3.6Δ.
MR recession with PPF has a high long-term effectiveness, even in patients with amblyopia and autism. Since no posterior scleral suturing is required, it minimizes the perforation risk associated with scleral PF.
MR recession with PPF is a safe and highly effective long-term treatment for ET with high AC/A ratio. Long-term results may surpass those of alternate procedures.
PMCID: PMC3979307  PMID: 22906381
Esotropia; Pulley; Strabismus
6.  Ocular Manifestations of Oblique Facial Clefts 
The Journal of craniofacial surgery  2010;21(5):1630-1631.
In the Tessier classification, craniofacial clefts are numbered from 0 to 14 and extend along constant axes through the eyebrows, eyelids, maxilla, nostrils, and the lips. We studied a patient with bilateral cleft 10 associated with ocular abnormalities.
Clinical report with orbital and cranial computed tomography.
After pregnancy complicated by oligohydramnios, digoxin, and lisinopril exposure, a boy was born with facial and ocular dysmorphism. Examination at age 26 months showed bilateral epibulbar dermoids, covering half the corneal surface, and unilateral morning glory anomaly of the optic nerve. Ductions of the right eye were normal, but the left eye had severely impaired ductions in all directions, left hypotropia, and esotropia. Under anesthesia, the left eye could not be rotated freely in any direction. Bilateral Tessier cleft number 10 was implicated by the presence of colobomata of the middle third of the upper eyelids and eyebrows. As the cleft continued into the hairline, there was marked anterior scalp alopecia. Computed x-ray tomography showed a left middle cranial fossa arachnoid cyst and calcification of the reflected tendon of the superior oblique muscle, trochlea, and underlying sclera, with downward and lateral globe displacement.
Tessier 10 clefts are very rare and usually associated with encephalocele. Bilateral 10 clefts have not been reported previously. In this case, there was coexisting unilateral morning glory anomaly and arachnoid cyst of the left middle cranial fossa but no encephalocele.
Bilateral Tessier facial cleft 10 may be associated with alopecia, morning glory anomaly, epibulbar dermoids, arachnoid cyst, and restrictive strabismus.
PMCID: PMC3976670  PMID: 20856062
Dermoid; facial cleft; morning glory anomaly; strabismus
7.  Functional magnetic resonance imaging of horizontal rectus muscles in esotropia 
Monkey neurophysiology suggests that changes in neural drive rather than extraocular muscle structure underlie sensory-induced strabismus. If this is true, then extraocular muscle structure should be normal. We used magnetic resonance imaging to measure horizontal rectus muscle size and contractility to determine whether muscle structure is a factor in human concomitant esotropia.
High-resolution, quasicoronal plane magnetic resonance imaging was performed in target-controlled central gaze, abduction, and adduction in 13 orthotropic controls (mean age, 38 ± 19 years) and 12 adults (mean age, 52 ± 16 years) who had concomitant esotropia averaging 28Δ ± 18Δ at distance. Thyroid ophthalmopathy was excluded. Horizontal rectus muscle cross sections were determined in 6 contiguous, 2-mm-thick midorbital image planes. Contractility was computed in each plane as the difference in cross section from contraction to relaxation.
Medial rectus muscle cross sections in multiple planes averaged up to 39% larger in esotropic patients than in controls (P <0.005), whereas lateral rectus muscle cross sections in esotropia were up to 28% larger but only significantly larger in one plane (P <0.02). Medial rectus contractility was increased by up to 60% in esotropic patients (P <0.005), whereas lateral rectus contractility in esotropia was slightly but not significantly supernormal.
Medial rectus muscle size is supernormal and lateral rectus muscle size is not subnormal in concomitant esotropia. This finding indicates that human concomitant esotropia is associated with peripheral muscular abnormality.
PMCID: PMC3976672  PMID: 23352382
8.  Long-Term Follow-up of Strabismus Surgery in Patients With Ocular Myasthenia Gravis 
To report the long-term postoperative results of strabismus surgery in patients diagnosed with ocular myasthenia gravis (OMG).
