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High-Resolution Magnetic Resonance Imaging Demonstrates Varied Anatomic Abnormalities in Brown Syndrome
High-Resolution Magnetic Resonance Imaging Demonstrates Varied Anatomic Abnormalities in Brown Syndrome Rahul Bhola, MD,a Arthur L. Rosenbaum, MD,a Maria C. Ortube, MD,a and Joseph L. Demer, MD, PhDa,b Inroduction: Although Brown syndrome classically is considered to be limited to the SO tendon sheath and trochlea, it does not always respond to SO surgery. We investigated mechanisms of Brown syndrome by magnetic resonance imaging (MRI). Methods: Three patients with congenital and 8 with acquired Brown syndrome were compared with matched normal subjects under a prospective protocol of high-resolution, multipositional orbital MRI using surface coils. Muscle size and contractility were determined using digital image analysis. Results: Five of 8 patients with acquired Brown syndrome had a history of trauma or surgery and demonstrated extensive scarring, avulsion, or fracture of the trochlea. One of the 8 had a cyst in the SO tendon. One congenital and one acquired case demonstrated inferior displacement of the lateral rectus (LR) pulley in adduction, with a normal SO tendon–trochlear complex. Such cases of Brown syndrome responded to surgical stabilization of the LR pulley. Two congenital cases had clinical findings of ipsilateral SO palsy confirmed on MRI by atrophy or absence of the SO belly. In congenital absence of the SO belly, the anterior tendon was present but terminated directly on the trochlea. Conclusion: High-resolution MRI demonstrates a variety of abnormalities in patients presenting with Brown syndrome, including atrophy or absence of the SO belly. Management in Brown syndrome should be tailored to the pathophysiology of the individual patient. (J AAPOS 2005;9:438-448) rown syndrome was first characterized in 1950 by Harold Whaley Brown as a restrictive limitation to elevation in adduction.1 On the basis of surgical findings, Brown implicated a short SO tendon sheath as the cause of this syndrome. Most subsequent reports have alternatively proposed an abnormality in the trochlear–SO tendon complex as the cause of restriction to elevation in adduction. Although SO surgery, including tenotomy, recession, or lengthening by a variety of techniques, has been used principally as surgical treatment for moderate-to-severe Brown syndrome, in our experience, not all patients respond to this surgery. Such surgical failures suggest other
B
a
From the Jules Stein Eye Institute, University of California, Los Angeles and the Department of Neurology, University of California, Los Angeles, California Presented at the 30th annual meeting of the American Association for Pediatric Ophthalmology and Strabismus, Washington, DC, March 27-31, 2004. Supported by USPHS NIH EY08313 & Research to Prevent Blindness. J.L.D. received an unrestricted award from Research to Prevent Blindness and is the Leonard Apt Professor of Ophthalmology at UCLA. A.L.R. is a recipient of a Research to Prevent Blindness Physician-Scientist Merit Award. Submitted March 9, 2004. Revision accepted June 17, 2005. Reprint requests: Joseph L. Demer MD, PhD, Jules Stein Eye Institute, 100 Stein Plaza, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-7002 (e-mail: [email protected]). Copyright © 2005 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2005/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2005.07.001 b
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mechanisms for Brown syndrome besides pathology of the SO tendon and trochlea. Knowledge of orbital and extraocular muscle (EOM) anatomy has progressed since the time of Harold Brown. Motivated by efforts to develop computer simulations of EOM behavior to guide strabismus surgery, researchers recently have conducted anatomical re-examinations of orbital anatomy using immunohistochemistry of serially sectioned orbits,2-4 computer reconstructions in virtual reality,5 and multipositional magnetic resonance imaging (MRI) with spatial resolution enhanced by use of surface coils6,7 and tissue resolution enhanced with paramagnetic contrast8 to study the functional anatomy of the EOMs.7,9-12 From these investigations has emerged a detailed picture of the vital role of EOM paths in determination of EOM function.13In brief, the action exerted by any EOM on the globe is determined not only by the magnitude of tension it exerts but also on the pulling direction of that tension. For any EOM, pulling direction is determined by its scleral insertion and the location of its functional origin. The functional origin of each EOM is at a connective tissue structure called a pulley. Harold Brown recognized the importance of the SO pulley—the classic trochlea—to SO function. We now know that all of the other EOMs have less rigid, but still essential, pulleys.3-5,8 The pathology of these pulleys causes incomitant strabismus that can clinically simulate oblique EOM dysfunction. For example, instability of the LR pulley has been demJournal of AAPOS
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onstrated by multipositional MRI to simulate Brown syndrome.14 It was observed that the instability of the pulleys was accentuated in particular gazes and was responsible for the incomitance of the deviation. Although clinical tests like alignment measurements, forced duction, forced generation, and saccadic velocity testing may be helpful in evaluating Brown syndrome, they may not define the pathophysiology accurately. Multipositional MRI can provide valuable additional clinical information to demonstrate a variety of different anatomical mechanisms in patients presenting clinically with Brown syndrome. We performed this study to explore the spectrum of clinical abnormalities in Brown syndrome.
MATERIALS AND METHODS Participating patients were selected from an ongoing, prospective study of orbital imaging in strabismic patients. Eleven consecutive cases of unilateral Brown syndrome were identified based on clinical findings, including 3 patients with congenital and 8 patients with acquired disorders. All the patients complained of constant or intermittent vertical diplopia and had limitation to elevation in adduction in one eye. A complete ophthalmic evaluation, including a detailed ocular motility examination, was performed in all the cases. Binocular alignment was measured using prism and alternate cover test both for distance and near in the cardinal gaze directions and with head tilt to each side, and with the Hess screen test in 21 fixation positions over a 30 degree field for each eye. Ductions and versions were quantified using a 9-point scale, with 0 suggesting a normal movement, – 4 signifying an inability to move the eye past midline, and ⫹4 signifying maximum observable overrotation. After obtaining written informed consent according to a protocol confirming to the Declaration of Helsinki and approved by the Institutional Review Board, each subject underwent multipositional high-resolution T1-weighted MRI with a 1.5-T General Electric Signa (Milwaukee, WI) scanner using methods previously described in detail.6,7 Depending on the clinical indication, T2 imaging was used occasionally in addition. Each subject’s head was carefully stabilized in a supine position with the nose aligned to the longitudinal and the pupils to the transverse light projection references of the scanner. Imaging of the orbits was performed in multiple gaze positions using a phased array of 4 surface coils deployed in a mask-like enclosure held strapped to the face. An adjustable array of monocular, afocal, illuminated fixation targets at 9 diagnostic positions of gaze was secured in front of each orbit with the center target in subjective central position for each eye. Head movement of the subjects was minimized by secure stabilization to the surface coil facemask and judicious use of padded restraints. Multiple contiguous quasicoronal digital images of 2-mm slice thickness were then obtained using a 256 ⫻ 256 matrix over an 8-cm2 field, giving pixel resolutions of 313
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m. Imaging was then repeated in multiple gaze positions. The trochlea and reflected SO tendon also were imaged using axial image planes of the same resolution. In appropriate cases, the inferior oblique muscle was imaged in quasisagittal image planes parallel to the long axis of the orbit. Digital MRIs were transferred to Macintosh computers (Apple Computer, Cupertino, CA) and converted to 8-bit tagged image file format and were quantitatively analyzed using the program NIH Image (W. Rasband, National Institute of Health; available by ftp from zippy. nimh.nih.gov or on floppy disk from NTIS, Springfield, VA, part number PB95-500195GEI). We studied the size of the EOMs in different gaze positions of both the eyes in all subjects. Change in EOM cross section from relaxed to contracting gaze positions was used as an index of contractility. Anatomical characteristics of the SO muscle and tendon and its relationship with the trochlea was evaluated in multiple gaze positions where clinically appropriate. Subject data were compared with the existing data of the normal rectus pulley positions relative to the globe center as determined by Clark et al15 in 22 orbits of 11 normal adults using the same NIH Image program and a similar prospective protocol of high-resolution, multipositional orbital MRI using surface coils.
RESULTS Twenty-two orbits of 11 subjects with Brown syndrome were analyzed. Clinical information of the subjects is summarized in Table 1. According to the anatomic abnormalities as elicited by MRI, 4 distinct mechanisms of Brown syndrome were identified: (1) trochlear damage; (2) SO tendon abnormalities; (3) abnormalities of rectus EOM pulleys; and (4) congenital abnormalities of SO muscle. Cases were segregated by mechanism. Trochlear Damage Case 1. This 17-year-old boy presented with a history of vertical binocular diplopia in upgaze after a bilateral frontal sinus surgery for bacterial sinusitis 3 months before his presentation. Uncorrected visual acuity was 20/15 in each eye. External examination was notable for healed Lynch incisions bilaterally (Figure 1) with a palpable scar web over the region of the left trochlea but without trochlear tenderness. There was marked limitation to supraduction of the right eye in adduction (Figure 1). The patient was orthotropic in all diagnostic fields, including head tilt, with the exception of upgaze, in which there was a large right hypotropia. High-resolution multipositional MRI revealed an extensive scarring in the region of both trochleas. Imaging with contrast demonstrated continuity of a cicatrix from the right frontoethmoidal sinus region through the trochlea entering the SO tendon (Figure 2). Case 2. This 36-year-old woman presented with a history of vertical binocular diplopia in up gaze, subsequent to a trauma on the left orbit from a softball. She
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440 Bhola et al TABLE 1 Clinical profile of patients Subject
Age(years)/sex
Onset
Central gaze deviation
1. 2. 3.
17/M 36/F 7/M
Acquired: frontal sinus surgery Acquired: trauma Acquired: dog bite
Orthotropic 4 PD Exophoria 18 PD LHT 7° Excy. OS
4.
21/F
Acquired: automotive accident
30 PD RHT 4° Excy. OD
5. 6. 7. 8. 9. 10.
64/F 36/F 11/F 69/M 53/F 14/M
Acquired: blepheroplasty Acquired: idiopathic Congenital Acquired: idiopathic Acquired: orbital decompression Congenital
Orthotropic 3 PD RH(T) 20 PD LHoT 10 PD XT 8 PD RHT 7° Excy. OD 20 PD LHoT 10° Incyc. OS 35 PD LHT
11.
