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DVD—a conceptual, clinical, and surgical overview
AAPOS Workshops DVD—a conceptual, clinical, and surgical overview Alex Christoff, BS, CO,a,* Edward L. Raab, MD, JD,b,* David L. Guyton, MD,a Michael C. Brodsky, MD,c Katherine J. Fray, BS, CO,d Kimberly Merrill, BS, CO,e Claire C. Hennessey, BS, CO,f Erick D. Bothun, MD,e,g and David G. Morrison, MDh SUMMARY
Dissociated vertical deviation (DVD) is a slow, disconjugate hypertropic deviation of a nonfixating eye. It is usually bilateral, asymmetrical, and often associated with congenital esotropia. The deviating eye elevates, abducts, and excyclotorts. This type of strabismus is often variable, making measurement and clinical quantification difficult. Specific knowledge of the mechanisms and characteristics of the dissociated deviation are required for proper assessment and effective treatment. There is currently no consensus on the mechanisms and pathophysiology of DVD. In this workshop, participants discuss the characteristics and most current methods for assessing and quantifying the deviation and explore the potential etiologies, clinical characteristics, and indications for surgical intervention and nonsurgical management of DVD. ( J AAPOS 2014;18:378-384)
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issociated vertical deviation (DVD) is recognized by clinicians as a slow, disconjugate hypertropic deviation of a nonfixating eye. It is usually bilateral, asymmetrical, and often associated with congenital esotropia. The deviating eye elevates, abducts, and excyclotorts. “Dissociated strabismus complex” is a more inclusive term for this entity. This type of strabismus is often variable, making measurement and clinical quantification difficult. There is currently no consensus on the mechanism and pathophysiology of DVD. Understanding the potential etiology, clinical characteristics, and indications for surgical intervention should help the reader gain a better insight into the proper way to assess and treat, both surgically and nonsurgically, dissociated deviations. This workshop begins with two of the most widely known concepts of the etiology of DVD, presented by their respective proponents. Three certified orthoptists then discuss measure-
Author affiliations: aThe Krieger Children’s Eye Center at the Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland; bDepartments of Ophthalmology and Pediatrics, Icahn School of Medicine at Mount Sinai, New York; cDepartment of Ophthalmology and Neurology, Mayo Clinic, Rochester, Minnesota; dUniversity of Arkansas Medical Center and Arkansas Children’s Hospital, Little Rock, Arkansas; eDepartments of Ophthalmology and Visual Neurosciences, University of Minnesota, Minneapolis, Minnesota; f Children’s Eye Center of South Texas, San Antonio, Texas; gDeparment of Pediatrics, University of Minnesota, Minneapolis, Minnesota; hDepartments of Ophthalmology and Pediatrics, Vanderbilt University, Nashville, Tennessee Presented at the 39th Annual Meeting of the American Association for Pediatric Ophthalmology and Strabismus, Boston, Massachusetts, April 3-7, 2013. * These authors contributed equally to this publication as joint principal authors, co-organizers, and comoderators of the workshop. Submitted December 2, 2013. Revision accepted March 23, 2014. Correspondence: Alex Christoff, BS, CO, Assistant Professor of Ophthalmology, The Krieger Children’s Eye Center at the Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, MD 21287-902 Copyright Ó 2014 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/$36.00 http://dx.doi.org/10.1016/j.jaapos.2014.03.009
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ment techniques and nonsurgical treatment options and provide a moving case presentation. Finally, 2 pediatric ophthalmologists who routinely perform surgery for dissociated strabismus present their surgical views on the procedures that they have found most effective in the surgical management of DVD and/or DHD.