Retrospective observational case series
The medical records of all patients with OMG who underwent strabismus surgery with at least 6 months of post-operative follow-up were reviewed. Nine patients met the study inclusion criteria. Main outcomes, including ocular alignment, number of surgeries, and sensory status were evaluated.
Of these patients, initially two had horizontal strabismus alone, three had vertical strabismus alone, three had both vertical and horizontal strabismus, and one patient had vertical and torsional strabismus. Length of pre-operative stability was 2.0 ± 2.5 years (range: 0.1–8.0 years). Mean preoperative horizontal and vertical deviations were 40.5 ± 32.5 prism diopters (PD) (range: 0–90 PD) and 25.6 ± 36.7 PD (range: 0–120 PD), respectively. Average length of follow-up after the first surgery was 5.7 ± 4.2 years (range: 0.7–10.6 years). Four patients (44%) underwent two operations. For patients requiring a second operation, time to second operation was 2.3 years (range: 0.4–5.0 years). Six patients(67%) were within 10 PD of orthotropia at distance in primary position at the final visit. Five patients (55%) had single vision after their surgeries.
Strabismus surgery can achieve good long-term binocular alignment in patients with ocular MG.
PMCID: PMC3607423  PMID: 23403387
myasthenia gravis; strabismus; adjustable; diplopia; stability
9.  Medial Rectus Recession Is as Effective as Lateral Rectus Resection in Divergence Paralysis Esotropia 
Archives of ophthalmology  2012;130(10):1280-1284.
To propose medial rectus (MR) recession to be equally as effective as lateral rectus (LR) resection, which has heretofore been the preferred treatment for divergence paralysis esotropia (DPE).
We examined a 17-year surgical experience comparing LR resection with MR recession in adults with DPE, defined as symptomatic distance esotropia (ET) at least double the asymptomatic ET of 10 or less prism diopters (Δ) at near.
Twenty-four patients with DPE underwent surgery. Six patients underwent bilateral LR resection and 2 underwent unilateral LR resection (group L), while 13 underwent bilateral MR recession and 3 underwent unilateral MR recession, with the target angle double the distance ET (group M). One of 8 patients in group L and 15 of 16 patients in group M underwent intraoperative adjustable surgery under topical anesthesia. Mean (SD) preoperative central gaze ET measured 15.0 (7.7) Δ at distance and 4.1 (3.4) Δ at near in group L, but 10.4 (6.8) Δ at distance and 0.6 (1.7) Δ at near in group M (P=.15; distance, 0.003, near). Postoperatively, no patient in either group had symptomatic diplopia or convergence insufficiency in follow-up from 8.5 to 40 months. Twice the usual surgical dose of MR recession per prism diopter was required to achieve correction of the distance deviation in DPE as compared with that recommended for ET generally and also for LR resection in the same condition.
Recession of the MR provides binocular single vision in DPE without convergence insufficiency at near, and it is convenient for intraoperative adjustment under topical anesthesia.
PMCID: PMC3608524  PMID: 22688183
10.  Nonclassical Innervation Patterns In Mammalian Extraocular Muscles 
Current eye research  2012;37(9):761-769.
The abducens (CN6) and oculomotor (CN3) nerves (nn) enter target extraocular muscles (EOMs) via their global surfaces; the trochlear (CN4) nerve enters the superior oblique (SO) muscle on its orbital surface. Motor nn are classically described as entering the EOMs in their middle thirds. We investigated EOM innervation that does not follow the classic pattern.
Intact, whole orbits of two humans and one each monkey, cow, and rabbit were paraffin embedded, serially sectioned in coronal plane, and prepared with Masson’s trichrome and by choline acetyltransferase (ChAT) immunohistochemistry. Nerves innervating EOMs were traced from the orbital apex toward the scleral insertion, and some were reconstructed in three dimensions.
Classical motor nn positive for ChAT entered rectus and SO EOMs and coursed anteriorly, without usually exhibiting recurrent branches. In every orbit, nonclassical (NC) nn entered each EOM well posterior to classical motor nn. These NC nn entered and arborized in the posterior EOMs, mainly within the orbital layer (OL), but often traveled into the global layer or entered an adjacent EOM. Other NC nn originated in the orbital apex and entered each EOM through its orbital surface, ultimately anastomosing with classical motor nn. Mixed sensory and motor nn interconnected EOM spindles.