8/M
Congenital
14 PD RHT 8 PD ET
MRI findings Scarring of right trochlea from the frontal sinus Adhesion bands left trochlea, SOT thickening Disorganization of left tendon/trochlear complex with scarring Right trochlear avulsion; left trochlear disruption Possible suture in reflected SOT Cyst in SOT posterior to trochlea Left LR pulley instability Left LR pulley instability Left LR pulley instability and adhesion to orbit Hypoplastic left SOM, fibrous band from sclera to trochlea Attenuation of right SOM, fibrous band from sclera to trochlea
PD, prism diopters; RHT, right hypertropia; LHT, left hypertropia; RH(T), intermittent right hypertropia; LHoT, left hypotropia; XT, exotropia; F, female. Excy, excycotorsion. LR, lateral rectus muscle; M, male; SOM, superior oblique muscle; SOT, superior oblique tendon.
FIG 1. Versions of subject 1 in 9 diagnostic positions of gaze, demonstrating underelevation on adduction of the right eye. Note scarring from the Lynch incisions over both trochleas.
complained of left trochlear pain, trochlear tenderness, and an occasional clicking sound from the left trochlear region when looking upward. Uncorrected visual acuity was 20/20 in each eye. There was limitation to elevation of the left eye in both abduction and adduction that was worse in adduction. At distance, there was 4⌬ of exophoria in primary gaze and in right gaze. She was orthotropic in left gaze and down gaze, but in up gaze exhibited a left hypotropia of 8⌬. At near gaze she had 8⌬ exophoria. High-resolution MRI demonstrated an abnormality in the left reflected SO tendon with adhesion bands in the trochlear region. The patient was administered steroid injections in the left trochlea without resolution of her symptoms. Subsequently, a surgical exploration of the left trochlea and SO was performed, which revealed an enlargement of the left SO tendon, which was found to be folded on itself with fibrous adhesions extending back to
the trochlea. The adhesions were lysed surgically, and the left trochlea was infiltrated with long and short acting steroids. Symptoms recurred after initial improvement. SO tenotomy with a compensatory surgery on the ipsilateral IO is planned. Case 3. This 7-year-old boy developed a vertical binocular diplopia and spontaneous right head tilt after being bitten by a dog above the left eye 5 months before his presentation. The clinical and examination findings of the patient have been previously reported.16 Multipositional MRI scans of the left orbit showed marked scarring in the area of the left trochlea along with SO tendon sheath thickening. There was marked disorganization of the tendon/trochlear complex. Case 4. This 21-year-old woman developed a vertical binocular diplopia after severe head trauma in an automotive collision. Visual acuity was 20/20 with a myopic cor-
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FIG 2. Coronal T1-weighted, contrast-enhanced MRI image of the right orbit of subject 1 showing a cicatrix from the right frontoethmoidal sinus region to the trochlea Note enhancement of the sinus mucosa.
rection. There was moderate overelevation in adduction of the right eye, with marked underelevation and downshoot in adduction of the left eye (Figure 3). There was mild limitation to infraduction of the right eye, particularly in adduction. At distance, there was 30⌬ right hypertropia in primary position, decreasing in right gaze and increasing in left gaze. The deviation increased in upgaze and diminished slightly in downgaze. Forced head tilt test revealed 50⌬ of right hypertropia with right head tilt diminishing to 15⌬ in left head tilt. At near there was 25 ⌬ right hypertropia with 6⌬ exotropia. Double Maddox rod testing demonstrated 3-4o right excyclotorsion. Highresolution MRI revealed right trochlear avulsion along with disengagement of the SO tendon and a trochlear disruption in the left eye (Figure 4). The patient underwent left SO tenotomy, a 10-mm right IO recession, and a 3-mm left inferior rectus recession on adjustable suture. At 3-week postoperative follow-up, she presented with a small consecutive left hypertropia that was treated successfully with a small spectacle prism. Superior Oblique Tendon Abnormalities Case 5. This 64-year-old woman complained of vertical binocular diplopia immediately after undergoing bilateral upper eyelid blepharoplasty 9 months before. Uncorrected visual acuity was 20/20 in each eye. There was marked limitation of elevation of the left eye in adduction (Figure 5). She was orthotropic in primary position but had 25⌬ left hypotropia in upward gaze to the right. Motion of a nodule could be palpated in the region of the left trochlea during attempted up and down gaze. Forced duction testing showed marked restriction to elevation of
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the left eye in adduction. Axial (Figure 6A) and coronal (Figure 6B) MRI revealed a nodular structure in the left reflected SO tendon just lateral to the trochlea, and multiple nodular structures in the anterior superomedial right orbit. These structures demonstrated a low intensity both on T1- and T2-weighted imaging, with a high-intensity rim suggestive of suture material or cautery effect from the blepharoplasty surgery interfering with the reflected SO tendon. Case 6. This 36 year-old woman noticed progressively increasing intermittent pain over the right trochlea with intermittent vertical diplopia beginning18 months before presentation. She also noticed a palpable click in the region of the right trochlea on shift from up- to downgaze. Details of this patient have been previously described in a case report.16 MRI showed a spherical structure in the SO tendon that was presumed to be a cyst. This cystic structure was seen to change anteroposterior position with vertical gaze shifts. In supraduction, the SO tendon was passively stretched and the cyst was pulled anteriorly. In primary position the cyst was posterior and began to abut the trochlea but apparently did not enter it. In infraduction the SO muscle contracted and the cyst retracted, distant from the trochlea. The patient’s symptoms can be explained by interference of the cyst with the trochlea; the cyst must be dragged through the trochlea on excursion from down- to upgaze. This causes a temporary restriction, which gives way with a palpable click as the bulk of the cyst moves anterior to the trochlea in upgaze. The SO tendon was explored surgically. The abnormal cystic structure surrounding the tendon was excised, and the surrounding area was infiltrated with steroids. The patient was asymptomatic on the first postoperative day. Abnormalities of Rectus Extraocular Muscle Pulleys Case 7. This 11-year-old girl presented with a history of anomalous head posture, inability to elevate the left eye in adduction, and left hypotropia since the age of 3 months. Uncorrected acuity was 20/20 in each eye. The patient had a 20° right face turn with a 5° chin elevation. There was marked underelevation of the left eye in adduction and moderate elevation limitation in abduction. There was a moderate overdepression of the left eye in adduction. In forced primary position at distance there was 20⌬ left hypotropia and 10⌬ exotropia. At near there was 20⌬ left hypotropia and 16⌬ exotropia. Intraoperative forced duction testing revealed marked restriction to supraduction of the left eye in adduction. Surgical exploration showed the anatomical position, fibers and tension of the SO tendon to be normal. Left SO tenotomy with a 7-mm silicon spacer failed to immediately relieve restriction to supraduction. The spacer was replaced with a suture and the posterior end of the SO tendon was allowed to retract approximately 15 mm. Postoperative examination on the first day and 6 months later showed minimal improvement in the anomalous head posture and ocular
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FIG 3. Versions of subject 4 in 9 diagnostic positions of gaze, demonstrating severe underelevation of the left eye on adduction with moderate underelevation on abduction.
FIG 4. case 4. Top row, Coronal T1 MRI showing dislocation of the right SO tendon after avulsion of the right trochlea. Damage to the left trochlea was evident, along with medial wall blow out fractures larger on the right than left. IO, IO muscle; MR, medial rectus muscle. Bottom row, Axial T1 MRI images showing posterior displacement of the path of the right SO tendon, in relation to the normal location of the reflected left SO tendon. SR, SR muscle.
rotations, with 16⌬ left hypotropia and 8⌬ exotropia in forced primary position. High-resolution MRI at this point revealed inferior displacement of the left LR pulley, a defect that was exaggerated in adduction. There was no such abnormality demonstrated in the right orbit. In view
of the anatomical abnormality on MRI, a second surgery was performed, consisting of a left LR recession and superior insertional transposition, with posterior reteroequatorial myopexy to prevent inferior slip of the LR pulley. Intraoperative forced duction testing was immediately completely relieved of restriction. Three months postoperatively the patient had a minimal left hypotropia in primary gaze and no anomalous head posture. Case 8. This 69 year-old men presented with a 1-year history of sudden onset of vertical diplopia worse in upgaze to the right. Corrected visual acuity was 20/20 in both eyes. He had a 5° chin elevation. Cover test revealed a Y-pattern exotropia with 8⌬ right hypertropia in primary position, which increased in upgaze to 16⌬ but was generally comitant in other gaze positions. The hypertropia slightly increased on forced left head tilt. Double Maddox rod test revealed right excyclotorsion of 7°. There was limitation of supraduction of the left globe, worse in adduction. Forced duction testing revealed restriction to supraduction of the left globe, greatest in adduction. High-resolution MRI revealed no anatomic abnormality of the left SO muscle, tendon or trochlea. Instability of the left LR pulley was seen on coronal imaging, with downward shift of the left LR on adduction. Case 9. This 53-year-old woman had a 5-year history of thyroid ophthalmolopathy. Immediately after undergoing left orbital decompression via a superotemporal approach 4 months before presentation, she noticed binocular vertical diplopia with relative tilting of images, greatest in right gaze and minimized with a left head tilt and right face turn. She also felt tightness inferotemporally in the left eye socket while looking to the right. Corrected visual acuity was 20/16 in the right and 20/50 in the left eye. There was severe limitation to elevation of the left eye in adduction, but with extreme elevating effort there was a
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FIG 5. Versions of case 5 in nine diagnostic gaze positions showing underelevation of the left eye in adduction.
