Acquired Nonparalytic Causes of Superior Oblique Dysfunction Gill Roper-Hall, D.B.O.T., C.O., C.O.M.T. Oscar A. Cruz, M.D. Sophia M. Chung, M.D.
ABSTRACT Background and Purpose: To conduct a retrospective study to investigate the causes of acquired superior oblique dysfunction, excluding paralysis, in a consecutive series of adult patients and to compare presenting symptoms and clinical findings. Methods: A retrospective review of all adult patients with superior oblique dysfunction between the ages of 18 and 80 who met the study profile was conducted at Saint Louis University Medical Center between January 2000 and April 2012. The presenting symptoms, clinical findings, and treatment course for each patient was recorded. The study was approved by the Institutional Review Board of our institution. Results: Acquired forms of nonparalytic superior oblique dysfunction were identified in forty-eight patients. These included superior oblique myokymia (twenty-three patients), superior oblique click syndrome or variable Brown syndrome (nine), canine tooth syndrome (five), spontaneous acquired Brown syndrome (four), iatrogenic or traumatic Brown syndrome (four), and ocular neuromyotonia affecting the superior oblique (three). Conclusions: Several nonparalytic entities were identified that caused superior oblique dysfunction. Clinical findings may be similar despite entirely different mechanisms. Subjective symptoms may be difficult for the patient to describe or for the examiner to elicit on the day of the examination. Specific techniques can be used in eliciting, differentiating, and documenting the conditions. These included trochlear palpation, modified head tilt technique, interpretation of torsion, and Hess charts.
INTRODUCTION
Requests for reprints should be addressed to: Gill RoperHall, D.B.O.T., C.O., C.O.M.T., Department of Ophthalmology, Saint Louis University Medical Center, 1755 S. Grand Blvd., St. Louis, MO 63131; e-mail: [email protected]
Cyclovertical diplopia caused by acquired superior oblique dysfunction, excluding fourth cranial nerve palsy, encompasses an interesting range of clinical entities. These include syndromes caused
© 2014 Board of Regents of the University of Wisconsin System, American Orthoptic Journal, Volume 64, 2014, ISSN 0065-955X, E-ISSN 1553-4448
American Orthoptic Journal
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by mechanical influences in which the superior oblique is impeded in its passage through the trochlea following disease or injury such as acquired forms of Brown, superior oblique click, and canine tooth syndromes.1-3 Neurophysiologic mechanisms causing conditions such as myokymia or myotonia can affect the smooth conduction of nervous impulses. The trochlear nerve is the only ocular motor cranial nerve affected by myokymia.4 Ocular neuromyotonia (ONM) can affect any ocular nerve or muscle, including the superior oblique.5 Diplopia can be intermittent or episodic in entities that affect the superior oblique and the description often raises concern for ocular myasthenia. This may be further misleading if the diplopia is absent on the day of the examination and cannot be elicited during testing. Some of the mechanical disorders can present with symptoms mimicking muscle paralysis, such an apparent inferior oblique palsy in Brown syndrome, or similar intermittent or episodic diplopia described by patients with neurologic entities such as superior oblique myokymia. Clinical findings may be similar despite entirely different mechanisms. Subjective symptoms in these conditions are sometimes difficult for the patient to describe or for the examiner to elicit on the day of the examination. Specific examination techniques can be used in differential diagnosis and these are described.
thyroid eye disease, orbital fracture, and myasthenia gravis. The presenting symptoms, clinical findings, and treatment course for each patient were recorded. The study was approved by the Institutional Review Board of our institution. All patients underwent full orthoptic and ophthalmic evaluation with particular attention to the function of the superior oblique muscle in its field of action on depression-in-adduction, but also on elevation-in-adduction, the gaze direction where the muscle should be fully relaxed as it slides through the trochlea. Hess charts were helpful in the differential diagnosis. Medical and neurological and neuroradiological work-up was performed as appropriate. RESULTS Acquired forms of nonparalytic superior oblique dysfunction were identified in forty-eight patients. There were twenty-eight women and twenty men with ages ranging from 18 to 79 (48.6 ± 16.5). The conditions included superior oblique myokymia (twenty-three patients), superior oblique click syndrome or variable Brown syndrome (nine), canine tooth syndrome (five), spontaneous acquired Brown syndrome (four), iatrogenic or traumatic Brown syndrome (four), and ocular neuromyotonia affecting the superior oblique (three) (Table). DISCUSSION
STUDY DESIGN AND METHODS A retrospective review of all adult patients with superior oblique dysfunction between the ages of 18 and 80 who met the study profile was conducted at Saint Louis University Medical Center between January 2000 and April 2012. Exclusion criteria were congenital or longstanding conditions, trochlear nerve paralysis, associated
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Acquired nonparalytic disorders of the superior oblique can be broadly divided into neurologic and mechanical causes. Neurologic Causes of Superior Oblique Dysfunction Superior oblique function can be interrupted by neurophysiologic mechanisms
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TABLE TYPES OF NONPARALYTIC CAUSES OF ACQUIRED SUPERIOR OBLIQUE DYSFUNCTION Acquired Superior Oblique Dysfunction SO myokymia SO Click or variable Brown syndrome Canine Tooth syndrome Spontaneously acquired Brown syndrome Iatrogenic or traumatic Brown syndrome Ocular neuromyotonia Total
23 9 5 4 4 3 48
that affect the normal contraction of the muscle. These include clinical entities such as myokymia and neuromyotonia. The superior oblique is the only muscle innervated by the trochlear nerve. The nerve is susceptible to trauma and paralysis from other causes not discussed within the scope of this paper. However, it is the only cranial nerve in which dysfunction causing myokymia has been reported. This entity is not described in other extraocular muscles.4, 6, 7
the most common finding. An additional twelve patients not included in the study were referred, examined, and diagnosed with suspected SOM, but the episodes were not elicited or observed during the examination. There is a spectrum of involvement in patients with SOM. In a series of six patients studied by Roper-Hall and Burde in 1978,8 it was noted that individual patients displayed different amplitudes and frequencies of oscillation and the timing and duration of the episodes also varied among individuals. Some displayed almost pure vertical diplopia whereas others described a torsional component; however, the pattern remained the same in each patient. This was also true for patients with SOM in the current series. Another observation in the previously reported and current series of patients was the occasional finding of a small superior oblique weakness during the resting phase. A minimal hypertropia of the affected eye switched to a hypotropia during an episode of SOM.8