EOMs exhibit a previously undescribed pattern of NC innervation originating in the proximal orbit that partially joins branches of the classical motor nn. This NC innervation appears preferential for the OL, and may have mixed supplemental motor and/or proprioceptive functions, perhaps depending upon species. The origin of the NC innervation is currently unknown.
PMCID: PMC3608520  PMID: 22559851
cranial nerve; eye movement; extra-ocular muscle; spindle
11.  Independent Passive Mechanical Behavior of Bovine Extraocular Muscle Compartments 
Intramuscular innervation of horizontal rectus extraocular muscles (EOMs) is segregated into superior and inferior (transverse) compartments, while all EOMs are also divided into global (GL) and orbital (OL) layers with scleral and pulley insertions, respectively. We sought evidence of potential independent action by examining passive mechanical coupling between EOM compartments.
Putative compartments of each of the six whole bovine anatomical EOMs were separately clamped to a physiologically controlled, dual channel microtensile load cell (5-mN force resolution) driven by independent, high-speed, linear motors having 20-nm position resolution. One channel at a time was extended or retracted by 3 to 5 mm, with the other channel stationary. Fiducials distributed on the EOM global surface enabled optical tracking of local deformation. Loading rates of 5 to 100 mm/sec were applied to explore speeds from slow vergence to saccades. Control loadings employed transversely loaded EOM and isotropic latex.
All EOM bellies and tendons exhibited substantial compartmental independence when loaded in the physiologic direction, both between OL and GL, and for arbitrary transverse parsings of EOM width ranging from 60%:40% to 80%:20%. Intercompartmental force coupling in the physiologic direction was less than or equal to 10% in all six EOMS even for saccadic loading rates. Coupling was much higher for nonphysiologic transverse EOM loading and isotropic latex. Optical tracking demonstrated independent strain distribution between EOM compartments.
Substantial mechanical independence exists among physiologically loaded fiber bundles in bovine EOMs and tendons, providing biomechanical support for the proposal that differential compartmental function in horizontal rectus EOMs contributes to novel torsional and vertical actions.
Dual-channel tensile loading demonstrates that adjacent extraocular muscle (EOMs) regions have marked mechanical independence. This finding supports the active pulley hypothesis and the proposal that topographic innervation within horizontal rectus EOMs could command torsional and vertical actions.
PMCID: PMC4113332  PMID: 23188730
12.  High-Resolution Magnetic Resonance Imaging of the Extraocular Muscles and Nerves Demonstrates Various Etiologies of Third Nerve Palsy 
American journal of ophthalmology  2006;143(2):280-287.
The etiology of third nerve palsy is usually diagnosed by history, motility examination, and presence of lid and pupil involvement, as well as cranial and vascular imaging. We used high-resolution magnetic resonance imaging (hrMRI) of the oculomotor nerve and affected extraocular muscles (EOMs) to investigate oculomotor palsy.
Prospective, noncomparative, observational case series in an academic referral setting.
Twelve patients with non-aneurysmal oculomotor palsy of duration 0.75 to 252 months were studied. In the orbit and along the intracranial oculomotor nerve, hrMRI at 1–2mm thickness was performed. Coronal plane images of each orbit were obtained in multiple, controlled gaze positions. Structural abnormalities of the oculomotor nerve and associated changes in EOM volume and contractility were evaluated.
Cases were categorized as tumor-related, congenital, diabetic, traumatic, and idiopathic according to clinical characteristics and hrMRI findings. Reduction of volume and contractility of affected EOMs were noted in six patients; however, there was no significant EOMs atrophy in two cases with diabetic oculomotor palsy, and four cases with aberrant regeneration. hrMRI demonstrated the oculomotor nerve at the midbrain and at EOMs in all cases, and in two case with previous normal neuroimaging elsewhere demonstrated contrast-enhancing tumors on the oculomotor nerve. One patient with apparently unilateral congenital inferior division oculomotor palsy had no detectable ipsilateral and a hypoplastic contralateral oculomotor nerve exiting the midbrain.
hrMRI provides valuable information in patients with oculomotor palsy, such as structural abnormalities of the orbit and oculomotor nerve, and atrophy and diminished contractility of innervated EOMs. This information could be helpful in diagnosis and management of oculomotor palsy.