snap-like, sudden upward rotation of the left eye nearly normalizing supraduction in adduction (Figure 7). There was a marked overdepression of the left eye in adduction. There was no limitation to elevation of the left eye in abduction. Forced duction testing revealed a marked resistance to passive supraduction in adduction, which was suddenly relieved with a prolonged effort to look up by the patient. At distance, there was 20⌬ left hypotropia in primary gaze that diminished to 4⌬ in left gaze, and increased to 40⌬ in right gaze. The left hypotropia was 30⌬ in upward gaze and was 10⌬ in downward gaze. At near, there was 25⌬ left hypotropia with 6⌬ exotropia. There was 25⌬ left hypotropia in right head tilt diminishing to 10⌬ in left head tilt. Double Maddox rod testing demonstrated 10° left incyclotropia. High-resolution MRI revealed postsurgical cicatrisation around the left LR muscle, with apparent adhesion of the inferior pole of that EOM to the orbital wall (Figure 8). There was no abnormality of trochlea and SO on either side. Instability of the left LR pulley was suspected. This instability was confirmed by intraoperative demonstration of obvious downward slip of the LR muscle path when rotating the eye from abduction to adduction using a muscle hook engaged at the LR insertion. The LR path was stabilized by joining its superior margin to the underlying sclera using a nonabsorbable suture; the left IR muscle was recessed 3.5 mm. Six months after surgery, the patient had a marked improvement of ocular versions, and was orthotropic in primary position. The ocular torticollis was eliminated. Congenital Abnormalities of the SO Muscle Case 10. This 14-year-old boy presented with intermittent vertical diplopia that had existed since early childhood. Visual acuity in each eye was 20/20. He spontaneously adopted a 10° head tilt to the right. There was down shoot of the left eye in adduction with marked inability to elevate the left globe in adduction and reduced ability to depress the left globe in adduction. There was mild limitation to full upward rotation of the left globe in straight up position. In forced primary position, cover testing revealed 35⌬ left hypertropia that increased to 40⌬ in down gaze. The left hypertropia was reduced to 14⌬ in levover-
sion, but was 25⌬ in dextroversion. The left hypertropia was reduced in upgaze to 6⌬. Forced head tilt testing showed a left hypertropia of 25⌬ on left head tilt reducing to 6⌬ on right head tilt. The increase of left hypertropia in down gaze and left head tilt clinically suggested coexistent SO paresis. High-resolution coronal MRI suggested complete absence of the left SO muscle belly (Figure 9A). The reflected tendon of the left SO was present, but apparently terminated on the trochlea. Axial MRI showed an attenuated remnant of the left SO belly, in contrast with a normal sized right SO belly (Figure 9B). The right SO was of normal size and demonstrated robust contraction from supraduction to infraduction. Intraoperative forced duction testing revealed marked restriction to elevation of the left eye in adduction. Surgical exploration revealed a dense fibrous band that attached to the sclera at the nasal border of the left superior rectus (SR) muscle, incorporating some of its fibers. The band was traced posteriorly for a distance of 8 mm to the same area as the reflected SO tendon, but normal tendon fibers could not be visualized. After dividing this fibrous band the left IO muscle was recessed, and the left IR was resected. At the time of last follow-up, 4 years postoperatively, the patient was orthotropic in primary gaze and free of ocular torticollis. The limitation to elevation in adduction was also markedly improved. Case 11. This 8-year-old boy presented with a lifelong left head tilt. Uncorrected visual acuity was 20/30 in the right and 20/25 in the left eye. Cycloplegic refraction revealed hyperopia of ⫹ 3.50 in the right eye and ⫹ 4.25 in the left eye. On examination, there was a left head tilt of 5°. There was limitation to elevation in adduction of the right eye (Figure 10). In forced primary position, there was 14⌬ right hypertropia and 8⌬ esotropia. The right hypertropia increased to 20⌬ in downgaze, was 8⌬ in dextroversion, and 14⌬ in levoversion. There was no hypertropia in the upgaze. Esotropia was eliminated by hyperopic correction. High-resolution MRI revealed a attenuation of the right SO muscle belly (Figure 11), with size less the 95% confidence limit of normal17 with the anterior tendon terminating directly on the trochlea similar to case 10. The left SO muscle was normal in size and had normal con-
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FIG 6. Case 5. A, Axial T1 MRI showing a nodule in the reflected tendon of the left SO muscle, with irregularity around the reflected tendon. B, Coronal T2 MRI image of the left orbit the nodule in the reflected tendon of the SO muscle.
tractile thickening from supraduction to infraduction. Intraoperative forced duction testing revealed a marked restriction to elevation of the right globe in adduction. Exploration revealed a fibrous band adhesion to the sclera at the nasal border of the SR. The band appeared to be in the same area as the SO tendon, but the tendon fibers could not be visualized. This fibrous band was divided, which immediately relieved the restriction to forced duction. The left IO muscle was recessed. At the time of last follow-up 5 year, 2 month postoperatively the patient was orthophoric in primary position, and free of anomalous head posture.
DISCUSSION Multipositional, high-resolution MRI has enhanced the understanding of incomitant strabismus by revealing multiple anatomical and functional abnormalities of the ex-
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traocular muscles and their pulleys.6,7,9,10-12,16 Surgical success in incomitant strabismus often depends on pathologic mechanism, so that treatment can be directed to its correction. Brown syndrome is a narrowly defined, restrictive, incomitant strabismus whose clinical features are nevertheless nonspecific to etiology. In 1950, Brown reported 8 cases having a restrictive limitation to elevation in adduction, a condition that he called the “SO tendon sheath syndrome.”1 This restriction to elevation was believed to be caused by secondary shortening of the anterior sheath of the SO tendon from congenital palsy of the “ipsilateral IO.” Pathology of the IO muscle is no longer considered important in Brown syndrome, but numerous other etiologies have been proposed. The inconsistent response to SO relaxation and tenotomy procedures in some of these cases inspired us to study the anatomical abnormalities associated with this syndrome using a multipositonal, high-resolution MRI. We here report 11 patients with Brown syndrome and ipsilateral restrictive limitation to elevation in adduction. Despite the typical clinical features, we found four distinct abnormalities of functional anatomy. Six of the 8 acquired cases developed Brown syndrome secondary to surgical or accidental trauma. Although all these cases had a similar clinical presentation with acute onset, multipositional MRI revealed varied abnormalities. Four of these traumatic cases demonstrated trochlear damage restricting free passage of the SO tendon through the trochlea. Case 1 developed Brown syndrome after a frontal sinus surgery. Blanchard and Young in 198418 and Rosenbaum and Astle19 in 1985 reported Brown syndrome after frontal sinus surgery. Improper surgical technique, such as placement of the surgical incision too low or excessive periosteal stripping near the trochlea, can contribute to the SO damage or restriction. In addition, a cicatrisation of the SO to the globe, bone or into the sinus scar tissue defect may restrict eye movement.19 High-resolution imaging with contrast explicitly demonstrated continuity of a ci catrix from the right frontal sinus region through the trochlea entering the SO tendon in case 1, thus revealing the cause of restrictive incomitance. Direct nonsurgical trauma to the superomedial orbit can disturb the function of the SO muscle, causing the clinical appearance of SO palsy, Brown syndrome, or both.20 Restricted elevation in adduction secondary to trauma can be a manifestation of either direct injury to trochlear-SO tendon complex the result of scarring from the inflammation surrounding the SO tendon.21 Highresolution MRI can be useful in such cases to define the exact anatomical abnormality. Three of our cases developed a Brown syndrome secondary to accidental trauma and showed varied abnormalities on MRI. Case 2 showed scarring in the area of the trochlea along with tendon sheath thickening. Case 3 demonstrated abnormalities in the reflected SO tendon anterior to the trochlea, with
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FIG 7. Versions of case 9 in 9 diagnostic positions of gaze, demonstrating underelevation and downshoot of the left eye in adduction.
FIG 8. case 9. Top- Axial images of the left orbit show normal SO tendon trochlear complex. Bottom-Coronal MRI of the left orbit in central gaze showing cicatrization near the inferior pole of the LR pulley after orbital decompression surgery. The orbitotomy site is visible superolaterally in the left orbit. LR, lateral rectus muscle; SO, SO muscle.
tendon thickening and adhesions. Case 4 revealed a trochlear disruption in one eye and a trochlear avulsion in the contralateral eye, presenting clinically as Brown syndrome with contralateral SO palsy. Incarceration of the SO tendon, with fat, orbicularis, levator aponeurosis, and septum has been reported after
blepharoplasty.22 Case 5 developed vertical binocular diplopia immediately after undergoing bilateral upper eyelid blepharoplasty. High-resolution MRI scan in this patient suggested that deeply placed blepharoplasty sutures, or possibly cautery, had included the reflected SO tendon. Impediment of free movement of the SO tendon in the trochlear tendon complex has been proposed as a cause of Brown syndrome. Inflammation by such etiologies as juvenile rheumatoid arthritis, lupus, and Sjogren’s syndrome,23-26 trauma or other restrictive phenomena have been proposed to compromise function. In 1971 RoperHall27 in their series described “SO ‘click’ syndrome” presumed to be an inflammatory form of Brown syndrome. The clinical picture can alternate between Brown syndrome and SO palsy, depending on the direction in which the tendon movement through the trochlea is impeded. One of our acquired cases presented with an intermittent picture of Brown syndrome with a palpable click over the trochlear region on change from supraduction to infraduction. Although the patient had no clinical evidence of any inflammatory or autoimmune disorder, a multipositional MRI showed the location and movement of a spherical structure in the SO tendon that correlated with the patient’s symptoms. This spherical structure was surgically confirmed to be a cyst that interfered with normal transit of the SO tendon through the trochlea. An acute onset of Brown syndrome was observed in case 9 after an orbital decompression surgery for thyroid ophthalmopathy that completely avoided the trochlear region. High-resolution MRI revealed evidence of damage to the left LR pulley. This indication of LR pulley instability was confirmed intraoperatively by demonstrating the shift in LR path during passive adduction of the eye. Supraplacement and stabilization of the LR path by superior myopexy corrected the limitation to elevation of the eye in adduction.
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FIG 9. T1 MRI in case 10. A, Coronal images showing apparent absence of left SO muscle (SO) but presence of its reflected tendon inserting on the trochlea. IO, IO muscle; LPS, levator palpebrae superioris muscle; ON, optic nerve; SR, SR muscle. B, Axial images showing a normal right SO belly, trochlea, and reflected tendon, but marked attenuation of the left SO posterior to the trochlea.