Superior Oblique Myokymia Testing Techniques of SOM Superior oblique myokymia (SOM) is a relatively rare, frequently undiagnosed ocular condition. Hoyt and Keane published the first series in 1970, although a few isolated cases were reported earlier.4 It is usually unilateral and characterized by brief recurrent episodes presenting with visual symptoms accompanied by physical ocular sensations. The most common description is of intermittent diplopia, either vertical, torsional or a combination, usually associated with oscillopsia with the image of one eye perceived to be jumping or shimmering. There is often an accompanying physical sensation that the eye is twitching or jumping synchronously with the visual movement.4, 6-8 Twenty-three cases of SOM were identified in our study, making this entity
American Orthoptic Journal
Patients with suspected myokymia may be examined by looking closely at conjunctival vessels, iris or tear film of the affected eye. If no movement is seen unaided, a magnifying lens, slit lamp microscope or ophthalmoscope may be used to verify fine oscillations. The eye is first viewed in primary gaze and again when the eye moves quickly into the field of action of the superior oblique. Alternate cover testing with the affected eye in depression-in-adduction may provide enough dissociation to bring out the oscillations. Tilting the head to the side of the suspected superior oblique at the same time asking the patient to move that eye quickly downward and inward may trigger an episode.
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Management of SOM
Testing Techniques of ONM
Most cases of superior oblique myokymia respond well to membrane stabilizing agents such as gabapentin, carbamazepine, and phenytoin. Some patients go into remission either spontaneously or when medications are tapered or discontinued. In our series, 19 of 23 observed cases of SOM were treated successfully with medications. Some patients continued their follow-up care with the referring physician and the outcome is unknown. Neuroradiologic evaluation is not generally indicated as the yield for cranial pathology is low in myokymia. Infrequently, extraocular muscle surgery is indicated for SOM. Simultaneous weakening of the inferior and superior oblique muscles of the affected eye has been reported with reasonable relief of symptoms.4, 6
When the superior oblique is affected by ONM, a sudden hypotropia will be noted lasting seconds to a few minutes, recurring several times an hour. It may be triggered by looking downward, or into the field of action of the superior oblique. It may be accompanied by exotropia and incyclotorsion, the secondary actions of the superior oblique. Assessing torsion during an episode can be helpful in confirming that it is the superior oblique and not the inferior rectus muscle undergoing sustained contraction.10 Patients may display a small hypertropia of the affected eye in the resting phase between episodes. This was noted in several patients in this series and by other authors.8, 11 In ONM, as seen in SOM, there is a spectrum among patients in the frequency, amplitude of excursion, duration, and recovery of the ocular disturbance, but the sustained contractions in ONM are much larger and more dramatic. In SOM, there is an irregular but rhythmic pattern during an episode; in ONM, there is one sustained contraction lasting seconds to minutes. In a previously reported case by the same authors, a patient first presented with classic SOM and at the next visit had developed a much different clinical picture diagnosed as ONM.10 This may suggest that the two conditions form part of a larger clinical spectrum, with similar mechanisms, particularly in the idiopathic cases of ONM. This questions the mechanism underlying both conditions. ONM has been reported to be due to ephaptic transmission in which there is lateral contact between nerve fibers across which impulses may be transmitted directly through the cell membranes rather than across a synapse.12 It has been reported as the mechanism involved in facial nerve disorders, epilepsy, neuromyotonia, ONM, and superior
Ocular Neuromyotonia The term ocular neuromyotonia (ONM) was first coined by Ricker and Mertens in 1970 and employed again by Papst in 1972, although there are earlier published descriptions of sporadic cases.5, 9 ONM is a rare but distinctive clinical entity characterized by involuntary episodic ocular deviations accompanied by diplopia. Its mechanism is not well understood. It may present with mild to severe symptoms. It can affect any nerve or muscle, and thus is not unique to the superior oblique, but the ocular behavior during an episode follows the same unique pattern in each patient. It is usually unilateral.10 Three patients in this series presented with ONM affecting the superior oblique. Two responded to membrane stabilizing medications; the third patient was on medications for an unrelated condition, and additional treatment for ONM was contraindicated. These cases are reported in more detail elsewhere.10
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oblique myokymia.13 Ephaptic transmission has been reported to occur with vascular compression at the nerve root.14, 15 It has been suggested that the mechanism causing ONM is due to a channelopathy causing acquired disruption of ion channels in the neuronal cell membrane as seen in systemic neuromyotonia.12 These channelopathies may result from autoimmune influences. This is an exciting new area of research. Management of ONM Prisms and extraocular muscle surgery are not indicated in patients with ONM unless there is an underlying ocular deviation in the resting phase between episodes. Patients may be taught to avoid the gaze direction where the muscle contraction is triggered, or to look in the opposite gaze direction to stretch or relieve the muscle contraction during an episode.16 Patients with ONM may be prescribed the same membrane stabilizing agents used to treat SOM such as gabapentin, carbamazepine, and phenytoin. Topical beta-blockers have been used with some success. ONM has been reported following radiation to the skull base and after prophylactic cranial radiation.17 Many cases of ONM are idiopathic, and others have been described in thyroid eye disease.18 If the cause has not been determined, patients with ONM should be referred for neurologic and neuroradiologic evaluation. Mechanical Causes of Superior Oblique Dysfunction The composition of the superior oblique is anatomically more tendon than muscle and can develop inflammation causing tendonitis. The trochlea is a unique structure and can be damaged by trauma, including iatrogenic complications in planned surgical procedures on adjacent structures, such as the sinuses.