PMCID: PMC1850712  PMID: 17173848
13.  Functional Morphometry of Horizontal Rectus Extraocular Muscles during Horizontal Ocular Duction 
We explored multiple quantitative measures of horizontal rectus extraocular muscle (EOM) morphology to determine the magnetic resonance imaging (MRI) measure best correlating with duction and thus contractility.
Surface coil coronal MRI was obtained in target-controlled central gaze and multiple positions of adduction and abduction in 26 orbits of 15 normal volunteers. Duction angles were determined by position changes of the globe-optic nerve junction. Cross-sectional areas, partial volumes, and location of peak cross-sections of the horizontal rectus EOMs were computed in contiguous image planes 2-mm thick spanning the EOM origins to the globe equator.
All measures correlated significantly with duction angle (P < 0.0001). The best measures obtainable in single image planes were the maximum change in the cross-sectional area between equivalent image planes, with coefficients of determination R2 = 0.92 for medial rectus (MR) and 0.91 for lateral rectus (LR), and percentage change in maximum cross-section with R2 = 0.79 for MR and 0.78 for LR. The best partial volume measure of contractility was the change in partial volumes in four contiguous posterior planes (R2 = 0.86 MR and for 0.89 LR), particularly when combined with the corresponding change in partial volume for the antagonist EOM (R2 = 0.95 for MR and LR).
EOM morphologic changes are highly correlated with degrees of duction and thus contractility. Both changes in single-plane maximum cross-sectional areas and posterior partial volumes provide accurate, quantitative measures of EOM contractility.
Magnetic resonance morphometry of horizontal rectus extraocular muscles is highly correlated with duction angle in normal subjects, suggesting that local volume and cross-section muscle features reflect contractile state.
PMCID: PMC3481603  PMID: 22997285
14.  Determination of Poisson Ratio of Bovine Extraocular Muscle by Computed X-Ray Tomography 
BioMed Research International  2012;2013:197479.
The Poisson ratio (PR) is a fundamental mechanical parameter that approximates the ratio of relative change in cross sectional area to tensile elongation. However, the PR of extraocular muscle (EOM) is almost never measured because of experimental constraints. The problem was overcome by determining changes in EOM dimensions using computed X-ray tomography (CT) at microscopic resolution during tensile elongation to determine transverse strain indicated by the change in cross-section. Fresh bovine EOM specimens were prepared. Specimens were clamped in a tensile fixture within a CT scanner (SkyScan, Belgium) with temperature and humidity control and stretched up to 35% of initial length. Sets of 500–800 contiguous CT images were obtained at 10-micron resolution before and after tensile loading. Digital 3D models were then built and discretized into 6–8-micron-thick elements. Changes in longitudinal thickness of each microscopic element were determined to calculate strain. Green's theorem was used to calculate areal strain in transverse directions orthogonal to the stretching direction. The mean PR from discretized 3D models for every microscopic element in 14 EOM specimens averaged 0.457 ± 0.004 (SD). The measured PR of bovine EOM is thus near the limit of incompressibility.
PMCID: PMC3591112  PMID: 23484091
15.  Non-aneurysmal Cranial Nerve Compression As Cause of Neuropathic Strabismus: Evidence from High-resolution Magnetic Resonance Imaging 
American journal of ophthalmology  2011;152(6):1067-1073.e2.
To seek evidence of neurovascular compression of motor cranial nerve (CN) in otherwise idiopathic neuropathic strabismus using high resolution magnetic resonance imaging (MRI).
Prospective, observational case series.
High-resolution, surface coil orbital MRI was performed in 10 strabismic patients with idiopathic oculomotor (CN3) or abducens (CN6) palsy. Relationships between CNs and intracranial arteries were demonstrated by 0.8 mm thick, 162 micron resolution, heavily T2 weighted MRI in fast imaging employing steady state acquisition sequence. Images were digitally analyzed to evaluate cross-sectional areas of extraocular muscles.