One congenital (case 7) and one acquired case (case 8) demonstrated a vertical instability of the LR pulley in adduction. In both patients there was an inferior displacement of the LR pulley of the involved eye, a defect that was exaggerated in adduction. This LR side slip causes restrictive limitation to elevation in adduction. Oh et al14 reported that instability of the pulleys redirects the passive elastic forces of the EOMs in certain gaze positions, thereby producing incomitant strabismus. It is presumed that LR pulley instability may develop or progress as the
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result of degeneration or trauma to the connective tissue suspensions of the LR pulley. The pulleys of the rectus EOMs normally minimize sideslip relative to the orbit of posterior EOM paths during globe rotation and determine the effective pulling direction of each EOM. MRI has demonstrated that these tissue sleeves stabilize EOM bellies relative to the orbit, permitting only the insertional ends of the EOMs to move with the globe rotation. Radial displacements of pulleys from the orbital center do not appear to influence binocular alignment. However, vertical displacement of the pulleys to their planes of action may influence the risk of strabismus by altering EOM pulling direction.15 Thus, heterotopy of the pulleys and pulley instability during ocular rotation may result in a redistribution of the elastic passive forces of the rectus EOMs in turn producing incomitant strabismus.14,28 The exaggerated malposition of the LR muscle was demonstrated during strabismus surgery in one of our cases and was found to be consistent with the MRI. Progressive LR heterotopy might occur because of gradual or abrupt dehiscence of the LR pulley suspension caused by connective tissue degeneration analogous to levator tendon dehiscence in aponeurotic blepharoptosis.2 Lack of a contribution of the SO to Brown syndrome in cases of LR pulley instability is indicated by failure of SO tenotomy to relieve restriction to elevation in adduction. Repositioning and stabilization of the malpositioned LR was effective instead. Intraoperative traction testing also may be helpful in distinguishing mechanisms of Brown syndrome. In classic Brown syndrome with restricted travel of the SO tendon through the trochlea, limitation to passive supraduction in adduction should be increased by globe retropulsion, while the opposite effect should occur with LR pulley instability. If preoperative MRI is unavailable, intraoperative minimal exploration of the ipsilateral LR could confirm if LR instability is the cause of Brown syndrome. A muscle hook placed under the LR insertion, and held lightly by its handle end, can be used to adduct the eye. Inferior shift of the LR pulley is then obvious from inferior shift of the LR path and globe extorsion as the eye is passively rotated into adduction. Although repetition of intraoperative forced duction testing after SO tenotomy can be used as another diagnostic marker for a non-SO cause of restriction to elevation in adduction, this is a significantly invasive maneuver that would better be avoided if the diagnosis can be reached by less traumatic means. Even if the diagnostically divided SO tendon were immediately re-anastamosed, the resulting scarring near the trochlea could easily impede tendon motion through it, and induce classic Brown syndrome. Surgery to stabilize the posterior unstable LR completely relieved the restriction and significantly corrected the vertical tropia in cases of Brown syndrome due to unstable LR pulleys. Few cases of Brown syndrome caused by restrictive bands with a normal SO tendon trochlear complex have
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FIG 10. Versions of case 11 in 9 diagnostic positions of gaze, demonstrating underelevation of the right eye in adduction.
FIG 11. Coronal T1 MRI of case 11 demonstrating hypoplasia of the right SO muscle.
been reported. Romaine29 suggested that in cases of Brown syndrome where no abnormality is found in the SO, then areas of Lockwood’s ligament, IO, and IR muscle should be surgically explored. According to Romaine, restricting bands near the IR or SO muscles could cause Brown syndrome. No such bands were encountered in the present series, and the availability of modern MRI now makes this noninvasive diagnostic option attractive in comparison to blind surgical exploration of the inferior orbit. Two of the congenital cases reported here demonstrated fibrous adhesion bands extending from the trochlear region to the nasal aspect of the SR muscle. One of these cases demonstrated an absence of the SO belly, and the other had a grossly atrophic SO muscle. Both these cases had a combined ipsilateral Brown syndrome with SO palsy, and so might not be regarded as typical Brown syndrome in this respect. The fibrous band was responsible for a restriction to elevation in adduction of the affected eye. This fibrous band could be a remnant of the anterior tendon of a congenitally maldeveloped SO muscle. The various distinct functional anatomical abnormalities demonstrated in both congenital and acquired cases of Brown syndrome highlight the importance of obtaining a specific etiological diagnosis in such patients preoperatively. Brown syndrome is only a syndrome, not a specific mechanism, and as such has a differential list of causes.
High-resolution, multipositional MRI can define in great detail the pathological anatomical abnormalities causing Brown syndrome, allowing rational individualization of surgical management without reliance on extensive exploratory surgery or a trial and error series of operations. High-quality orbital MRI is currently within the technical capabilities of many North American medical centers, but for this purpose must be requested in some specific detail by the strabismologist. Where adequate imaging is unavailable, knowledge of the possible mechanisms described here can aid in interpretation of intraoperative traction testing to localize some of the specific mechanisms responsible for Brown syndrome.
References 1. Brown HW.Congenital structural muscle anomalies. In: Allen JH, editor. Strabismus Ophthalmic Symposium. St Louis: CV Mosby, 1950, pp. 205-36. 2. Oh SY, Poukens V Demer JL. Quantitative analysis of extraocular muscle layers in monkey and human. Invest Ophthalmol Vis Sci. 2001;42:10-6. 3. Demer JL. The orbital pulley system—a revolution in concepts of orbital anatomy. Ann NY Acad Sci 2002;956:17-32. 4. Kono R, Poukens V, Demer JL. Quantitative analysis of the structure of the human extraocular muscle pulley system. Invest Ophthalmol Vis Sci 2002;43:2923-32. 5. Miller JM, Demer JL, Poukens V, Pavlowski DS, Nguyen HN, Rossi EA. Extraocular connective tissue architecture. J Vision 2003;2:12-23. 6. Demer JL, Miller JM.Orbital imaging in strabismus surgery. In: Rosenbaum AL, Santiago P, editors. Clinical strabismus management: principles and surgical techniques. New York: Mosby; 1999, 84-98. 7. Demer JL, Clark RA, Kono R, Wright W, Velez F, Rosenbaum AL. A 12-year, prospective study of extraocular muscle imaging in complex strabismus. J AAPOS. 2002;6:337-47. 8. Demer JL, Oh SY, Clark RA, Poukens V. Evidence for a pulley of the inferior oblique muscle. Invest Ophthalmol Vis Sci. 2003;44:3856-65. 9. Demer JL, Miller JM, Koo EY, Rosenbaum AL. Quantitative magnetic resonance morphometry of the extra- ocular muscles: a new diagnostic tool in paralytic strabismus. J Ped Opththalmol Strabismus 1994;31:177-88. 10. Kono R, Clark RA, Demer JL. Active pulleys: magnetic resonance imaging of rectus muscle paths in tertiary gazes. Invest Ophthalmol Vis Sci 2002;43:2179-88. 11. Demer JL, Kono R, Wright W. Magnetic resonance imaging of human extraocular muscles in convergence. J Neurophysiol 2003;9: 2072-85.
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448 Bhola et al 12. Kono R Demer JL. Magnetic resonance imaging of the functional anatomy of the inferior oblique muscle in superior oblique palsy. Ophthalmology 2003;110:1219-29. 13. Demer JL. Pivotal role of orbital connective tissues in binocular alignment and strabismus. The Friedenwald lecture. Invest Ophthalmol Vis Sci 2004;45:729-38. 14. Oh SY, Clark RA, Velez F, Rosenbaum AL, Demer JL. Incomitant strabismus associated with instability of rectus pulleys. Invest Ophthalmol Vis Sci 2002;43:2169-78. 15. Clark RA, Miller JM, Demer JL. Three-dimensional location of human rectus pulleys by path inflections in secondary gaze positions. Invest Ophthalmol Vis Sci 2000;41:3787-97. 16. Siegel LM, DeSalles NL, Rosenbaum AL, Demer JL. Magnetic resonance imaging features of two cases of acquired Brown syndrome. Strabismus 1998;6:19-29. 17. Demer JL, Miller JM. Magnetic resonance imaging of the functional anatomy of the superior oblique muscle. Invest Ophthalmol Vis Sci 1995;36:906-13. 18. Blanchard CL, Young LA. Acquired inflammatory superior oblique tendon sheath (Brown syndrome). Report of a case following frontal sinus surgery. Arch Otolaryngol 1984;110:120-122 19. Rosenbuam AL, Astle WF. Superior oblique and inferior rectus muscle injury following frontal and intranasal sinus surgery. J Pediatr Ophthalmol Strabismus 1985;22:194-202.
20. Wilson EM, Eustis SH, JR., Parks MM. Brown syndrome Surv Ophthalmol 1989;34:153-72. 21. Wright KW, Silverstein D, Marrone AC, Smith RE. Acquired inflammatory superior oblique tendon sheath syndrome—a clinopathologic study. Arch Ophthalmol 1982;100:1752-4. 22. Levine MR, Boynton J, Tenzel RR, Miller GR. Complications of blepheroplasty. Ophthalmic Surg 1975;6:47-53. 23. Barnette JA, Griffiths JC, West RH. ,Acquired Brown syndrome . Ann Rheum Dis; 1993;52:835. (letter comment) 24. Hermann JS. Acquired Brown syndrome of inflammatory origin. Arch Ophthalmol 1978;96:1228-32. 25. Whitefield L, Isenberg DA, Brazier DJ, Forbes J. Acquired Brown syndrome in systemic lupus erythematosus. Br J Rheum 1995;34: 1092-4. 26. Brahma AK, Hay E, Sturgess DA, Morgan LH. Acquired Brown syndrome and primary Sjogren’s syndrome . Br J Ophthalmol 1995; 79:89-90. (letter) 27. Roper-Hall MJ, Roper-Hall G. The superior oblique “click” syndrome in Orthoptics. Proc Second Int Orthoptic Congress Amsterdam, May 1971:11-13. 28. Clark RA, Miller JM, Rosenbaum AL, Demer JL. Heterotopic muscle pulleys or oblique muscle dysfunction? J AAPOS 1998;2:17-25. 29. Romaine HH. Motility surgery. NY State J Med 1963;63:1511-4.