Dissociated Vertical Deviation: Mechanism and Purpose In the late 1990s we analyzed a series of scleral search coil recordings of young adults with DVD and were able to identify the various cyclovertical muscles primarily involved in the components of the DVD response and show that each of the component movements obeys Hering’s law. We concluded that DVD is an acquired (learned), often anticipatory, response to taking up fixation with one eye, either when the fellow eye is covered, or spontaneously.1-4 Fixation with one eye in these patients stimulates latent nystagmus, both horizontal and cyclovertical, interfering with vision. The latent nystagmus is conjugate, with the fixing eye typically drifting inward, downward, and intorting, with the refixation saccades of the fixing eye therefore being outward, upward, and extorting. Horizontally, the patient may learn to use a head turn to fix with the adducting eye, which can help damp the horizontal component of the nystagmus (Alexander’s law), but more commonly uses convergence to damp the horizontal nystagmus to improve vision. The latent nystagmus is typically greater when the nondominant eye fixes and more convergence is needed to try to damp the nystagmus. This leads to a larger esodeviation (or smaller exodeviation) when the nondominant eye fixes—the hallmark of so-called dissociated horizontal deviation.5
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Volume 18 Number 4 / August 2014 The patient also learns to damp the cyclovertical nystagmus. Sometimes the otolithic response from a particular head tilt will interfere with this vestibulardriven latent nystagmus, and the patient adopts that head tilt to see better.4 Some of our patients compulsively used this head tilt even though visual acuity improved by only a few letters. Typically the head tilt would persist when the nonfixing eye was covered but would change or disappear when the fixing eye was covered. The cyclovertical nystagmus can also be damped by vergence. Normal disparity-driven vertical vergence involves primarily the superior oblique muscle driving the higher eye downward and the inferior oblique muscle driving the lower eye upward.1,2 The patient with DVD has learned to drive and magnify this vertical vergence to help damp the cyclovertical latent nystagmus—thus creating the clinical phenomenon that we call DVD. The superior oblique muscle tries to drive the fixing eye downward, but this is balanced by a simultaneous upward version to keep the fixing eye fixing, driven primarily by both superior rectus muscles. The fixing eye thus simply intorts, easily seen on recordings and often clinically visible as well. The nonfixing eye, however, is driven upward by its contracting inferior oblique muscle and also by the simultaneous upward version. The net result is the nonfixing eye’s elevating, extorting, and either abducting or adducting, depending on how much convergence is being used to damp the horizontal component of the latent nystagmus. Additional observations support our conclusion that DVD and DHD are used to damp latent or manifest latent nystagmus to improve vision.1,2 Several patients with DVD could read down the eye chart with eyes essentially straight and peripherally fusing until they reached the 20/60 or 20/ 40 line of letters. At that point they broke fusion, fixated with one eye, and read farther down the chart. One patient with weak fusion commented that she liked to fuse most of the time, but when she had to see something most clearly in the distance, she broke fusion, looked with one eye, and let the other eye turn up.4 We measured her visual acuity under both conditions, and it was consistently 3 letters better when the DVD was present. In the scleral search coil recordings, the latent nystagmus typically appeared, or the manifest latent nystagmus worsened, when either eye was covered and always became damped as the DVD developed, as indicated by decreasing velocity of the slow phases.1,2 Occasionally, however, patients with DVD showed no clinically apparent latent nystagmus upon covering either eye. We believe this was because in these patients the DVD was so efficient that it anticipatorily occurred and blocked the latent nystagmus from developing in the first place. Some patients with DVD could voluntarily fix with one eye or the other and even could “imagine” doing so in total darkness. When these patients imagined taking up “fixation” with one eye in total darkness, typical DVD still occurred, recorded with the scleral search coils.4 These
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recordings were consistent with DVD’s being a learned, anticipatory, reflexive eye movement that occurs on taking up fixation with one eye. This type of learned, anticipatory eye movement is somewhat analogous to the “bounce” or “rebound” phenomenon often seen during prism and cover testing of strabismic patients. We thus find strong evidence that DVD serves to improve visual acuity in the fixing eye by helping damp latent or manifest latent nystagmus. This insight should prove useful to us in developing techniques, surgical or otherwise, to treat this vexing form of misalignment. DLG
What is DVD? What can explain this innate, involuntary, unconscious, stereotypical eye movement, in which either eye rotates dorsally in patients with infantile strabismus? I believe that DVD is an atavism. An atavism refers to the reappearance in an individual of characteristics of some remote ancestor that have been absent in intervening generations. What kind of atavism could produce DVD? DVD corresponds to a human dorsal light reflex, a balancing reflex that was first identified in lower lateraleyed animals such as fish over a century ago.6,7 When you turn off the room lights and illuminate the left side of a fish this luminance disparity will cause the fish to tilt leftward toward the light.6,7 Why does luminance disparity induce a body tilt? Maintaining vertical orientation is a critical evolutionary function. In nature, the sky provides a space-stable luminance hemisphere that is always in alignment with the gravitational vertical. In lateral-eyed animals, the balance of luminance input from the two eyes feeds binocular information into the vestibular nucleus and vestibulocerebellum to calibrate tilt position.8 These visuo-vestibular pathways try to maintain equal luminance input to assist the vestibular system in maintaining an upright body position.8 When the system is tricked by illumination of the left eye in a dark room, the system registers the body as tilted toward the right (with its left eye facing the sky) and tries to reequilibrate luminance input by tilting to the left.6,7 When the body is stabilized vertically and the left eye is illuminated, the unilluminated right eye rotates dorsally and the illuminated eye rotates ventrally in an attempt to reequilibrate the balance of luminance to the two eyes.7 It is this binocular component of the dorsal light reflex that is recapitulated in humans with DVD. When cortical binocular vision fails to develop in infancy, this innate subcortical reflex is again expressed in the form of DVD.8 When either eye is covered, the covered eye rotates toward the top of the head (dorsally, as in fish).9 Unlike in fish, however, humans have binocular visual cortex grafted atop lower subcortical centers so that this visual reflex is now triggered by a spontaneous cortical suppression of one eye rather than binocular luminance disparity.10 When a patient with infantile strabismus fixes with one eye, this subcortical visual reflex manifests as a
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Volume 18 Number 4 / August 2014 Finally, you would expect to see remnants of this primitive visual reflex in normal binocular humans.15 All of these findings have been documented. MCB
The Reversed Fixation Test
FIG 1. Video-oculography in a patient with bilateral DVD and latent nystagmus (upper panel) showing a brief true vertical divergence of the eyes, causing them to initially rotate in opposite directions when either eye is occluded (lower panel). OD, right eye; OS, left eye.