In one patient with CN3 palsy, an ectatic posterior communicating artery markedly flattened and thinned the ipsilateral subarachnoid CN3. Cross-sections of the affected medial, superior and inferior rectus muscles 10 mm posterior to the globe-optic nerve junction were 17.2 ±2. 5 mm2, 15.5 ± 1.3 mm2, and 9.9 ± 0.8 mm2, significantly smaller than the values of 23.6 ± 1.9, 30.4 ± 4.1, 28.8 ± 4.6 mm2 of the unaffected side (P < 0.001). In two patients with otherwise unexplained CN6 palsy, ectatic basilar arteries contacted CN6. Mean cross-sections of affected lateral rectus muscles were 24.0 ± 2.3 and 29.8 ± 3.1 mm2, significantly smaller than the values of 33.5 ± 4.1 mm2 and 36.9 ± 1.6 mm2 in unaffected contralateral eyes (P < 0.05).
Non-aneurysmal motor CN compression should be considered as a cause of CN3 and CN6 paresis with neurogenic muscle atrophy, when MRI demonstrates vascular distortion of the involved CN. Demonstration of a benign vascular etiology can terminate continuing diagnostic investigations and expedite rational management of the strabismus.
PMCID: PMC3223327  PMID: 21861970
16.  Differential Lateral Rectus Compartmental Contraction during Ocular Counter-Rolling 
The lateral rectus (LR) and medial rectus (MR) extraocular muscles (EOMs) have largely nonoverlapping superior and inferior innervation territories, suggesting functional compartmental specialization. We used magnetic resonance imaging (MRI) in humans to investigate differential compartmental activity in the rectus EOMs during head tilt, which evokes ocular counter-rolling, a torsional vestibulo-ocular reflex (VOR).
MRI in quasi-coronal planes was analyzed during target-controlled central gaze in 90° right and left head tilts in 12 normal adults. Cross sections and posterior partial volumes of the transverse portions of the four rectus EOMs were compared in contiguous image planes 2 mm thick spanning the orbit from origins to globe equator, and used as indicators of contractility.
Horizontal rectus EOMs had significantly greater posterior volumes and maximum cross sections in their inferior compartments (P < 10−8). In orbit tilt up (extorted) compared with orbit tilt down (intorted) head tilts, contractile changes in LR maximum cross section (P < 0.0001) and posterior partial volume (P < 0.05) were significantly greater in the inferior but not in the superior compartment. These changes were not explainable by horizontal or vertical eye position changes. A weaker compartmental effect was suggested for MR. The vertical rectus EOMs did not exhibit significant compartmental contractile changes during head tilt. Mechanical modeling suggests that differential LR contraction may contribute to physiological cyclovertical effects.
Selective activation of the two LR, and possibly MR, compartments correlates with newly recognized segregation of intramuscular innervation into distinct compartments, and probably contributes to noncommutative torsion during the VOR.
Magnetic resonance imaging of extraocular muscles during ocular counter-rolling demonstrates selective activation of the lateral rectus inferior but not superior compartment. This is novel functional evidence that differential rectus compartmental activation contributes to a vestibulo-ocular reflex.
PMCID: PMC3367472  PMID: 22427572
17.  Adjustable Augmented Rectus Muscle Transposition Surgery with or Without Ciliary Vessel Sparing for Abduction Deficiencies 
Strabismus  2014;22(2):74-80.
Vertical rectus transposition (VRT) is useful in abduction deficiencies. Posterior fixation sutures enhance the effect of VRT, but usually preclude the use of adjustable sutures. Augmentation of VRT by resection of the transposed muscles allows for an adjustable technique that can reduce induced vertical deviations and overcorrections.
We retrospectively reviewed the records of all patients undergoing adjustable partial or full tendon VRT augmented by resection of the transposed muscles. Ciliary vessels were preserved in most of the patients by either splitting the transposed muscle or by dragging the transposed muscle without disrupting the muscle insertion.