An Eye on the Arts – The Arts on the Eye
THE LAST RAYS of evening light are filtering through the window when Vishnu sees the image. A man is standing over his body on the landing down below. He kneels besides him, and pulls back the sheet. With one hand, the man touches Vishnu’s cheek; with the other, he presses the forehead and brushes the wisps of hair off the eyes. Fingertips trace across Vishnu’s lips, then down his chin, and to his chest, where they rub against his heart. The man has his eyes closed. His neck is arched, head tilted upwards, lips reciting silent words. Vishnu has seen this silhouette before, he knows he should recognize the crouching figure. The man’s eyes open. Their whiteness reaches through the dark. They are large and milky, staring up through the air, through the ceiling, through the stone, at some point outside in the sky. Vishnu looks at them and is unsure if they are filled with reverence or fear. The eyes blink, the fingers caress the tufts of chest hair, the lips open and close. Soft words float slowly up from the upturned face. Vishnu sees the gray hair, sees the bulbous nose, sees the pockmarks on the cheeks. Recognition floods in finally. He peers down at Mr. Jalal on the landing, crouching next to his body, staring up through the darkness towards heaven.—Manil Suri (from The Death of Vishnu, HarperCollins)
B
a
From the Jules Stein Eye Institute, University of California, Los Angeles and the Department of Neurology, University of California, Los Angeles, California Presented at the 30th annual meeting of the American Association for Pediatric Ophthalmology and Strabismus, Washington, DC, March 27-31, 2004. Supported by USPHS NIH EY08313 & Research to Prevent Blindness. J.L.D. received an unrestricted award from Research to Prevent Blindness and is the Leonard Apt Professor of Ophthalmology at UCLA. A.L.R. is a recipient of a Research to Prevent Blindness Physician-Scientist Merit Award. Submitted March 9, 2004. Revision accepted June 17, 2005. Reprint requests: Joseph L. Demer MD, PhD, Jules Stein Eye Institute, 100 Stein Plaza, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-7002 (e-mail: [email protected]). Copyright © 2005 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/2005/$35.00 ⫹ 0 doi:10.1016/j.jaapos.2005.07.001 b
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mechanisms for Brown syndrome besides pathology of the SO tendon and trochlea. Knowledge of orbital and extraocular muscle (EOM) anatomy has progressed since the time of Harold Brown. Motivated by efforts to develop computer simulations of EOM behavior to guide strabismus surgery, researchers recently have conducted anatomical re-examinations of orbital anatomy using immunohistochemistry of serially sectioned orbits,2-4 computer reconstructions in virtual reality,5 and multipositional magnetic resonance imaging (MRI) with spatial resolution enhanced by use of surface coils6,7 and tissue resolution enhanced with paramagnetic contrast8 to study the functional anatomy of the EOMs.7,9-12 From these investigations has emerged a detailed picture of the vital role of EOM paths in determination of EOM function.13In brief, the action exerted by any EOM on the globe is determined not only by the magnitude of tension it exerts but also on the pulling direction of that tension. For any EOM, pulling direction is determined by its scleral insertion and the location of its functional origin. The functional origin of each EOM is at a connective tissue structure called a pulley. Harold Brown recognized the importance of the SO pulley—the classic trochlea—to SO function. We now know that all of the other EOMs have less rigid, but still essential, pulleys.3-5,8 The pathology of these pulleys causes incomitant strabismus that can clinically simulate oblique EOM dysfunction. For example, instability of the LR pulley has been demJournal of AAPOS
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onstrated by multipositional MRI to simulate Brown syndrome.14 It was observed that the instability of the pulleys was accentuated in particular gazes and was responsible for the incomitance of the deviation. Although clinical tests like alignment measurements, forced duction, forced generation, and saccadic velocity testing may be helpful in evaluating Brown syndrome, they may not define the pathophysiology accurately. Multipositional MRI can provide valuable additional clinical information to demonstrate a variety of different anatomical mechanisms in patients presenting clinically with Brown syndrome. We performed this study to explore the spectrum of clinical abnormalities in Brown syndrome.
MATERIALS AND METHODS Participating patients were selected from an ongoing, prospective study of orbital imaging in strabismic patients. Eleven consecutive cases of unilateral Brown syndrome were identified based on clinical findings, including 3 patients with congenital and 8 patients with acquired disorders. All the patients complained of constant or intermittent vertical diplopia and had limitation to elevation in adduction in one eye. A complete ophthalmic evaluation, including a detailed ocular motility examination, was performed in all the cases. Binocular alignment was measured using prism and alternate cover test both for distance and near in the cardinal gaze directions and with head tilt to each side, and with the Hess screen test in 21 fixation positions over a 30 degree field for each eye. Ductions and versions were quantified using a 9-point scale, with 0 suggesting a normal movement, – 4 signifying an inability to move the eye past midline, and ⫹4 signifying maximum observable overrotation. After obtaining written informed consent according to a protocol confirming to the Declaration of Helsinki and approved by the Institutional Review Board, each subject underwent multipositional high-resolution T1-weighted MRI with a 1.5-T General Electric Signa (Milwaukee, WI) scanner using methods previously described in detail.6,7 Depending on the clinical indication, T2 imaging was used occasionally in addition. Each subject’s head was carefully stabilized in a supine position with the nose aligned to the longitudinal and the pupils to the transverse light projection references of the scanner. Imaging of the orbits was performed in multiple gaze positions using a phased array of 4 surface coils deployed in a mask-like enclosure held strapped to the face. An adjustable array of monocular, afocal, illuminated fixation targets at 9 diagnostic positions of gaze was secured in front of each orbit with the center target in subjective central position for each eye. Head movement of the subjects was minimized by secure stabilization to the surface coil facemask and judicious use of padded restraints. Multiple contiguous quasicoronal digital images of 2-mm slice thickness were then obtained using a 256 ⫻ 256 matrix over an 8-cm2 field, giving pixel resolutions of 313
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m. Imaging was then repeated in multiple gaze positions. The trochlea and reflected SO tendon also were imaged using axial image planes of the same resolution. In appropriate cases, the inferior oblique muscle was imaged in quasisagittal image planes parallel to the long axis of the orbit. Digital MRIs were transferred to Macintosh computers (Apple Computer, Cupertino, CA) and converted to 8-bit tagged image file format and were quantitatively analyzed using the program NIH Image (W. Rasband, National Institute of Health; available by ftp from zippy. nimh.nih.gov or on floppy disk from NTIS, Springfield, VA, part number PB95-500195GEI). We studied the size of the EOMs in different gaze positions of both the eyes in all subjects. Change in EOM cross section from relaxed to contracting gaze positions was used as an index of contractility. Anatomical characteristics of the SO muscle and tendon and its relationship with the trochlea was evaluated in multiple gaze positions where clinically appropriate. Subject data were compared with the existing data of the normal rectus pulley positions relative to the globe center as determined by Clark et al15 in 22 orbits of 11 normal adults using the same NIH Image program and a similar prospective protocol of high-resolution, multipositional orbital MRI using surface coils.
RESULTS Twenty-two orbits of 11 subjects with Brown syndrome were analyzed. Clinical information of the subjects is summarized in Table 1. According to the anatomic abnormalities as elicited by MRI, 4 distinct mechanisms of Brown syndrome were identified: (1) trochlear damage; (2) SO tendon abnormalities; (3) abnormalities of rectus EOM pulleys; and (4) congenital abnormalities of SO muscle. Cases were segregated by mechanism. Trochlear Damage Case 1. This 17-year-old boy presented with a history of vertical binocular diplopia in upgaze after a bilateral frontal sinus surgery for bacterial sinusitis 3 months before his presentation. Uncorrected visual acuity was 20/15 in each eye. External examination was notable for healed Lynch incisions bilaterally (Figure 1) with a palpable scar web over the region of the left trochlea but without trochlear tenderness. There was marked limitation to supraduction of the right eye in adduction (Figure 1). The patient was orthotropic in all diagnostic fields, including head tilt, with the exception of upgaze, in which there was a large right hypotropia. High-resolution multipositional MRI revealed an extensive scarring in the region of both trochleas. Imaging with contrast demonstrated continuity of a cicatrix from the right frontoethmoidal sinus region through the trochlea entering the SO tendon (Figure 2). Case 2. This 36-year-old woman presented with a history of vertical binocular diplopia in up gaze, subsequent to a trauma on the left orbit from a softball. She
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440 Bhola et al TABLE 1 Clinical profile of patients Subject
Age(years)/sex
Onset
Central gaze deviation
1. 2. 3.
17/M 36/F 7/M
Acquired: frontal sinus surgery Acquired: trauma Acquired: dog bite
Orthotropic 4 PD Exophoria 18 PD LHT 7° Excy. OS
4.
21/F
Acquired: automotive accident
30 PD RHT 4° Excy. OD
5. 6. 7. 8. 9. 10.
64/F 36/F 11/F 69/M 53/F 14/M
Acquired: blepheroplasty Acquired: idiopathic Congenital Acquired: idiopathic Acquired: orbital decompression Congenital
Orthotropic 3 PD RH(T) 20 PD LHoT 10 PD XT 8 PD RHT 7° Excy. OD 20 PD LHoT 10° Incyc. OS 35 PD LHT
11.
8/M
Congenital
14 PD RHT 8 PD ET
MRI findings Scarring of right trochlea from the frontal sinus Adhesion bands left trochlea, SOT thickening Disorganization of left tendon/trochlear complex with scarring Right trochlear avulsion; left trochlear disruption Possible suture in reflected SOT Cyst in SOT posterior to trochlea Left LR pulley instability Left LR pulley instability Left LR pulley instability and adhesion to orbit Hypoplastic left SOM, fibrous band from sclera to trochlea Attenuation of right SOM, fibrous band from sclera to trochlea
PD, prism diopters; RHT, right hypertropia; LHT, left hypertropia; RH(T), intermittent right hypertropia; LHoT, left hypotropia; XT, exotropia; F, female. Excy, excycotorsion. LR, lateral rectus muscle; M, male; SOM, superior oblique muscle; SOT, superior oblique tendon.