American Orthoptic Journal
FIGURE 1: Photograph showing restriction on right up-gaze of the left eye caused by traumatic injury to the trochlea. (Photo courtesy of author.)
Acquired Brown Syndrome Spontaneously acquired Brown syndrome can occur as a result of inflammation or from direct trauma to the trochlea. The tendon is unable to move through the trochlea, and the eye is restricted on elevation-in-adduction, the field of action of the inferior oblique muscle. Unless attention is given to the history and unique clinical findings surrounding the onset, the condition may be misdiagnosed. The restriction is usually nonvariable resembling the familiar Brown syndrome seen in childhood (Figure 1 and 2).1 Intermittent Brown Syndrome In some cases, the trochlea is affected by the same mechanisms noted above, but the superior oblique retains its ability to move through the trochlea despite being intermittently impeded in its passage. This causes symptoms with variable ocular limitation and subjective changes in diplopia. It may be absent at times, or become restricted in the field of action of the inferior oblique. Superior Oblique Click Syndrome The superior oblique click syndrome is a related condition in which a physical sensation is reported, often with a click, as the
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FIGURE 2: Hess chart of same patient confirming the marked restriction (plotted as patient sees it).
FIGURE 3: Hess chart of a patient with superior oblique click syndrome affecting the left eye. Note variability on right up-gaze on attempted elevation-in-adduction.
tendon “catches” as it passes through the trochlea. It may resemble Brown syndrome with a pseudo inferior oblique weakness on up-gaze or a superior oblique palsy on down-gaze depending on the direction in which the movement of the tendon is impeded. The click is felt by the patient and may be audible to both the patient and observer. Both these acquired presentations are likely to be inflammatory in origin. The term click syndrome was first coined by Roper-Hall and Roper-Hall in 1972 (Figure 3).3 Canine Tooth Syndrome In this condition, there is inability to elevate or depress the eye normally when
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it is in the adducted position. This was first described by Knapp in 1974 in his Scobee Lecture on classification of superior oblique palsies. There is an ipsilateral Brown syndrome with an apparent superior oblique palsy (Class VII).2 This is due to trochlear damage caused by inflammation, or injuries such as a dog bite, in which normal passage of the superior oblique tendon through the trochlea is impeded. Five patients in our study had canine tooth syndrome, two from trauma, two from inflammation or scarring, and one from a presumed longstanding Brown syndrome whose restriction began to move more freely after an intense 7-hour period using a laptop. He developed variable dip-
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FIGURE 4: Hess chart of a patient with canine tooth syndrome in the right eye. Note restriction of both up-gaze and down-gaze in the adducted position.
lopia on down-gaze and was referred to rule out ocular myasthenia. Two others were referred with presumptive diagnoses of acquired fourth cranial nerve paralysis. Limitation in the field of action of the inferior and superior oblique muscles consistent with canine tooth syndrome was documented after formal measurements and Hess charts (Figure 4). Four patients underwent a resect-recess procedure on the contralateral inferior rectus muscle with relief of diplopia on down-gaze.19, 20 The remaining patient prefers to use a compensatory head posture while considering surgery. Examination Techniques for Mechanical Causes All patients should undergo formal orthoptic and ophthalmologic evaluation. Familiarity with these entities and taking a careful history can help narrow the diagnosis in many cases. Hess or Lancaster charts are helpful in the differential diagnosis. Patients are encouraged to bring videos or photographs of the affected eye during an episode. In suspected cases of acquired Brown syndrome, some variability may be seen or actual resistance felt or heard by the patient. Palpation of the trochlear area
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FIGURE 5: Photograph showing technique to palpate the trochlear area to test for point tenderness. (Photo courtesy of author.)