hyperdeviation of the other eye. Cortical suppression can also be triggered by occlusion, suffusion with light, blurring, or otherwise degrading the visual image presented to the eye.10 This is why DVD can occur spontaneously and why a binocular luminance disparity need not be present to evoke this reflex in humans. What are the defining features of a dorsal light reflex that characterize DVD? First, DVD is atavistic insofar as it recapitulates a subcortical visual reflex, which is expressed in humans only when higher cortical functions are disabled.8-10 Second, it is accompanied by other reflex binocular movements, such as latent nystagmus, which also are known to arise from subcortical visual reflexes (Figure 1).11 Third, some patients with DVD maintain a head tilt toward the side of the fixing eye that is not compensatory for single binocular vision.12,13 Finally, DVD is modulated by binocular luminance disparity once fixation is established, as demonstrated by the Bielschowsky phenomenon.14 What are some clinical tests of this hypothesis? First, if DVD is a human dorsal light reflex, you would expect it to produce a dorsal rotation of the nonfixing eye. Second, although this dorsal rotation appears to be monocular on clinical examination, DVD should produce a brief vertical divergence movement of the two eyes, that should be detectable on eye movement recordings (Figure 1). Third, the torsional component of the dorsal rotation should not cause a subjective visual tilt but should compensate for one because the movement of DVD is compensatory for an altered internal sense of vertical. Fourth, the incursion of this primitive subcortical reflex should cause the uncovered eye to briefly descend below fixation on alternate cover testing. Fifth, if cortical suppression is the trigger, then DVD should be fundamentally incompatible with diplopia.
Dissociated horizontal deviation (DHD) is a variable horizontal deviation of the eyes that can manifest as an asymmetrical exotropia. It usually follows bimedial recession for infantile esotropia but can also occur in isolation.16 Not all asymmetrical exodeviations result from DHD. A patient with uncorrected anisometropia may have the appearance of a dissociated deviation due to different degrees of accommodative convergence when fixating with either eye. It is therefore important for patients to be wearing their full cycloplegic refraction in order to avoid this measurement error. Asymmetrical deviations can occur from a variety of reasons. After bimedial recessions, for example, patients can simply have unequal exodeviations with each eye fixating due to unequal adduction force in the two eyes. Rare patients with straight eyes may even have a unilateral esodeviation when fixing with the nonpreferred eye.17 Conversely, some patients can have a consecutive exotropia and equal deviations with each eye fixating and still have a DHD. A patient with symmetrical DHD can rarely have equal deviations with either eye fixating. Thus asymmetry of exodeviation in the primary position is neither necessary nor sufficient to establish the diagnosis of DHD. How then can the diagnosis be confirmed? The reversed fixation test (RFT) is a technique that was originally described by Mattheus and colleagues18 to clinically visualize small degrees of DVD. It was later adapted for DHD by Gr€af, who described it as the “decisive diagnostic tool for DHD.”17 The purpose of the RFT is to enable you to detect and accurately measure dissociated horizontal movements. (See Table 1 for a description of how to perform the RFT.) Although DHD was classically thought to be a horizontal expression of the same divergence innervation that characterizes DVD, Brodsky and Fray19 found that DHD arises from dissociated esotonus that is usually superimposed by monocular fixation on a baseline exodeviation (usually resulting from strabismus surgery). Fixation with the nonpreferred eye exerts a much greater esotonus than fixation with the preferred eye, which explains the occasional conversion of an exotropia to an esotropia when the nonpreferred eye takes up fixation. By using the RFT, they found that that DHD lies buried away within a consecutive exotropia in 50% of patients who have a history of infantile esotropia. In addition, they found the RFT to be especially useful in distinguishing DHD from the secondary effects of asymmetric postoperative medial rectus muscle weakness. Finally, the RFT confirmed the presence of a DHD in consecutive exotropia that was symmetrical when either eye was fixating. This effect was due to a fixation duress created by greater medial rectus weakness from strabismus
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Volume 18 Number 4 / August 2014 Table 1. Performing the RFT in a consecutive, left exodeviation 1. Perform prism and alternate cover testing and neutralize the left exodeviation with a prism. 2. Shift the occluder to the right eye and ensure no movement of the left eye through neutralizing prism. 3. Patient fixates with the left eye through prism for at least 5 seconds; RFT is performed by shifting the occluder back to the left eye. 4. Right eye observed for any refixation movement: a. No movement seen 5 negative RFT (no dissociated component) b. Movement seen 5 positive RFT (dissociated component present)
Table 2. Common clinical presentation of DHD using the RFT Fixation through neutralizing prism with eye that exerts greater esotonus (eye with larger exodeviation) induces an abduction movement of the contralateral eye. Fixation through neutralizing prism with eye that exerts less esotonus (eye with smaller exodeviation) induces an equal adduction movement of the contralateral eye.