FIG 1. Versions of subject 1 in 9 diagnostic positions of gaze, demonstrating underelevation on adduction of the right eye. Note scarring from the Lynch incisions over both trochleas.
complained of left trochlear pain, trochlear tenderness, and an occasional clicking sound from the left trochlear region when looking upward. Uncorrected visual acuity was 20/20 in each eye. There was limitation to elevation of the left eye in both abduction and adduction that was worse in adduction. At distance, there was 4⌬ of exophoria in primary gaze and in right gaze. She was orthotropic in left gaze and down gaze, but in up gaze exhibited a left hypotropia of 8⌬. At near gaze she had 8⌬ exophoria. High-resolution MRI demonstrated an abnormality in the left reflected SO tendon with adhesion bands in the trochlear region. The patient was administered steroid injections in the left trochlea without resolution of her symptoms. Subsequently, a surgical exploration of the left trochlea and SO was performed, which revealed an enlargement of the left SO tendon, which was found to be folded on itself with fibrous adhesions extending back to
the trochlea. The adhesions were lysed surgically, and the left trochlea was infiltrated with long and short acting steroids. Symptoms recurred after initial improvement. SO tenotomy with a compensatory surgery on the ipsilateral IO is planned. Case 3. This 7-year-old boy developed a vertical binocular diplopia and spontaneous right head tilt after being bitten by a dog above the left eye 5 months before his presentation. The clinical and examination findings of the patient have been previously reported.16 Multipositional MRI scans of the left orbit showed marked scarring in the area of the left trochlea along with SO tendon sheath thickening. There was marked disorganization of the tendon/trochlear complex. Case 4. This 21-year-old woman developed a vertical binocular diplopia after severe head trauma in an automotive collision. Visual acuity was 20/20 with a myopic cor-
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FIG 2. Coronal T1-weighted, contrast-enhanced MRI image of the right orbit of subject 1 showing a cicatrix from the right frontoethmoidal sinus region to the trochlea Note enhancement of the sinus mucosa.
rection. There was moderate overelevation in adduction of the right eye, with marked underelevation and downshoot in adduction of the left eye (Figure 3). There was mild limitation to infraduction of the right eye, particularly in adduction. At distance, there was 30⌬ right hypertropia in primary position, decreasing in right gaze and increasing in left gaze. The deviation increased in upgaze and diminished slightly in downgaze. Forced head tilt test revealed 50⌬ of right hypertropia with right head tilt diminishing to 15⌬ in left head tilt. At near there was 25 ⌬ right hypertropia with 6⌬ exotropia. Double Maddox rod testing demonstrated 3-4o right excyclotorsion. Highresolution MRI revealed right trochlear avulsion along with disengagement of the SO tendon and a trochlear disruption in the left eye (Figure 4). The patient underwent left SO tenotomy, a 10-mm right IO recession, and a 3-mm left inferior rectus recession on adjustable suture. At 3-week postoperative follow-up, she presented with a small consecutive left hypertropia that was treated successfully with a small spectacle prism. Superior Oblique Tendon Abnormalities Case 5. This 64-year-old woman complained of vertical binocular diplopia immediately after undergoing bilateral upper eyelid blepharoplasty 9 months before. Uncorrected visual acuity was 20/20 in each eye. There was marked limitation of elevation of the left eye in adduction (Figure 5). She was orthotropic in primary position but had 25⌬ left hypotropia in upward gaze to the right. Motion of a nodule could be palpated in the region of the left trochlea during attempted up and down gaze. Forced duction testing showed marked restriction to elevation of
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the left eye in adduction. Axial (Figure 6A) and coronal (Figure 6B) MRI revealed a nodular structure in the left reflected SO tendon just lateral to the trochlea, and multiple nodular structures in the anterior superomedial right orbit. These structures demonstrated a low intensity both on T1- and T2-weighted imaging, with a high-intensity rim suggestive of suture material or cautery effect from the blepharoplasty surgery interfering with the reflected SO tendon. Case 6. This 36 year-old woman noticed progressively increasing intermittent pain over the right trochlea with intermittent vertical diplopia beginning18 months before presentation. She also noticed a palpable click in the region of the right trochlea on shift from up- to downgaze. Details of this patient have been previously described in a case report.16 MRI showed a spherical structure in the SO tendon that was presumed to be a cyst. This cystic structure was seen to change anteroposterior position with vertical gaze shifts. In supraduction, the SO tendon was passively stretched and the cyst was pulled anteriorly. In primary position the cyst was posterior and began to abut the trochlea but apparently did not enter it. In infraduction the SO muscle contracted and the cyst retracted, distant from the trochlea. The patient’s symptoms can be explained by interference of the cyst with the trochlea; the cyst must be dragged through the trochlea on excursion from down- to upgaze. This causes a temporary restriction, which gives way with a palpable click as the bulk of the cyst moves anterior to the trochlea in upgaze. The SO tendon was explored surgically. The abnormal cystic structure surrounding the tendon was excised, and the surrounding area was infiltrated with steroids. The patient was asymptomatic on the first postoperative day. Abnormalities of Rectus Extraocular Muscle Pulleys Case 7. This 11-year-old girl presented with a history of anomalous head posture, inability to elevate the left eye in adduction, and left hypotropia since the age of 3 months. Uncorrected acuity was 20/20 in each eye. The patient had a 20° right face turn with a 5° chin elevation. There was marked underelevation of the left eye in adduction and moderate elevation limitation in abduction. There was a moderate overdepression of the left eye in adduction. In forced primary position at distance there was 20⌬ left hypotropia and 10⌬ exotropia. At near there was 20⌬ left hypotropia and 16⌬ exotropia. Intraoperative forced duction testing revealed marked restriction to supraduction of the left eye in adduction. Surgical exploration showed the anatomical position, fibers and tension of the SO tendon to be normal. Left SO tenotomy with a 7-mm silicon spacer failed to immediately relieve restriction to supraduction. The spacer was replaced with a suture and the posterior end of the SO tendon was allowed to retract approximately 15 mm. Postoperative examination on the first day and 6 months later showed minimal improvement in the anomalous head posture and ocular
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FIG 3. Versions of subject 4 in 9 diagnostic positions of gaze, demonstrating severe underelevation of the left eye on adduction with moderate underelevation on abduction.
FIG 4. case 4. Top row, Coronal T1 MRI showing dislocation of the right SO tendon after avulsion of the right trochlea. Damage to the left trochlea was evident, along with medial wall blow out fractures larger on the right than left. IO, IO muscle; MR, medial rectus muscle. Bottom row, Axial T1 MRI images showing posterior displacement of the path of the right SO tendon, in relation to the normal location of the reflected left SO tendon. SR, SR muscle.
rotations, with 16⌬ left hypotropia and 8⌬ exotropia in forced primary position. High-resolution MRI at this point revealed inferior displacement of the left LR pulley, a defect that was exaggerated in adduction. There was no such abnormality demonstrated in the right orbit. In view
of the anatomical abnormality on MRI, a second surgery was performed, consisting of a left LR recession and superior insertional transposition, with posterior reteroequatorial myopexy to prevent inferior slip of the LR pulley. Intraoperative forced duction testing was immediately completely relieved of restriction. Three months postoperatively the patient had a minimal left hypotropia in primary gaze and no anomalous head posture. Case 8. This 69 year-old men presented with a 1-year history of sudden onset of vertical diplopia worse in upgaze to the right. Corrected visual acuity was 20/20 in both eyes. He had a 5° chin elevation. Cover test revealed a Y-pattern exotropia with 8⌬ right hypertropia in primary position, which increased in upgaze to 16⌬ but was generally comitant in other gaze positions. The hypertropia slightly increased on forced left head tilt. Double Maddox rod test revealed right excyclotorsion of 7°. There was limitation of supraduction of the left globe, worse in adduction. Forced duction testing revealed restriction to supraduction of the left globe, greatest in adduction. High-resolution MRI revealed no anatomic abnormality of the left SO muscle, tendon or trochlea. Instability of the left LR pulley was seen on coronal imaging, with downward shift of the left LR on adduction. Case 9. This 53-year-old woman had a 5-year history of thyroid ophthalmolopathy. Immediately after undergoing left orbital decompression via a superotemporal approach 4 months before presentation, she noticed binocular vertical diplopia with relative tilting of images, greatest in right gaze and minimized with a left head tilt and right face turn. She also felt tightness inferotemporally in the left eye socket while looking to the right. Corrected visual acuity was 20/16 in the right and 20/50 in the left eye. There was severe limitation to elevation of the left eye in adduction, but with extreme elevating effort there was a
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FIG 5. Versions of case 5 in nine diagnostic gaze positions showing underelevation of the left eye in adduction.