with the tip of the examiner’s thumb or finger can often reveal point tenderness, consistent with an inflammatory process (Figure 5). It is possible, on occasion, to feel the nodule as it passes and even assist its progress through the trochlea. Forced duction testing can be helpful in confirming, or even relieving, a restriction of the affected eye as it attempts to elevate in adduction. Plotting Hess or Lancaster charts may be helpful. These charts may document variability in the field of action of either the inferior or superior oblique depending on whether the superior oblique tendon becomes impeded as the eye moves up or down. In cases of superior oblique click syndrome, it may “catch” as it moves in either direction alternating between hypertropia resembling a superior oblique under-action, or hypotropia with apparent pseudoparesis of the inferior oblique (Figure 3).3
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Management of Superior Oblique Dysfunction from Mechanical Causes In the presence of trochlear inflammation, oral corticosteroids, or nonsteroidal anti-inflammatory oral agents such as naproxyn, can be prescribed. An injection of Kenalog ® (triamcinolone) into the trochlear area may be given in refractory cases. Many cases of acquired Brown syndrome resolve spontaneously, and conservative observation is indicated. Some become permanent. In other reported cases, longstanding restriction may resolve. Surgical intervention in the trochlear area or on the affected superior oblique is occasionally justified, but may be unpredictable and cause further scarring or inflammation. Recession of the contralateral superior rectus muscle may be considered. In canine tooth syndrome, performing a fadenoperation or resect-recess procedure on the contralateral inferior rectus muscle relieves diplopia on down-gaze.20, 21 CONCLUSIONS In this study, several clinical conditions were identified that caused superior oblique dysfunction. Clinical findings may be similar despite entirely different mechanisms. Because many of the conditions are intermittent or episodic, they are susceptible to initial misdiagnosis. Subjective symptoms in these entities are sometimes difficult for the patient to describe or for the examiner to elicit on the day of the examination. Longer periods of observation in the clinic are necessary in these unusual entities because an episode may be missed if the examination is cursory. Specific techniques can be used in differential diagnosis. Continued exposure to descriptions of SOM, ONM, and superior oblique click syndrome in the literature may have contributed to the increased frequency of reported cases. The advent of cell phone cam-
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eras to demonstrate an ocular deviation, or capture a brief episode of an abnormal eye movement occurring intermittently at home or in the clinic, has also helped in the differential diagnosis of these conditions previously considered rare. REFERENCES 1. Brown HW: Congenital structural motor anomalies in strabismus. In: Allen JH, ed. Strabismus Ophthalmic Symposium 1. St. Louis: CV Mosby Co.; 1950, pp. 205-236. 2. Knapp P: Classification and treatment of superior oblique palsy. Am Orthopt J 1974; 24:18-22. 3. Roper- Hall MJ, Roper- Hall G: The superior oblique “click” syndrome. In: Proceedings of the 2nd International Orthoptic Congress. Amsterdam: Excerpta Medica; 1972, pp. 360-366. 4. Hoyt WF, Keane JR: Superior oblique myokymia. Arch Ophthalmol 1970; 84:461-467. 5. Ricker VK, Mertens HG: Okulare neuromyotonie. Klin Monatsbl Augenheilkd 1970; 156:837-842. 6. Susac JO, Smith JL, Schatz NJ: Superior oblique myokymia. Arch Neurol 1973; 29:432-434. 7. Leigh RJ, Zee DS, eds. The Neurology of Eye Movements, 4th ed. New York: Oxford University Press; 2006, pp. 426-427. 8. Roper-Hall G, Burde RM: Superior oblique myokymia. Am Orthopt J 1978; 28:58-63. 9. Papst W: Zür differentialdiagnose der okulären neuromyotonie. Ophthalmologica 1972; 164:252263. 10. Roper-Hall G, Chung SM, Cruz OA: Ocular neuromyotonia: Differential diagnosis and treatment. Strabismus 2013; 26:131-136. 11. McMain K, Parkinson J, Maxner C, LaRoche R: Case report: Ocular neuromyotonia. Am Orthopt J 2000; 50:120-125. 12. Leigh RJ, Zee DS, eds. The Neurology of Eye Movements. pp. 437-438. 13. Vighetto A, Tilikete C: Les syndromes oculomoteurs par hyperactivité neurogène et leur traitement. Neurochirurgie 2009; 55:272-278. 14. Tilikete C, Vial C, Niederlaender M, Bonnier PL, Vighetto A: Idiopathic ocular neuromyotonia: A neurovascular compression syndrome? J Neurol Neurosurg Psychiatry 2000; 69:642-644. 15. Versino M, Colnaghi S, Todeschini A, Candeloro E, et al.: Ocular neuromyotonia with both tonic and paroxysmal components due to vascular compression. J Neurol 2005: 252:227-229. 16. Safran AB, Magistris M: Terminating attacks of ocular neuromyotonia. J Neuroophthalmol 1998; 18:47-48.
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17. Miller NR, Lee AG: Adult-onset acquired oculomotor nerve paresis with cyclic spasms: Relationship to ocular neuromyotonia. Am J Ophthalmol 2004; 137:70-76. 18. Chung SM, Lee AG, Holds JB, Roper-Hall G, Cruz OA: Ocular neuromyotonia in Graves dysthyroid orbitopathy. Arch Ophthalmol 1997; 115:365-370. 19. Scott AB: Posterior fixation: Adjustable and without posterior sutures. In: Lennerstrand G, ed. Update on Strabismus and Pediatric Ophthalmology. Boca Raton, FL: CRC Press; 1994, pp. 399-401. 20. Roper-Hall G, Cruz OA: Results of combined resection-recession on a single rectus muscle for
American Orthoptic Journal
incomitant deviations. Submitted for publication—under review. 21. Cuppers C: The so-called fadenoperation: Surgical corrections by small-defined changes of the arc of contact. In: Fells P, ed. Transactions Second Congress of the International Strabismological Association. Marseille: Diffusion Generale de Librairie; 1976, p. 395.