surgery being offset by the greater dissociated esotonus that is simultaneously exerted during fixation with the nonpreferred eye. The RFT permits a shift in visual fixation from one eye to the other, while the subject maintains the eyes in their prism-neutralized position. Any movement in the uncovered eye is purely driven by a shift in the balance of visual inputs derived from the right and left eyes. Thus corrective refixation movements are only seen in the presence of dissociated deviations. To measure a DHD, simply have the patient hold the neutralizing prism over the exodeviated eye. The examiner neutralizes the additional movement noted with a positive RFT. The size of the refixation movement is usually small (approximately 2D-10D). This small movement represents the difference in esotonus that is being exerted by fixation with each eye. (See Table 2 for the common clinical presentation of DHD using the RFT.) The diagnostic utility of the RFT has inherent limitations. First, it must be performed with the cycloplegic refractive findings in place in a noncycloplegic state to eliminate the dissociated motor effects caused by anisometropia. Second, a positive RFT does not rule out coexistent paretic and restrictive conditions; it simply identifies the presence of a dissociated component. Third, in the setting of equal vision, DHD can be inherently symmetrical, making it impossible to distinguish from a garden variety intermittent exotropia using the RFT. This situation can be suspected when the amplitude of the horizontal deviation increases when the patient becomes distracted or inattentive and therefore ceases to fixate. If suspected (based on the
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associated findings of latent nystagmus or DVD), ask the patient to solve a difficult mathematical problem in their head and watch both eyes drift outward from their previously measured position. Finally, the RFT requires patient cooperation, visual attention, and central fixation. Despite these limitations, the RFT is quick, easy to perform, and diagnostic of DHD when found to be positive. KJF
DVD Measurement Techniques Dissociated vertical deviation (DVD) can be difficult to diagnose and even more difficult to measure. This part of the workshop explains two techniques that are useful in determining and neutralizing the deviation.20 The measurement of DVD can be complex, even for experienced examiners. DVD can vary from visit to visit and examiner to examiner.21 Neutralization of the DVD could have a poor endpoint because of latent nystagmus and redress. It is important to take into consideration the cooperation of the patient. Can you assess the patient with a true prism and alternate cover test (PACT)? Can you only estimate the deviation? Some examiners use the estimation technique for assessing DVD. This allows for not only a grading scale of how large the DVD is but also helps determine the control of DVD. On the grading scale of 1-4, DVD graded as 1 is a small angle, \5D, with excellent control. A DVD graded as 2 is a small angle with poorer control, maybe tropic, with several covers. Grade 3 indicates poorly controlled DVD .10D. A DVD graded as 4 is manifest and .15D. This technique is most useful in infants and/or uncooperative patients. The other measurement technique is an adapted prism and alternate cover test with each eye fixing. This technique is similar to the reversed fixation test described by Kommerell and Mattheus21 and Brodsky and Fray.22,23 First, the examiner holds base down prism over one eye and looks only at the eye behind the prism, adding base down prism until the eye behind the prism stops moving. The contralateral eye is ignored. Repeat the technique with the prism over the other eye. This should be performed in all fields of gaze with each eye fixing. Pay close attention to the presence of a true hypotropia of the nonfixing eye in primary position and side gazes. The hypotropia may only be present initially (during binocular viewing) and then build to a DVD with the PACT. This can occur with DHD as well. The examiner should also note control of the DVD as phoric, intermittent, or manifest. Performing the PACT with a slow, extended cover test allows the examiner to bring out the full amount of DVD. I may perform a Marlowe occlusion prior to measuring the DVD on the best controlled patients. The Marlowe is a prolonged occlusion that dissociates patients. The examiner places a patch over one eye for 45 minutes and then measures the strabismus without allowing the patient to be binocular.