snap-like, sudden upward rotation of the left eye nearly normalizing supraduction in adduction (Figure 7). There was a marked overdepression of the left eye in adduction. There was no limitation to elevation of the left eye in abduction. Forced duction testing revealed a marked resistance to passive supraduction in adduction, which was suddenly relieved with a prolonged effort to look up by the patient. At distance, there was 20⌬ left hypotropia in primary gaze that diminished to 4⌬ in left gaze, and increased to 40⌬ in right gaze. The left hypotropia was 30⌬ in upward gaze and was 10⌬ in downward gaze. At near, there was 25⌬ left hypotropia with 6⌬ exotropia. There was 25⌬ left hypotropia in right head tilt diminishing to 10⌬ in left head tilt. Double Maddox rod testing demonstrated 10° left incyclotropia. High-resolution MRI revealed postsurgical cicatrisation around the left LR muscle, with apparent adhesion of the inferior pole of that EOM to the orbital wall (Figure 8). There was no abnormality of trochlea and SO on either side. Instability of the left LR pulley was suspected. This instability was confirmed by intraoperative demonstration of obvious downward slip of the LR muscle path when rotating the eye from abduction to adduction using a muscle hook engaged at the LR insertion. The LR path was stabilized by joining its superior margin to the underlying sclera using a nonabsorbable suture; the left IR muscle was recessed 3.5 mm. Six months after surgery, the patient had a marked improvement of ocular versions, and was orthotropic in primary position. The ocular torticollis was eliminated. Congenital Abnormalities of the SO Muscle Case 10. This 14-year-old boy presented with intermittent vertical diplopia that had existed since early childhood. Visual acuity in each eye was 20/20. He spontaneously adopted a 10° head tilt to the right. There was down shoot of the left eye in adduction with marked inability to elevate the left globe in adduction and reduced ability to depress the left globe in adduction. There was mild limitation to full upward rotation of the left globe in straight up position. In forced primary position, cover testing revealed 35⌬ left hypertropia that increased to 40⌬ in down gaze. The left hypertropia was reduced to 14⌬ in levover-
sion, but was 25⌬ in dextroversion. The left hypertropia was reduced in upgaze to 6⌬. Forced head tilt testing showed a left hypertropia of 25⌬ on left head tilt reducing to 6⌬ on right head tilt. The increase of left hypertropia in down gaze and left head tilt clinically suggested coexistent SO paresis. High-resolution coronal MRI suggested complete absence of the left SO muscle belly (Figure 9A). The reflected tendon of the left SO was present, but apparently terminated on the trochlea. Axial MRI showed an attenuated remnant of the left SO belly, in contrast with a normal sized right SO belly (Figure 9B). The right SO was of normal size and demonstrated robust contraction from supraduction to infraduction. Intraoperative forced duction testing revealed marked restriction to elevation of the left eye in adduction. Surgical exploration revealed a dense fibrous band that attached to the sclera at the nasal border of the left superior rectus (SR) muscle, incorporating some of its fibers. The band was traced posteriorly for a distance of 8 mm to the same area as the reflected SO tendon, but normal tendon fibers could not be visualized. After dividing this fibrous band the left IO muscle was recessed, and the left IR was resected. At the time of last follow-up, 4 years postoperatively, the patient was orthotropic in primary gaze and free of ocular torticollis. The limitation to elevation in adduction was also markedly improved. Case 11. This 8-year-old boy presented with a lifelong left head tilt. Uncorrected visual acuity was 20/30 in the right and 20/25 in the left eye. Cycloplegic refraction revealed hyperopia of ⫹ 3.50 in the right eye and ⫹ 4.25 in the left eye. On examination, there was a left head tilt of 5°. There was limitation to elevation in adduction of the right eye (Figure 10). In forced primary position, there was 14⌬ right hypertropia and 8⌬ esotropia. The right hypertropia increased to 20⌬ in downgaze, was 8⌬ in dextroversion, and 14⌬ in levoversion. There was no hypertropia in the upgaze. Esotropia was eliminated by hyperopic correction. High-resolution MRI revealed a attenuation of the right SO muscle belly (Figure 11), with size less the 95% confidence limit of normal17 with the anterior tendon terminating directly on the trochlea similar to case 10. The left SO muscle was normal in size and had normal con-
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FIG 6. Case 5. A, Axial T1 MRI showing a nodule in the reflected tendon of the left SO muscle, with irregularity around the reflected tendon. B, Coronal T2 MRI image of the left orbit the nodule in the reflected tendon of the SO muscle.
tractile thickening from supraduction to infraduction. Intraoperative forced duction testing revealed a marked restriction to elevation of the right globe in adduction. Exploration revealed a fibrous band adhesion to the sclera at the nasal border of the SR. The band appeared to be in the same area as the SO tendon, but the tendon fibers could not be visualized. This fibrous band was divided, which immediately relieved the restriction to forced duction. The left IO muscle was recessed. At the time of last follow-up 5 year, 2 month postoperatively the patient was orthophoric in primary position, and free of anomalous head posture.
DISCUSSION Multipositional, high-resolution MRI has enhanced the understanding of incomitant strabismus by revealing multiple anatomical and functional abnormalities of the ex-
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traocular muscles and their pulleys.6,7,9,10-12,16 Surgical success in incomitant strabismus often depends on pathologic mechanism, so that treatment can be directed to its correction. Brown syndrome is a narrowly defined, restrictive, incomitant strabismus whose clinical features are nevertheless nonspecific to etiology. In 1950, Brown reported 8 cases having a restrictive limitation to elevation in adduction, a condition that he called the “SO tendon sheath syndrome.”1 This restriction to elevation was believed to be caused by secondary shortening of the anterior sheath of the SO tendon from congenital palsy of the “ipsilateral IO.” Pathology of the IO muscle is no longer considered important in Brown syndrome, but numerous other etiologies have been proposed. The inconsistent response to SO relaxation and tenotomy procedures in some of these cases inspired us to study the anatomical abnormalities associated with this syndrome using a multipositonal, high-resolution MRI. We here report 11 patients with Brown syndrome and ipsilateral restrictive limitation to elevation in adduction. Despite the typical clinical features, we found four distinct abnormalities of functional anatomy. Six of the 8 acquired cases developed Brown syndrome secondary to surgical or accidental trauma. Although all these cases had a similar clinical presentation with acute onset, multipositional MRI revealed varied abnormalities. Four of these traumatic cases demonstrated trochlear damage restricting free passage of the SO tendon through the trochlea. Case 1 developed Brown syndrome after a frontal sinus surgery. Blanchard and Young in 198418 and Rosenbaum and Astle19 in 1985 reported Brown syndrome after frontal sinus surgery. Improper surgical technique, such as placement of the surgical incision too low or excessive periosteal stripping near the trochlea, can contribute to the SO damage or restriction. In addition, a cicatrisation of the SO to the globe, bone or into the sinus scar tissue defect may restrict eye movement.19 High-resolution imaging with contrast explicitly demonstrated continuity of a ci catrix from the right frontal sinus region through the trochlea entering the SO tendon in case 1, thus revealing the cause of restrictive incomitance. Direct nonsurgical trauma to the superomedial orbit can disturb the function of the SO muscle, causing the clinical appearance of SO palsy, Brown syndrome, or both.20 Restricted elevation in adduction secondary to trauma can be a manifestation of either direct injury to trochlear-SO tendon complex the result of scarring from the inflammation surrounding the SO tendon.21 Highresolution MRI can be useful in such cases to define the exact anatomical abnormality. Three of our cases developed a Brown syndrome secondary to accidental trauma and showed varied abnormalities on MRI. Case 2 showed scarring in the area of the trochlea along with tendon sheath thickening. Case 3 demonstrated abnormalities in the reflected SO tendon anterior to the trochlea, with
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FIG 7. Versions of case 9 in 9 diagnostic positions of gaze, demonstrating underelevation and downshoot of the left eye in adduction.
FIG 8. case 9. Top- Axial images of the left orbit show normal SO tendon trochlear complex. Bottom-Coronal MRI of the left orbit in central gaze showing cicatrization near the inferior pole of the LR pulley after orbital decompression surgery. The orbitotomy site is visible superolaterally in the left orbit. LR, lateral rectus muscle; SO, SO muscle.
tendon thickening and adhesions. Case 4 revealed a trochlear disruption in one eye and a trochlear avulsion in the contralateral eye, presenting clinically as Brown syndrome with contralateral SO palsy. Incarceration of the SO tendon, with fat, orbicularis, levator aponeurosis, and septum has been reported after
blepharoplasty.22 Case 5 developed vertical binocular diplopia immediately after undergoing bilateral upper eyelid blepharoplasty. High-resolution MRI scan in this patient suggested that deeply placed blepharoplasty sutures, or possibly cautery, had included the reflected SO tendon. Impediment of free movement of the SO tendon in the trochlear tendon complex has been proposed as a cause of Brown syndrome. Inflammation by such etiologies as juvenile rheumatoid arthritis, lupus, and Sjogren’s syndrome,23-26 trauma or other restrictive phenomena have been proposed to compromise function. In 1971 RoperHall27 in their series described “SO ‘click’ syndrome” presumed to be an inflammatory form of Brown syndrome. The clinical picture can alternate between Brown syndrome and SO palsy, depending on the direction in which the tendon movement through the trochlea is impeded. One of our acquired cases presented with an intermittent picture of Brown syndrome with a palpable click over the trochlear region on change from supraduction to infraduction. Although the patient had no clinical evidence of any inflammatory or autoimmune disorder, a multipositional MRI showed the location and movement of a spherical structure in the SO tendon that correlated with the patient’s symptoms. This spherical structure was surgically confirmed to be a cyst that interfered with normal transit of the SO tendon through the trochlea. An acute onset of Brown syndrome was observed in case 9 after an orbital decompression surgery for thyroid ophthalmopathy that completely avoided the trochlear region. High-resolution MRI revealed evidence of damage to the left LR pulley. This indication of LR pulley instability was confirmed intraoperatively by demonstrating the shift in LR path during passive adduction of the eye. Supraplacement and stabilization of the LR path by superior myopexy corrected the limitation to elevation of the eye in adduction.
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FIG 9. T1 MRI in case 10. A, Coronal images showing apparent absence of left SO muscle (SO) but presence of its reflected tendon inserting on the trochlea. IO, IO muscle; LPS, levator palpebrae superioris muscle; ON, optic nerve; SR, SR muscle. B, Axial images showing a normal right SO belly, trochlea, and reflected tendon, but marked attenuation of the left SO posterior to the trochlea.