Key words: superior oblique, Brown syndrome, superior oblique myokymia, superior oblique click syndrome, canine tooth syndrome, ocular neuromyotonia
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ABSTRACT Background and Purpose: To conduct a retrospective study to investigate the causes of acquired superior oblique dysfunction, excluding paralysis, in a consecutive series of adult patients and to compare presenting symptoms and clinical findings. Methods: A retrospective review of all adult patients with superior oblique dysfunction between the ages of 18 and 80 who met the study profile was conducted at Saint Louis University Medical Center between January 2000 and April 2012. The presenting symptoms, clinical findings, and treatment course for each patient was recorded. The study was approved by the Institutional Review Board of our institution. Results: Acquired forms of nonparalytic superior oblique dysfunction were identified in forty-eight patients. These included superior oblique myokymia (twenty-three patients), superior oblique click syndrome or variable Brown syndrome (nine), canine tooth syndrome (five), spontaneous acquired Brown syndrome (four), iatrogenic or traumatic Brown syndrome (four), and ocular neuromyotonia affecting the superior oblique (three). Conclusions: Several nonparalytic entities were identified that caused superior oblique dysfunction. Clinical findings may be similar despite entirely different mechanisms. Subjective symptoms may be difficult for the patient to describe or for the examiner to elicit on the day of the examination. Specific techniques can be used in eliciting, differentiating, and documenting the conditions. These included trochlear palpation, modified head tilt technique, interpretation of torsion, and Hess charts.
INTRODUCTION
Requests for reprints should be addressed to: Gill RoperHall, D.B.O.T., C.O., C.O.M.T., Department of Ophthalmology, Saint Louis University Medical Center, 1755 S. Grand Blvd., St. Louis, MO 63131; e-mail: [email protected]
Cyclovertical diplopia caused by acquired superior oblique dysfunction, excluding fourth cranial nerve palsy, encompasses an interesting range of clinical entities. These include syndromes caused
© 2014 Board of Regents of the University of Wisconsin System, American Orthoptic Journal, Volume 64, 2014, ISSN 0065-955X, E-ISSN 1553-4448
American Orthoptic Journal
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by mechanical influences in which the superior oblique is impeded in its passage through the trochlea following disease or injury such as acquired forms of Brown, superior oblique click, and canine tooth syndromes.1-3 Neurophysiologic mechanisms causing conditions such as myokymia or myotonia can affect the smooth conduction of nervous impulses. The trochlear nerve is the only ocular motor cranial nerve affected by myokymia.4 Ocular neuromyotonia (ONM) can affect any ocular nerve or muscle, including the superior oblique.5 Diplopia can be intermittent or episodic in entities that affect the superior oblique and the description often raises concern for ocular myasthenia. This may be further misleading if the diplopia is absent on the day of the examination and cannot be elicited during testing. Some of the mechanical disorders can present with symptoms mimicking muscle paralysis, such an apparent inferior oblique palsy in Brown syndrome, or similar intermittent or episodic diplopia described by patients with neurologic entities such as superior oblique myokymia. Clinical findings may be similar despite entirely different mechanisms. Subjective symptoms in these conditions are sometimes difficult for the patient to describe or for the examiner to elicit on the day of the examination. Specific examination techniques can be used in differential diagnosis and these are described.
thyroid eye disease, orbital fracture, and myasthenia gravis. The presenting symptoms, clinical findings, and treatment course for each patient were recorded. The study was approved by the Institutional Review Board of our institution. All patients underwent full orthoptic and ophthalmic evaluation with particular attention to the function of the superior oblique muscle in its field of action on depression-in-adduction, but also on elevation-in-adduction, the gaze direction where the muscle should be fully relaxed as it slides through the trochlea. Hess charts were helpful in the differential diagnosis. Medical and neurological and neuroradiological work-up was performed as appropriate. RESULTS Acquired forms of nonparalytic superior oblique dysfunction were identified in forty-eight patients. There were twenty-eight women and twenty men with ages ranging from 18 to 79 (48.6 ± 16.5). The conditions included superior oblique myokymia (twenty-three patients), superior oblique click syndrome or variable Brown syndrome (nine), canine tooth syndrome (five), spontaneous acquired Brown syndrome (four), iatrogenic or traumatic Brown syndrome (four), and ocular neuromyotonia affecting the superior oblique (three) (Table). DISCUSSION
STUDY DESIGN AND METHODS A retrospective review of all adult patients with superior oblique dysfunction between the ages of 18 and 80 who met the study profile was conducted at Saint Louis University Medical Center between January 2000 and April 2012. Exclusion criteria were congenital or longstanding conditions, trochlear nerve paralysis, associated
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Acquired nonparalytic disorders of the superior oblique can be broadly divided into neurologic and mechanical causes. Neurologic Causes of Superior Oblique Dysfunction Superior oblique function can be interrupted by neurophysiologic mechanisms
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TABLE TYPES OF NONPARALYTIC CAUSES OF ACQUIRED SUPERIOR OBLIQUE DYSFUNCTION Acquired Superior Oblique Dysfunction SO myokymia SO Click or variable Brown syndrome Canine Tooth syndrome Spontaneously acquired Brown syndrome Iatrogenic or traumatic Brown syndrome Ocular neuromyotonia Total
23 9 5 4 4 3 48
that affect the normal contraction of the muscle. These include clinical entities such as myokymia and neuromyotonia. The superior oblique is the only muscle innervated by the trochlear nerve. The nerve is susceptible to trauma and paralysis from other causes not discussed within the scope of this paper. However, it is the only cranial nerve in which dysfunction causing myokymia has been reported. This entity is not described in other extraocular muscles.4, 6, 7
the most common finding. An additional twelve patients not included in the study were referred, examined, and diagnosed with suspected SOM, but the episodes were not elicited or observed during the examination. There is a spectrum of involvement in patients with SOM. In a series of six patients studied by Roper-Hall and Burde in 1978,8 it was noted that individual patients displayed different amplitudes and frequencies of oscillation and the timing and duration of the episodes also varied among individuals. Some displayed almost pure vertical diplopia whereas others described a torsional component; however, the pattern remained the same in each patient. This was also true for patients with SOM in the current series. Another observation in the previously reported and current series of patients was the occasional finding of a small superior oblique weakness during the resting phase. A minimal hypertropia of the affected eye switched to a hypotropia during an episode of SOM.8