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DVD is often found in conjunction with a horizontal strabismus. I neutralize the larger deviation first.24 KM
Living with Dissociated Vertical Deviation My patients’ parents often ask me, “What is it like living with strabismus? Can you teach me how to help my child navigate through life with misaligned eyes?” Educating my patients and their parents on a life without binocularity is a profound part of my career as a certified orthoptist. Having strabismus allows me to better understand, empathize with, counsel, and treat my patients and their families. Living with dissociated vertical deviation (DVD) can certainly feel like a curse! Because my DVD can become manifest at any given time, I feel self-conscious about having no control of the deviation. As an adult, I worry about its presence more with stress, fatigue, illness, and anxiety. Occasionally, there are times (my wedding day!) when I am forced to plan around my strabismus. Unfortunately, I have not discovered a way to control DVD. However, ridding all visual input by closing my eyes for about 10 seconds seems to offer a reset on my eye alignment. Most of the time, this simple act eliminates the DVD and restores my microesotropic angle. The year is 1988 and my little sister and I are playing dolls on the living room floor when she looks up at me and innocently asks, “Does that hurt, when your eye floats up to the ceiling like that?” Yes, sometimes it does. The sensation is not necessarily pain but more discomfort, and there is greater discomfort with larger DVD. This feeling is extremely difficult to describe, but there is a slight tugging sensation and pressure in the superior orbit. If you have a patient with DVD complaining of obscure eye pain or pressure, consider the DVD as a possible cause. We are all aware that a breakthrough in suppression can lead to intractable diplopia. This is often a result of a life event causing enormous stress and anxiety. During preparation for orthoptic oral board examinations, I awoke one morning to intractable diplopia that brought my life to a halt! During this harrowing ordeal, I gleaned insight into how suppression really works. For me personally, suppression is easiest and best when DVD is manifest. When this is the case, I switch fixation to my nondominant left eye, causing a 25D DVD of the right eye, and the intractable diplopia is eliminated. This allows me to sense and experience good suppression. I then switch fixation back to my dominant right eye and attempt to feel suppression again. Can a person feel suppression? Absolutely! The inability to localize the diplopic image makes intractable diplopia more of a sensation. Rather than seeing the image, you feel its presence. When you are keenly aware of the way intractable diplopia feels, you soon realize the way good suppression feels. As you visually concentrate on the real image, you can watch the diplopic image slowly fade away. In my opinion, this makes relearning suppression a “mind over matter” situation.
Volume 18 Number 4 / August 2014 In summary, it is imperative that we show careful consideration and validation not only to a patient’s cosmetic insecurities but also to the sensory anomalies that are associated with strabismus. They can cause great discomfort and make life’s simple tasks challenging. I hope to have provided you with a better understanding of your patients’ abnormal sensory experiences and given you ideas on how to help your patients overcome them. CCH
Surgical Approach to DVD Nonsurgical management of DVD can sometimes be successful in mild cases. Amblyopia treatment for optimum visual acuity can help control DVD. Consider the possibility of an overminus prescription for a patient with DVD to stimulate accommodation and control of latent nystagmus and the overall control of the DVD. When a DVD is asymmetric in a visually mature patient with good vision in both eyes, refractive error correction can be designed to encourage fixation by the eye with the greater dissociated deviation. The surgical correction of DVD can be challenging. Despite the fact that the deviation can be lessened, patients should have adequate counseling that the deviation can never be truly “cured” because the root cause of the problem lies in the sensory system. Many DVD’s are small and inconspicuous. These deviations can be observed; however, when a deviation is large and frequently manifest, or when it is associated with an abnormal head posture, surgery is often the best course of action. As with all forms of strabismus, surgical planning begins with a complete examination, including visual acuity, sensory status, motility examination, and measurement of the angle of deviation. The extraocular muscle chosen for initial surgery often depends on the presence or absence of inferior oblique overaction. In the absence of inferior oblique muscle overaction, vertical rectus surgery is generally performed. Several procedures have been evaluated in this treatment of DVD, including vertical recession/resection, inferior rectus resection alone, superior rectus recession with or without posterior fixation sutures, and supramaximal superior rectus recession.25-28 Currently, most ophthalmologists tend to favor large superior rectus recession. Fixed suture or hang-back techniques can be performed. Care should be taken to avoid scarring of the superior oblique complex with either surgical approach. Inferior oblique anterior transposition frequently becomes the first-line approach when inferior oblique muscle overaction is present, yet this approach has been reported successful even in patients lacking such dysfunction.29,30 When reinserting the inferior oblique, it is placed just temporal to the inferior rectus insertion. Many surgeons try to narrow the reinsertion and avoid placement anterior to the inferior rectus insertion. Nasal transposition of the inferior oblique tendon has also been described.31 Inferior oblique weakening without