One congenital (case 7) and one acquired case (case 8) demonstrated a vertical instability of the LR pulley in adduction. In both patients there was an inferior displacement of the LR pulley of the involved eye, a defect that was exaggerated in adduction. This LR side slip causes restrictive limitation to elevation in adduction. Oh et al14 reported that instability of the pulleys redirects the passive elastic forces of the EOMs in certain gaze positions, thereby producing incomitant strabismus. It is presumed that LR pulley instability may develop or progress as the
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result of degeneration or trauma to the connective tissue suspensions of the LR pulley. The pulleys of the rectus EOMs normally minimize sideslip relative to the orbit of posterior EOM paths during globe rotation and determine the effective pulling direction of each EOM. MRI has demonstrated that these tissue sleeves stabilize EOM bellies relative to the orbit, permitting only the insertional ends of the EOMs to move with the globe rotation. Radial displacements of pulleys from the orbital center do not appear to influence binocular alignment. However, vertical displacement of the pulleys to their planes of action may influence the risk of strabismus by altering EOM pulling direction.15 Thus, heterotopy of the pulleys and pulley instability during ocular rotation may result in a redistribution of the elastic passive forces of the rectus EOMs in turn producing incomitant strabismus.14,28 The exaggerated malposition of the LR muscle was demonstrated during strabismus surgery in one of our cases and was found to be consistent with the MRI. Progressive LR heterotopy might occur because of gradual or abrupt dehiscence of the LR pulley suspension caused by connective tissue degeneration analogous to levator tendon dehiscence in aponeurotic blepharoptosis.2 Lack of a contribution of the SO to Brown syndrome in cases of LR pulley instability is indicated by failure of SO tenotomy to relieve restriction to elevation in adduction. Repositioning and stabilization of the malpositioned LR was effective instead. Intraoperative traction testing also may be helpful in distinguishing mechanisms of Brown syndrome. In classic Brown syndrome with restricted travel of the SO tendon through the trochlea, limitation to passive supraduction in adduction should be increased by globe retropulsion, while the opposite effect should occur with LR pulley instability. If preoperative MRI is unavailable, intraoperative minimal exploration of the ipsilateral LR could confirm if LR instability is the cause of Brown syndrome. A muscle hook placed under the LR insertion, and held lightly by its handle end, can be used to adduct the eye. Inferior shift of the LR pulley is then obvious from inferior shift of the LR path and globe extorsion as the eye is passively rotated into adduction. Although repetition of intraoperative forced duction testing after SO tenotomy can be used as another diagnostic marker for a non-SO cause of restriction to elevation in adduction, this is a significantly invasive maneuver that would better be avoided if the diagnosis can be reached by less traumatic means. Even if the diagnostically divided SO tendon were immediately re-anastamosed, the resulting scarring near the trochlea could easily impede tendon motion through it, and induce classic Brown syndrome. Surgery to stabilize the posterior unstable LR completely relieved the restriction and significantly corrected the vertical tropia in cases of Brown syndrome due to unstable LR pulleys. Few cases of Brown syndrome caused by restrictive bands with a normal SO tendon trochlear complex have
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FIG 10. Versions of case 11 in 9 diagnostic positions of gaze, demonstrating underelevation of the right eye in adduction.
FIG 11. Coronal T1 MRI of case 11 demonstrating hypoplasia of the right SO muscle.
been reported. Romaine29 suggested that in cases of Brown syndrome where no abnormality is found in the SO, then areas of Lockwood’s ligament, IO, and IR muscle should be surgically explored. According to Romaine, restricting bands near the IR or SO muscles could cause Brown syndrome. No such bands were encountered in the present series, and the availability of modern MRI now makes this noninvasive diagnostic option attractive in comparison to blind surgical exploration of the inferior orbit. Two of the congenital cases reported here demonstrated fibrous adhesion bands extending from the trochlear region to the nasal aspect of the SR muscle. One of these cases demonstrated an absence of the SO belly, and the other had a grossly atrophic SO muscle. Both these cases had a combined ipsilateral Brown syndrome with SO palsy, and so might not be regarded as typical Brown syndrome in this respect. The fibrous band was responsible for a restriction to elevation in adduction of the affected eye. This fibrous band could be a remnant of the anterior tendon of a congenitally maldeveloped SO muscle. The various distinct functional anatomical abnormalities demonstrated in both congenital and acquired cases of Brown syndrome highlight the importance of obtaining a specific etiological diagnosis in such patients preoperatively. Brown syndrome is only a syndrome, not a specific mechanism, and as such has a differential list of causes.
High-resolution, multipositional MRI can define in great detail the pathological anatomical abnormalities causing Brown syndrome, allowing rational individualization of surgical management without reliance on extensive exploratory surgery or a trial and error series of operations. High-quality orbital MRI is currently within the technical capabilities of many North American medical centers, but for this purpose must be requested in some specific detail by the strabismologist. Where adequate imaging is unavailable, knowledge of the possible mechanisms described here can aid in interpretation of intraoperative traction testing to localize some of the specific mechanisms responsible for Brown syndrome.
References 1. Brown HW.Congenital structural muscle anomalies. In: Allen JH, editor. Strabismus Ophthalmic Symposium. St Louis: CV Mosby, 1950, pp. 205-36. 2. Oh SY, Poukens V Demer JL. Quantitative analysis of extraocular muscle layers in monkey and human. Invest Ophthalmol Vis Sci. 2001;42:10-6. 3. Demer JL. The orbital pulley system—a revolution in concepts of orbital anatomy. Ann NY Acad Sci 2002;956:17-32. 4. Kono R, Poukens V, Demer JL. Quantitative analysis of the structure of the human extraocular muscle pulley system. Invest Ophthalmol Vis Sci 2002;43:2923-32. 5. Miller JM, Demer JL, Poukens V, Pavlowski DS, Nguyen HN, Rossi EA. Extraocular connective tissue architecture. J Vision 2003;2:12-23. 6. Demer JL, Miller JM.Orbital imaging in strabismus surgery. In: Rosenbaum AL, Santiago P, editors. Clinical strabismus management: principles and surgical techniques. New York: Mosby; 1999, 84-98. 7. Demer JL, Clark RA, Kono R, Wright W, Velez F, Rosenbaum AL. A 12-year, prospective study of extraocular muscle imaging in complex strabismus. J AAPOS. 2002;6:337-47. 8. Demer JL, Oh SY, Clark RA, Poukens V. Evidence for a pulley of the inferior oblique muscle. Invest Ophthalmol Vis Sci. 2003;44:3856-65. 9. Demer JL, Miller JM, Koo EY, Rosenbaum AL. Quantitative magnetic resonance morphometry of the extra- ocular muscles: a new diagnostic tool in paralytic strabismus. J Ped Opththalmol Strabismus 1994;31:177-88. 10. Kono R, Clark RA, Demer JL. Active pulleys: magnetic resonance imaging of rectus muscle paths in tertiary gazes. Invest Ophthalmol Vis Sci 2002;43:2179-88. 11. Demer JL, Kono R, Wright W. Magnetic resonance imaging of human extraocular muscles in convergence. J Neurophysiol 2003;9: 2072-85.
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448 Bhola et al 12. Kono R Demer JL. Magnetic resonance imaging of the functional anatomy of the inferior oblique muscle in superior oblique palsy. Ophthalmology 2003;110:1219-29. 13. Demer JL. Pivotal role of orbital connective tissues in binocular alignment and strabismus. The Friedenwald lecture. Invest Ophthalmol Vis Sci 2004;45:729-38. 14. Oh SY, Clark RA, Velez F, Rosenbaum AL, Demer JL. Incomitant strabismus associated with instability of rectus pulleys. Invest Ophthalmol Vis Sci 2002;43:2169-78. 15. Clark RA, Miller JM, Demer JL. Three-dimensional location of human rectus pulleys by path inflections in secondary gaze positions. Invest Ophthalmol Vis Sci 2000;41:3787-97. 16. Siegel LM, DeSalles NL, Rosenbaum AL, Demer JL. Magnetic resonance imaging features of two cases of acquired Brown syndrome. Strabismus 1998;6:19-29. 17. Demer JL, Miller JM. Magnetic resonance imaging of the functional anatomy of the superior oblique muscle. Invest Ophthalmol Vis Sci 1995;36:906-13. 18. Blanchard CL, Young LA. Acquired inflammatory superior oblique tendon sheath (Brown syndrome). Report of a case following frontal sinus surgery. Arch Otolaryngol 1984;110:120-122 19. Rosenbuam AL, Astle WF. Superior oblique and inferior rectus muscle injury following frontal and intranasal sinus surgery. J Pediatr Ophthalmol Strabismus 1985;22:194-202.
20. Wilson EM, Eustis SH, JR., Parks MM. Brown syndrome Surv Ophthalmol 1989;34:153-72. 21. Wright KW, Silverstein D, Marrone AC, Smith RE. Acquired inflammatory superior oblique tendon sheath syndrome—a clinopathologic study. Arch Ophthalmol 1982;100:1752-4. 22. Levine MR, Boynton J, Tenzel RR, Miller GR. Complications of blepheroplasty. Ophthalmic Surg 1975;6:47-53. 23. Barnette JA, Griffiths JC, West RH. ,Acquired Brown syndrome . Ann Rheum Dis; 1993;52:835. (letter comment) 24. Hermann JS. Acquired Brown syndrome of inflammatory origin. Arch Ophthalmol 1978;96:1228-32. 25. Whitefield L, Isenberg DA, Brazier DJ, Forbes J. Acquired Brown syndrome in systemic lupus erythematosus. Br J Rheum 1995;34: 1092-4. 26. Brahma AK, Hay E, Sturgess DA, Morgan LH. Acquired Brown syndrome and primary Sjogren’s syndrome . Br J Ophthalmol 1995; 79:89-90. (letter) 27. Roper-Hall MJ, Roper-Hall G. The superior oblique “click” syndrome in Orthoptics. Proc Second Int Orthoptic Congress Amsterdam, May 1971:11-13. 28. Clark RA, Miller JM, Rosenbaum AL, Demer JL. Heterotopic muscle pulleys or oblique muscle dysfunction? J AAPOS 1998;2:17-25. 29. Romaine HH. Motility surgery. NY State J Med 1963;63:1511-4.
An Eye on the Arts – The Arts on the Eye
THE LAST RAYS of evening light are filtering through the window when Vishnu sees the image. A man is standing over his body on the landing down below. He kneels besides him, and pulls back the sheet. With one hand, the man touches Vishnu’s cheek; with the other, he presses the forehead and brushes the wisps of hair off the eyes. Fingertips trace across Vishnu’s lips, then down his chin, and to his chest, where they rub against his heart. The man has his eyes closed. His neck is arched, head tilted upwards, lips reciting silent words. Vishnu has seen this silhouette before, he knows he should recognize the crouching figure. The man’s eyes open. Their whiteness reaches through the dark. They are large and milky, staring up through the air, through the ceiling, through the stone, at some point outside in the sky. Vishnu looks at them and is unsure if they are filled with reverence or fear. The eyes blink, the fingers caress the tufts of chest hair, the lips open and close. Soft words float slowly up from the upturned face. Vishnu sees the gray hair, sees the bulbous nose, sees the pockmarks on the cheeks. Recognition floods in finally. He peers down at Mr. Jalal on the landing, crouching next to his body, staring up through the darkness towards heaven.—Manil Suri (from The Death of Vishnu, HarperCollins)