Superior Oblique Myokymia Testing Techniques of SOM Superior oblique myokymia (SOM) is a relatively rare, frequently undiagnosed ocular condition. Hoyt and Keane published the first series in 1970, although a few isolated cases were reported earlier.4 It is usually unilateral and characterized by brief recurrent episodes presenting with visual symptoms accompanied by physical ocular sensations. The most common description is of intermittent diplopia, either vertical, torsional or a combination, usually associated with oscillopsia with the image of one eye perceived to be jumping or shimmering. There is often an accompanying physical sensation that the eye is twitching or jumping synchronously with the visual movement.4, 6-8 Twenty-three cases of SOM were identified in our study, making this entity
American Orthoptic Journal
Patients with suspected myokymia may be examined by looking closely at conjunctival vessels, iris or tear film of the affected eye. If no movement is seen unaided, a magnifying lens, slit lamp microscope or ophthalmoscope may be used to verify fine oscillations. The eye is first viewed in primary gaze and again when the eye moves quickly into the field of action of the superior oblique. Alternate cover testing with the affected eye in depression-in-adduction may provide enough dissociation to bring out the oscillations. Tilting the head to the side of the suspected superior oblique at the same time asking the patient to move that eye quickly downward and inward may trigger an episode.
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Management of SOM
Testing Techniques of ONM
Most cases of superior oblique myokymia respond well to membrane stabilizing agents such as gabapentin, carbamazepine, and phenytoin. Some patients go into remission either spontaneously or when medications are tapered or discontinued. In our series, 19 of 23 observed cases of SOM were treated successfully with medications. Some patients continued their follow-up care with the referring physician and the outcome is unknown. Neuroradiologic evaluation is not generally indicated as the yield for cranial pathology is low in myokymia. Infrequently, extraocular muscle surgery is indicated for SOM. Simultaneous weakening of the inferior and superior oblique muscles of the affected eye has been reported with reasonable relief of symptoms.4, 6
When the superior oblique is affected by ONM, a sudden hypotropia will be noted lasting seconds to a few minutes, recurring several times an hour. It may be triggered by looking downward, or into the field of action of the superior oblique. It may be accompanied by exotropia and incyclotorsion, the secondary actions of the superior oblique. Assessing torsion during an episode can be helpful in confirming that it is the superior oblique and not the inferior rectus muscle undergoing sustained contraction.10 Patients may display a small hypertropia of the affected eye in the resting phase between episodes. This was noted in several patients in this series and by other authors.8, 11 In ONM, as seen in SOM, there is a spectrum among patients in the frequency, amplitude of excursion, duration, and recovery of the ocular disturbance, but the sustained contractions in ONM are much larger and more dramatic. In SOM, there is an irregular but rhythmic pattern during an episode; in ONM, there is one sustained contraction lasting seconds to minutes. In a previously reported case by the same authors, a patient first presented with classic SOM and at the next visit had developed a much different clinical picture diagnosed as ONM.10 This may suggest that the two conditions form part of a larger clinical spectrum, with similar mechanisms, particularly in the idiopathic cases of ONM. This questions the mechanism underlying both conditions. ONM has been reported to be due to ephaptic transmission in which there is lateral contact between nerve fibers across which impulses may be transmitted directly through the cell membranes rather than across a synapse.12 It has been reported as the mechanism involved in facial nerve disorders, epilepsy, neuromyotonia, ONM, and superior
Ocular Neuromyotonia The term ocular neuromyotonia (ONM) was first coined by Ricker and Mertens in 1970 and employed again by Papst in 1972, although there are earlier published descriptions of sporadic cases.5, 9 ONM is a rare but distinctive clinical entity characterized by involuntary episodic ocular deviations accompanied by diplopia. Its mechanism is not well understood. It may present with mild to severe symptoms. It can affect any nerve or muscle, and thus is not unique to the superior oblique, but the ocular behavior during an episode follows the same unique pattern in each patient. It is usually unilateral.10 Three patients in this series presented with ONM affecting the superior oblique. Two responded to membrane stabilizing medications; the third patient was on medications for an unrelated condition, and additional treatment for ONM was contraindicated. These cases are reported in more detail elsewhere.10
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oblique myokymia.13 Ephaptic transmission has been reported to occur with vascular compression at the nerve root.14, 15 It has been suggested that the mechanism causing ONM is due to a channelopathy causing acquired disruption of ion channels in the neuronal cell membrane as seen in systemic neuromyotonia.12 These channelopathies may result from autoimmune influences. This is an exciting new area of research. Management of ONM Prisms and extraocular muscle surgery are not indicated in patients with ONM unless there is an underlying ocular deviation in the resting phase between episodes. Patients may be taught to avoid the gaze direction where the muscle contraction is triggered, or to look in the opposite gaze direction to stretch or relieve the muscle contraction during an episode.16 Patients with ONM may be prescribed the same membrane stabilizing agents used to treat SOM such as gabapentin, carbamazepine, and phenytoin. Topical beta-blockers have been used with some success. ONM has been reported following radiation to the skull base and after prophylactic cranial radiation.17 Many cases of ONM are idiopathic, and others have been described in thyroid eye disease.18 If the cause has not been determined, patients with ONM should be referred for neurologic and neuroradiologic evaluation. Mechanical Causes of Superior Oblique Dysfunction The composition of the superior oblique is anatomically more tendon than muscle and can develop inflammation causing tendonitis. The trochlea is a unique structure and can be damaged by trauma, including iatrogenic complications in planned surgical procedures on adjacent structures, such as the sinuses.