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Volume 18 Number 4 / August 2014 anteriorization is less effective, although standard inferior oblique recession combined with simultaneous weakening of the superior oblique for DVD has been reported favorably.32 Most DVDs and their surgical correction are bilateral. In a case series by von Noorden,33 170 cases of DVD were reviewed and only 24 (14%) were found to be unilateral. However, most cases (91%) were asymmetric in presentation. When bilateral superior rectus surgery is performed, larger supramaximal surgical numbers are targeted. A 6–7 mm recession is recommended for a small deviation, 8–9 mm for a medium deviation, and 10–11 mm for a large deviation. Bilateral inferior oblique anterior transposition to the inferior rectus insertion is often advocated when inferior oblique overaction is present no matter the magnitude of preoperative DVD. Surgeons may opt for a unilateral procedure on a rectus or inferior oblique muscle when manifest DVD is found in an eye that is never used for fixation. Unilateral surgery should be approached with caution if the patient has good visual acuity in each eye because fixation switch may occur. When unilateral surgery is performed, the surgical dose can be highly variable. Superior rectus recessions are generally preferred, using at least 5 mm for a small deviation (10D), 6–7 mm for a medium deviation (15D-20D), and 8–9 mm for a large deviation (25D-30D). Asymmetric bilateral superior rectus surgery can be performed as well using similar recession amounts. Asymmetric placement or resection of the inferior oblique during anteriorization has been reported with varying efficacy for markedly asymmetric DVD.34,35 Postoperative complications can occur. Eyelid retraction is common immediately after superior rectus recession surgery because of the association of the superior rectus and the levator complex but rarely persists beyond the postoperative recover period.36 Asymmetric surgery may result in a true hypotropia of the eye having the greater muscle recession or transposition. Additionally, torsion due to superior oblique muscle scarring can also occur. Lower eyelid fullness is common after inferior oblique anterior transposition. Limitation of elevation on abduction, also termed the antielevation syndrome, is more common after the inferior oblique muscle is advanced anterior to the insertion of the inferior rectus muscle. The most common complication after DVD surgery is recurrence of the deviation. In this circumstance, re-recession of the superior rectus muscle or further advancing an inferior oblique muscle is possible, but results are difficult to predict. For a second operation, many surgeons choose to approach the unoperated elevator: if the first surgery was superior recession, an inferior oblique anterior transposition or weakening would be done; if inferior oblique surgery was first performed, a superior rectus recession could be chosen. An initial, combined surgery on both the inferior oblique and superior rectus has been found helpful to avoid postoperative recurrence of the DVD.37 Risks of this combined approach include limita-
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tion in elevation and upper eyelid retraction. Inferior rectus resection of 4–5 mm has also been advocated for recurrent DVD. Results of this technique are less predictable than with primary surgery.38 EDB, DGM References 1. Guyton DL, Cheeseman EW Jr, Ellis FJ, Straumann D, Zee DS. Dissociated vertical deviation: an exaggerated normal eye movement used to damp cyclovertical latent nystagmus. Trans Am Ophthalmol Soc 1998;96:389-429. 2. Cheeseman EW, Guyton DL. Vertical fusional vergence: the key to dissociated vertical deviation. Arch Ophthalmol 1999;117:1188-91. 3. Guyton DL. Dissociated vertical deviation: Etiology, mechanism, and associated phenomena. J AAPOS 2000;4:131-44. 4. Guyton DL. Dissociated vertical deviation: An acquired nystagmus blockage phenomenon. Am Orthoptic J 2004;54:77-87. 5. Zubcov AA, Reinecke RD, Calhoun JH. Asymmetric horizontal tropias, DVD, and manifest latent nystagmus: an explanation of dissociated horizontal deviation. J Pediatr Ophthalmol Strabismus 1990;27:59-64. € 6. Von Holst E. Uber den Lichtr€ uckenreflex bei Fische. Pubbl Stn Zool Ges 1935;37:109-14. 7. Graf W, Meyer D. Central mechanisms counteract visually induced tonus asymmetries: a study of ocular responses to unilateral illumination in goldfish. J Comp Physiol 1983;150:473-81. 8. Brodsky MC. Dissociated vertical divergence: a righting reflex gone wrong. Arch Ophthalmol 1999;117:1216-22. 9. Brodsky MC. Perceptual correlates of the human dorsal light reflex. Arch Ophthalmol 2002;120:1174-8. 10. Brodsky MC. Dissociated vertical divergence: cortical or subcortical in origin. Strabismus 2011;19:67-8. 11. Brodsky MC. Latent nystagmus: vestibular nystagmus with a twist. Arch Ophthalmol 2004;122:202-9. 12. Crone RA. Alternating hyperphoria. Brit J Ophthalmol 1954;38:591-604. 13. Lang J. Congenital convergent strabismus. Int Ophthalmol Clin 1972;4:88-92. 14. Bielschowsky A. Disturbances of the vertical motor muscles of the eyes. Arch Ophthalmol 1938;20:190-96. 15. van Rijn LJ, ten Tusscher MPM, de Jong I, Hendrikse F. Asymmetrical vertical phorias indicating dissociated vertical deviation in subjects with normal binocular vision. Vision Res 1998;38:2973-8. 16. Romero-Apis D, Castellanos-Bracamontes A. Dissociated horizontal deviation: clinical finings and surgical results in 20 patients. Binoc Vis Q 1992;7:173-8. 17. Gr€af M. Dissociated horizontal deviations (DHD): terminology, diagnosis, and etiology. In Faber TJ, ed. Transactions of the 26th Meeting of the European Strabismological Association, Florence, June 2001. Tokyo: Swets & Zeiinger; 2001:105–8. 18. Mattheus S, Deberitz I, Kommerell G. Differentialdiagnose zwischen inkomitierendem und dissoziiertem Schielen. Arbeitskreis Schielbehandung Berufsverband Augen€artze Deutschlands 1976;10:135-7. 19. Brodsky MC, Fray KJ. Dissociated horizontal deviation after surgery for infantile esotropia: Clinical characteristics and proposed pathophysiologic mechanisms. Arch Ophthalmol 2007;125:1683-92. 20. Strominger MB, Rogers GL, Wagner RS. Dissociated vertical deviation and inferior oblique overaction. J Pediatr Ophthalmol Starbismus 2008;46:132-6. 21. Kommerell G, Mattheus S. Reversed fixation test as a means to differentiate between dissociated and nondissociated strabismus. Strabismus 1996;4:3-9. 22. Brodsky M, Fray K. How to perform the reversed fixation test. Am Orthop J 2007;57:118-22. 23. Batra N. Evaluation of vertical deviations secondary to other causes. Am Orthop J 2011;61:49-52.