Seven patients with abducens palsy and one with esotropic Duane syndrome were included. Both vertical rectus muscles were symmetrically resected by 3–5 mm. Preoperative central gaze esotropia of 30.6 ± 12.9Δ (range, 17–50Δ) decreased to 10.6 ± 8.8Δ (range, 0–25Δ) at the final visit (p = 0.003). Three patients required postoperative adjustment by recession of one of the transposed muscles due to an induced vertical deviation (mean 9.3Δ reduced to 0Δ), coupled with overcorrection (mean exotropia 11.3Δ reduced to 0 in two patients and exophoria 2Δ in one patient). At the final follow-up visit 3.8 ± 2.6 months postoperatively, one patient had a vertical deviation <4Δ, and none had overcorrection or anterior segment ischemia. Three patients required further surgery for recurrent esotropia.
Augmentation of VRT by resection of the transposed muscles can be performed with adjustable sutures and vessel-sparing technique. This allows for postoperative control of overcorrections and induced vertical deviations as well as less risk of anterior segment ischemia.
PMCID: PMC4100592  PMID: 24738948
Adjustable; augmented; esotropia; transposition; vessel-sparing
18.  Expanding Repertoire In The Oculomotor Periphery: Selective Compartmental Function In Rectus Extraocular Muscles 
Since connective tissue pulleys implement Listing's law by systematically changing rectus extraocular muscle (EOM) pulling directions, non-Listing's law gaze-dependence of the vestibulo-ocular reflex is currently inexplicable. Differential activation of compartments within rectus EOMs may endow the ocular motor system with more behavioral diversity than previously supposed. Innervation to horizontal, but not vertical, rectus EOMs of mammals is segregated into superior and inferior compartments. Magnetic resonance imaging in normal subjects demonstrates contractile changes in the lateral rectus (LR) inferior, but not superior, compartment during ocular counter-rolling (OCR) induced by head tilt. In human orbits ipsilesional to unilateral superior oblique palsy, neither LR compartment exhibits contractile change during head tilt, although the inferior compartment contracts normally in contralesional orbits. This suggests that differential compartmental LR contraction assists normal OCR. Computational simulation suggests that differential compartmental action in horizontal rectus EOMs could achieve more force than required by vertical fusional vergence.
PMCID: PMC3286355  PMID: 21950970
extraocular muscles; magnetic resonance imaging; motor nerve; pulleys; vestibulo-ocular reflex
19.  Enhanced Vertical Rectus Contractility by Magnetic Resonance Imaging in Superior Oblique Palsy 
Archives of Ophthalmology  2011;129(7):904-908.
To seek evidence for causative secondary changes in extraocular muscle volume, cross-sectional area, and contractility in superior oblique (SO) palsy using magnetic resonance imaging, given that vertical deviations in SO palsy greatly exceed those explained by loss of SO vertical action alone.
High-resolution, quasi-coronal orbital magnetic resonance images in target-controlled central gaze, supraduction, and infraduction were obtained in 12 patients with chronic unilateral SO palsy and 36 age-matched healthy volunteers using an 8-cm field of view and 2-mm slice thickness. Digital image analysis was used to quantify rectus extraocular muscle and SO cross-sectional areas and volumes. Measurements were compared with those of controls in central gaze to detect hypertrophy or atrophy and during vertical gaze changes to detect excess contractility.
In central gaze, the paretic SO was significantly atrophic (P<.001) and the contralesional superior rectus (SR) was significantly hypertrophic (P=.02). Across the range of vertical duction from supraduction to infraduction, both the contralesional SR (P=.04) and inferior rectus (P=.001) exhibited significantly supernormal contractile changes in maximum cross-sectional area. Contractile changes in the ipsilesional SR and inferior rectus exhibited a similar but insignificant trend (.08
Central gaze hypertrophy of the contralesional SR may be secondary to chronic excess innervation to compensate for relative hypotropia of this eye. Supernormal contralesional SR and inferior rectus contractility suggests that dynamic patterns of abnormal innervation to vertical rectus extraocular muscles may contribute to large hypertropias often observed in SO palsy.
PMCID: PMC3286651  PMID: 21746981
Nanoindentation by magnetic microspheres imaged by optical interferometry permits determination of the viscoelastic properties of fine local regions of each layer of the cornea. This approach provides robust biomechanical data on corneal creep behavior that scales reliably with the magnitude of applied force throughout the tissue.