American Orthoptic Journal
FIGURE 1: Photograph showing restriction on right up-gaze of the left eye caused by traumatic injury to the trochlea. (Photo courtesy of author.)
Acquired Brown Syndrome Spontaneously acquired Brown syndrome can occur as a result of inflammation or from direct trauma to the trochlea. The tendon is unable to move through the trochlea, and the eye is restricted on elevation-in-adduction, the field of action of the inferior oblique muscle. Unless attention is given to the history and unique clinical findings surrounding the onset, the condition may be misdiagnosed. The restriction is usually nonvariable resembling the familiar Brown syndrome seen in childhood (Figure 1 and 2).1 Intermittent Brown Syndrome In some cases, the trochlea is affected by the same mechanisms noted above, but the superior oblique retains its ability to move through the trochlea despite being intermittently impeded in its passage. This causes symptoms with variable ocular limitation and subjective changes in diplopia. It may be absent at times, or become restricted in the field of action of the inferior oblique. Superior Oblique Click Syndrome The superior oblique click syndrome is a related condition in which a physical sensation is reported, often with a click, as the
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FIGURE 2: Hess chart of same patient confirming the marked restriction (plotted as patient sees it).
FIGURE 3: Hess chart of a patient with superior oblique click syndrome affecting the left eye. Note variability on right up-gaze on attempted elevation-in-adduction.
tendon “catches” as it passes through the trochlea. It may resemble Brown syndrome with a pseudo inferior oblique weakness on up-gaze or a superior oblique palsy on down-gaze depending on the direction in which the movement of the tendon is impeded. The click is felt by the patient and may be audible to both the patient and observer. Both these acquired presentations are likely to be inflammatory in origin. The term click syndrome was first coined by Roper-Hall and Roper-Hall in 1972 (Figure 3).3 Canine Tooth Syndrome In this condition, there is inability to elevate or depress the eye normally when
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it is in the adducted position. This was first described by Knapp in 1974 in his Scobee Lecture on classification of superior oblique palsies. There is an ipsilateral Brown syndrome with an apparent superior oblique palsy (Class VII).2 This is due to trochlear damage caused by inflammation, or injuries such as a dog bite, in which normal passage of the superior oblique tendon through the trochlea is impeded. Five patients in our study had canine tooth syndrome, two from trauma, two from inflammation or scarring, and one from a presumed longstanding Brown syndrome whose restriction began to move more freely after an intense 7-hour period using a laptop. He developed variable dip-
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FIGURE 4: Hess chart of a patient with canine tooth syndrome in the right eye. Note restriction of both up-gaze and down-gaze in the adducted position.
lopia on down-gaze and was referred to rule out ocular myasthenia. Two others were referred with presumptive diagnoses of acquired fourth cranial nerve paralysis. Limitation in the field of action of the inferior and superior oblique muscles consistent with canine tooth syndrome was documented after formal measurements and Hess charts (Figure 4). Four patients underwent a resect-recess procedure on the contralateral inferior rectus muscle with relief of diplopia on down-gaze.19, 20 The remaining patient prefers to use a compensatory head posture while considering surgery. Examination Techniques for Mechanical Causes All patients should undergo formal orthoptic and ophthalmologic evaluation. Familiarity with these entities and taking a careful history can help narrow the diagnosis in many cases. Hess or Lancaster charts are helpful in the differential diagnosis. Patients are encouraged to bring videos or photographs of the affected eye during an episode. In suspected cases of acquired Brown syndrome, some variability may be seen or actual resistance felt or heard by the patient. Palpation of the trochlear area
American Orthoptic Journal
FIGURE 5: Photograph showing technique to palpate the trochlear area to test for point tenderness. (Photo courtesy of author.)