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24. von Noorden GK, Campos EC. Binocular Vision and Ocular Motility: Theory and management of Strabismus. 6th ed. St. Louis: Mosby; 2002:377-95. 25. Noel LP, Parks MM. Dissociated vertical deviation: associated findings and results of surgical management. Can J Ophthalmol 1982; 17:10-12. 26. Braverman DE, Scott WE. Surgical correction of dissociated vertical divergence. J Pediatr Ophthalmol Strabismus 1977;14:337-42. 27. Sargent RA. Surgical correction of dissociated hyperdeviation. Am Orthoptic J 1976;26:89-99. 28. Sprague JB, Moore S, Eggers H, et al. Dissociated vertical deviation: treatment with the Faden operation of Cuppers. Arch Ophthalmol 1980;98:465-8. 29. Burke JP, Scott WE, Kutschke PJ. Anterior transposition of the inferior oblique muscle for dissociated vertical deviation. Ophthalmol 1993;100:245-50. 30. Bothun ED, Summers CG. Unilateral inferior oblique anterior transposition for dissociated vertical deviation. J AAPOS 2004;8: 259-63. 31. Fard MA. Anterior and nasal transposition of the inferior oblique muscle for dissociated vertical deviation associated with inferior oblique muscle overaction. J AAPOS 2013;14:35-8.
Volume 18 Number 4 / August 2014 32. Gamio S. A surgical alternative for dissociative vertical deviation based on new pathologic concepts: weakening all four oblique eye muscles. Outcomes and results in 9 cases. Binocul Vis Strabismus Q 2002;17:15-24. 33. Von Noorden GK. Current concepts of infantile esotropia (Bowman lecture). Eye 1988;2:343. 34. Pineles SL, Velez G, Velez FG. Asymmetric inferior oblique anterior transposition for incomitant asymmetric dissociated vertical deviation. Graefes Arch Clin Exp Ophthalmol 2013;251:2639-42. 35. Farvardin M, Attarzadeh A. Combined resection and anterior transposition of the inferior oblique muscle for the treatment of moderate to large dissociated vertical deviation associated with inferior oblique muscle overaction. J Pediatr Ophthalmol Strabismus 2002;39:268-72. quiz 293-4. 36. Coats DK. Treatment of vertical deviations secondary to other causes. Am Orthoptic J 2011;61:53-7. 37. Varn MM, Saunders RA, Wilson ME. Combined bilateral superior rectus muscle recession and inferior oblique muscle weakening for dissociated vertical deviation. J AAPOS 1997;1:134-7. 38. Esswein Kapp MB, von Noorden GK. Treatment of residual dissociated vertical deviation with inferior rectus resection. J Pediatr Ophthalmol Strabismus 1994;31:262-4.