A novel nanoindentation technique was used to biomechanically characterize each of three main layers of the cornea by using Hertzian viscoelastic formulation of creep, the deformation resulting from sustained-force application.
The nanoindentation method known as mechanical interferometry imaging (MII) with <1-nm displacement precision was used to observe indentation of bovine corneal epithelium, endothelium, and stroma by a spherical ferrous probe in a calibrated magnetic field. For each specimen, creep testing was performed using two different forces for 200 seconds. Measurements for single force were used to build a quantitative Hertzian model that was then used to predict creep behavior for another imposed force.
For all three layers, displacement measurements were highly repeatable and were well predicted by Hertzian models. Although short- and long-term stiffnesses of the endothelium were highest of the three layers at 339.2 and 20.2 kPa, respectively, both stromal stiffnesses were lowest at 100.4 and 3.6 kPa, respectively. Stiffnesses for the epithelium were intermediate at 264.6 and 12.2 kPa, respectively.
Precise, repeatable measurements of corneal creep behavior can be conveniently obtained using MII at mechanical scale as small as one cell thickness. When interpreted in analytical context of Hertzian viscoelasticity, MII technique proved to be a powerful tool for biomechanical characterization of time-dependent biomechanics of corneal regions.
PMCID: PMC3388749  PMID: 21969299
Rectus muscle plication is an alternative muscle-strengthening procedure to rectus muscle resection. Possible advantages of rectus muscle plication include a lower risk of “lost” muscles and anterior segment ischemia.
This was a retrospective case series describing a surgical procedure for rectus muscle plication using an adjustable suture technique that can be employed on any of the four rectus muscles.
A total of 5 adult patients underwent adjustable suture plication procedures. Of these, 2 patients required suture adjustment postoperatively. At the final follow-up visit, all of the patients maintained satisfactory ocular alignment within 6Δ of orthotropia for horizontal deviations and 2Δ of orthotropia for vertical deviations. Diplopia was eliminated in all cases with preoperative diplopia. There were no postoperative complications or unexpected shifts in ocular alignment.
Rectus muscle plication using this adjustable suture technique may serve as an alternative to rectus muscle resection and may be particularly useful in patients who are at risk for anterior segment ischemia or those in whom a shorter anesthesia time is recommended.
PMCID: PMC3814036  PMID: 24160967
Magnetic resonance imaging (MRI) can provide unique information about extraocular muscle (EOM) structure and function. Prior high-resolution motility imaging studies employed T1 weighting, which provides intrinsic contrast of dark-appearing EOMs against bright orbital fat and is suitable for intravenous contrast. However, time-consuming T1 sequences are subject to motion artifacts. We evaluated an alternative T2-weighted fast spin-echo pulse sequence that emphasizes tissue-free fluid.
We prospectively used high resolution, surface coil technique for orbital MRI at 1.5T in 21 normal and 113 living strabismic subjects and 2 monkey cadavers using T2 fast spin-echo (T2FSE) weighting (long repetition time, short echo time). T2FSE was compared with T1 in 17 subjects, and with T1 in 506 different living subjects, and 12 cadavers.
For 2 mm thick coronal MRIs of 312 μm resolution spanning the entire orbit, T1 acquisition required 218 seconds, whereas T2FSE required 150 seconds (31% faster). T2-defined the globe border better, and provided intrinsic contrast between EOMs and their pulleys. While both T1 and T2 demonstrated motor nerves to EOMs in living subjects, only T1 was satisfactory with injected contrast and in cadavers.
For motility imaging, T2FSE is faster than T1 MRI and demonstrates superior tissue details of EOMs and other orbital tissues. T2FSE of the orbits can be performed using widely available standard equipment. We suggest that T2FSE be the preferred method for clinical imaging of EOM structure, function, and innervation, although T1 may be more appropriate when intravenous contrast must be employed.
PMCID: PMC3057399  PMID: 21397801
American journal of ophthalmology  2010;150(6):925-931.e2.
To determine by magnetic resonance imaging (MRI) the prevalence and anatomy of anomalous EOM bands.