with the tip of the examiner’s thumb or finger can often reveal point tenderness, consistent with an inflammatory process (Figure 5). It is possible, on occasion, to feel the nodule as it passes and even assist its progress through the trochlea. Forced duction testing can be helpful in confirming, or even relieving, a restriction of the affected eye as it attempts to elevate in adduction. Plotting Hess or Lancaster charts may be helpful. These charts may document variability in the field of action of either the inferior or superior oblique depending on whether the superior oblique tendon becomes impeded as the eye moves up or down. In cases of superior oblique click syndrome, it may “catch” as it moves in either direction alternating between hypertropia resembling a superior oblique under-action, or hypotropia with apparent pseudoparesis of the inferior oblique (Figure 3).3
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Management of Superior Oblique Dysfunction from Mechanical Causes In the presence of trochlear inflammation, oral corticosteroids, or nonsteroidal anti-inflammatory oral agents such as naproxyn, can be prescribed. An injection of Kenalog ® (triamcinolone) into the trochlear area may be given in refractory cases. Many cases of acquired Brown syndrome resolve spontaneously, and conservative observation is indicated. Some become permanent. In other reported cases, longstanding restriction may resolve. Surgical intervention in the trochlear area or on the affected superior oblique is occasionally justified, but may be unpredictable and cause further scarring or inflammation. Recession of the contralateral superior rectus muscle may be considered. In canine tooth syndrome, performing a fadenoperation or resect-recess procedure on the contralateral inferior rectus muscle relieves diplopia on down-gaze.20, 21 CONCLUSIONS In this study, several clinical conditions were identified that caused superior oblique dysfunction. Clinical findings may be similar despite entirely different mechanisms. Because many of the conditions are intermittent or episodic, they are susceptible to initial misdiagnosis. Subjective symptoms in these entities are sometimes difficult for the patient to describe or for the examiner to elicit on the day of the examination. Longer periods of observation in the clinic are necessary in these unusual entities because an episode may be missed if the examination is cursory. Specific techniques can be used in differential diagnosis. Continued exposure to descriptions of SOM, ONM, and superior oblique click syndrome in the literature may have contributed to the increased frequency of reported cases. The advent of cell phone cam-
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eras to demonstrate an ocular deviation, or capture a brief episode of an abnormal eye movement occurring intermittently at home or in the clinic, has also helped in the differential diagnosis of these conditions previously considered rare. REFERENCES 1. Brown HW: Congenital structural motor anomalies in strabismus. In: Allen JH, ed. Strabismus Ophthalmic Symposium 1. St. Louis: CV Mosby Co.; 1950, pp. 205-236. 2. Knapp P: Classification and treatment of superior oblique palsy. Am Orthopt J 1974; 24:18-22. 3. Roper- Hall MJ, Roper- Hall G: The superior oblique “click” syndrome. In: Proceedings of the 2nd International Orthoptic Congress. Amsterdam: Excerpta Medica; 1972, pp. 360-366. 4. Hoyt WF, Keane JR: Superior oblique myokymia. Arch Ophthalmol 1970; 84:461-467. 5. Ricker VK, Mertens HG: Okulare neuromyotonie. Klin Monatsbl Augenheilkd 1970; 156:837-842. 6. Susac JO, Smith JL, Schatz NJ: Superior oblique myokymia. Arch Neurol 1973; 29:432-434. 7. Leigh RJ, Zee DS, eds. The Neurology of Eye Movements, 4th ed. New York: Oxford University Press; 2006, pp. 426-427. 8. Roper-Hall G, Burde RM: Superior oblique myokymia. Am Orthopt J 1978; 28:58-63. 9. Papst W: Zür differentialdiagnose der okulären neuromyotonie. Ophthalmologica 1972; 164:252263. 10. Roper-Hall G, Chung SM, Cruz OA: Ocular neuromyotonia: Differential diagnosis and treatment. Strabismus 2013; 26:131-136. 11. McMain K, Parkinson J, Maxner C, LaRoche R: Case report: Ocular neuromyotonia. Am Orthopt J 2000; 50:120-125. 12. Leigh RJ, Zee DS, eds. The Neurology of Eye Movements. pp. 437-438. 13. Vighetto A, Tilikete C: Les syndromes oculomoteurs par hyperactivité neurogène et leur traitement. Neurochirurgie 2009; 55:272-278. 14. Tilikete C, Vial C, Niederlaender M, Bonnier PL, Vighetto A: Idiopathic ocular neuromyotonia: A neurovascular compression syndrome? J Neurol Neurosurg Psychiatry 2000; 69:642-644. 15. Versino M, Colnaghi S, Todeschini A, Candeloro E, et al.: Ocular neuromyotonia with both tonic and paroxysmal components due to vascular compression. J Neurol 2005: 252:227-229. 16. Safran AB, Magistris M: Terminating attacks of ocular neuromyotonia. J Neuroophthalmol 1998; 18:47-48.
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17. Miller NR, Lee AG: Adult-onset acquired oculomotor nerve paresis with cyclic spasms: Relationship to ocular neuromyotonia. Am J Ophthalmol 2004; 137:70-76. 18. Chung SM, Lee AG, Holds JB, Roper-Hall G, Cruz OA: Ocular neuromyotonia in Graves dysthyroid orbitopathy. Arch Ophthalmol 1997; 115:365-370. 19. Scott AB: Posterior fixation: Adjustable and without posterior sutures. In: Lennerstrand G, ed. Update on Strabismus and Pediatric Ophthalmology. Boca Raton, FL: CRC Press; 1994, pp. 399-401. 20. Roper-Hall G, Cruz OA: Results of combined resection-recession on a single rectus muscle for
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incomitant deviations. Submitted for publication—under review. 21. Cuppers C: The so-called fadenoperation: Surgical corrections by small-defined changes of the arc of contact. In: Fells P, ed. Transactions Second Congress of the International Strabismological Association. Marseille: Diffusion Generale de Librairie; 1976, p. 395.
Key words: superior oblique, Brown syndrome, superior oblique myokymia, superior oblique click syndrome, canine tooth syndrome, ocular neuromyotonia
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