Prospective, observational case series.
High resolution, multi-positional, surface coil orbital MRI was performed using T1 or T2 fast spin echo weighting with target fixation control under a prospective protocol in normal adult subjects and a diverse group of strabismic patients between 1996 and 2009. Images demonstrating anomalous EOM bands were analyzed digitally to evaluate their sizes and paths, correlating findings with complete ophthalmic and motility examinations.
Among 118 orthotropic and 453 strabismic subjects, one (0.8%) orthotropic and 11 (2.4%) strabismic subjects exhibited unilateral or bilateral orbital bands having MRI signal characteristics identical to EOM. Most bands occurred without other EOM dysplasia and coursed in the retrobulbar space between rectus EOMs such as medial (MR) to lateral rectus (LR), or superior (SR) to inferior rectus (IR), or from one EOM to the globe. In two cases, horizontal bands from MR to LR immediately posterior to the globe apparently limited supraduction by collision with the optic nerve. All bands were too deep to be approached via conventional strabismus surgical approaches.
About 2% of humans exhibit on MRI deep orbital bands consistent with supernumerary EOMs. While band anatomy is non-oculorotary, some bands may cause restrictive strabismus.
PMCID: PMC2991531  PMID: 20801423
This paper characterized bovine extraocular muscles (EOMs) using creep, which represents long-term stretching induced by a constant force. After preliminary optimization of testing conditions, 20 fresh EOM samples were subjected to four different loading rates of 1.67, 3.33, 8.33, and 16.67%/s, after which creep was observed for 1,500 s. A published quasilinear viscoelastic (QLV) relaxation function was transformed to a creep function that was compared with data. Repeatable creep was observed for each loading rate and was similar among all six anatomical EOMs. The mean creep coefficient after 1,500 seconds for a wide range of initial loading rates was at 1.37 ± 0.03 (standard deviation, SD). The creep function derived from the relaxation-based QLV model agreed with observed creep to within 2.7% following 16.67%/s ramp loading. Measured creep agrees closely with a derived QLV model of EOM relaxation, validating a previous QLV model for characterization of EOM biomechanics.
PMCID: PMC3216464  PMID: 22131809
High-resolution MRI shows heterogeneous extraocular muscle features in strabismus, typical of superior oblique palsy. Rectus pulley counterrotations in response to head tilt may be paradoxical and depend on the presence of superior oblique atrophy, which is detected in half of patients.
Although alteration in hypertropia induced by head tilt is considered a clinical criterion for diagnosis of superior oblique (SO) palsy, the mechanism of this head-tilt–dependent hypertropia (HTDHT) is unclear. In this study, magnetic resonance imaging (MRI) was used to study extraocular muscle (EOM) responses to head tilt in HTDHT.
Orbital MRI was used to study 16 normal subjects and 22 subjects with HTDT, of whom 12 had unilateral SO atrophy and 10 had “masquerading” SO palsy with normal SO size. Sizes and paths of all EOMs were compared in 90° roll tilts.
Normal subjects exhibited the expected 3° to 7° physiologic extorsion of all four rectus pulleys in the orbit up-versus-down roll positions, corresponding to ocular counterrolling. In orbits with SO atrophy, the lateral (LR) and inferior rectus (IR) pulleys paradoxically intorted by approximately 2°. Subjects with HTDHT but normal SO size exhibited reduced or reversed extorsion of the medial, superior, and LR pulleys, whereas pulley shift was normal in nonhypertropic fellow orbits in HTDHT. In normal subjects and in SO atrophy, the inferior oblique (IO) muscle contracted in the orbit up-versus-down roll position, but paradoxically relaxed in HTDHT without SO atrophy.
The ipsilesional IR and LR pulleys shift abnormally during head tilt in HTDHT with SO atrophy. In HTDHT without SO atrophy, the ipsilesional MR, SO, and LR pulleys shift abnormally, and the IO relaxes paradoxically during head tilt. These widespread alterations in EOM pulling directions suggest that complex neural adjustments to the otolith–ocular reflexes mediate HTDHT.
PMCID: PMC3109014  PMID: 21282574

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