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Dissociated vertical deviation (DVD) is a slow, disconjugate hypertropic deviation of a nonfixating eye. It is usually bilateral, asymmetrical, and often associated with congenital esotropia. The deviating eye elevates, abducts, and excyclotorts. This type of strabismus is often variable, making measurement and clinical quantification difficult. Specific knowledge of the mechanisms and characteristics of the dissociated deviation are required for proper assessment and effective treatment. There is currently no consensus on the mechanisms and pathophysiology of DVD. In this workshop, participants discuss the characteristics and most current methods for assessing and quantifying the deviation and explore the potential etiologies, clinical characteristics, and indications for surgical intervention and nonsurgical management of DVD. ( J AAPOS 2014;18:378-384)
D
issociated vertical deviation (DVD) is recognized by clinicians as a slow, disconjugate hypertropic deviation of a nonfixating eye. It is usually bilateral, asymmetrical, and often associated with congenital esotropia. The deviating eye elevates, abducts, and excyclotorts. “Dissociated strabismus complex” is a more inclusive term for this entity. This type of strabismus is often variable, making measurement and clinical quantification difficult. There is currently no consensus on the mechanism and pathophysiology of DVD. Understanding the potential etiology, clinical characteristics, and indications for surgical intervention should help the reader gain a better insight into the proper way to assess and treat, both surgically and nonsurgically, dissociated deviations. This workshop begins with two of the most widely known concepts of the etiology of DVD, presented by their respective proponents. Three certified orthoptists then discuss measure-
Author affiliations: aThe Krieger Children’s Eye Center at the Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, Maryland; bDepartments of Ophthalmology and Pediatrics, Icahn School of Medicine at Mount Sinai, New York; cDepartment of Ophthalmology and Neurology, Mayo Clinic, Rochester, Minnesota; dUniversity of Arkansas Medical Center and Arkansas Children’s Hospital, Little Rock, Arkansas; eDepartments of Ophthalmology and Visual Neurosciences, University of Minnesota, Minneapolis, Minnesota; f Children’s Eye Center of South Texas, San Antonio, Texas; gDeparment of Pediatrics, University of Minnesota, Minneapolis, Minnesota; hDepartments of Ophthalmology and Pediatrics, Vanderbilt University, Nashville, Tennessee Presented at the 39th Annual Meeting of the American Association for Pediatric Ophthalmology and Strabismus, Boston, Massachusetts, April 3-7, 2013. * These authors contributed equally to this publication as joint principal authors, co-organizers, and comoderators of the workshop. Submitted December 2, 2013. Revision accepted March 23, 2014. Correspondence: Alex Christoff, BS, CO, Assistant Professor of Ophthalmology, The Krieger Children’s Eye Center at the Wilmer Institute, The Johns Hopkins University School of Medicine, Baltimore, MD 21287-902 Copyright Ó 2014 by the American Association for Pediatric Ophthalmology and Strabismus. 1091-8531/$36.00 http://dx.doi.org/10.1016/j.jaapos.2014.03.009
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ment techniques and nonsurgical treatment options and provide a moving case presentation. Finally, 2 pediatric ophthalmologists who routinely perform surgery for dissociated strabismus present their surgical views on the procedures that they have found most effective in the surgical management of DVD and/or DHD.
Dissociated Vertical Deviation: Mechanism and Purpose In the late 1990s we analyzed a series of scleral search coil recordings of young adults with DVD and were able to identify the various cyclovertical muscles primarily involved in the components of the DVD response and show that each of the component movements obeys Hering’s law. We concluded that DVD is an acquired (learned), often anticipatory, response to taking up fixation with one eye, either when the fellow eye is covered, or spontaneously.1-4 Fixation with one eye in these patients stimulates latent nystagmus, both horizontal and cyclovertical, interfering with vision. The latent nystagmus is conjugate, with the fixing eye typically drifting inward, downward, and intorting, with the refixation saccades of the fixing eye therefore being outward, upward, and extorting. Horizontally, the patient may learn to use a head turn to fix with the adducting eye, which can help damp the horizontal component of the nystagmus (Alexander’s law), but more commonly uses convergence to damp the horizontal nystagmus to improve vision. The latent nystagmus is typically greater when the nondominant eye fixes and more convergence is needed to try to damp the nystagmus. This leads to a larger esodeviation (or smaller exodeviation) when the nondominant eye fixes—the hallmark of so-called dissociated horizontal deviation.5
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Volume 18 Number 4 / August 2014 The patient also learns to damp the cyclovertical nystagmus. Sometimes the otolithic response from a particular head tilt will interfere with this vestibulardriven latent nystagmus, and the patient adopts that head tilt to see better.4 Some of our patients compulsively used this head tilt even though visual acuity improved by only a few letters. Typically the head tilt would persist when the nonfixing eye was covered but would change or disappear when the fixing eye was covered. The cyclovertical nystagmus can also be damped by vergence. Normal disparity-driven vertical vergence involves primarily the superior oblique muscle driving the higher eye downward and the inferior oblique muscle driving the lower eye upward.1,2 The patient with DVD has learned to drive and magnify this vertical vergence to help damp the cyclovertical latent nystagmus—thus creating the clinical phenomenon that we call DVD. The superior oblique muscle tries to drive the fixing eye downward, but this is balanced by a simultaneous upward version to keep the fixing eye fixing, driven primarily by both superior rectus muscles. The fixing eye thus simply intorts, easily seen on recordings and often clinically visible as well. The nonfixing eye, however, is driven upward by its contracting inferior oblique muscle and also by the simultaneous upward version. The net result is the nonfixing eye’s elevating, extorting, and either abducting or adducting, depending on how much convergence is being used to damp the horizontal component of the latent nystagmus. Additional observations support our conclusion that DVD and DHD are used to damp latent or manifest latent nystagmus to improve vision.1,2 Several patients with DVD could read down the eye chart with eyes essentially straight and peripherally fusing until they reached the 20/60 or 20/ 40 line of letters. At that point they broke fusion, fixated with one eye, and read farther down the chart. One patient with weak fusion commented that she liked to fuse most of the time, but when she had to see something most clearly in the distance, she broke fusion, looked with one eye, and let the other eye turn up.4 We measured her visual acuity under both conditions, and it was consistently 3 letters better when the DVD was present. In the scleral search coil recordings, the latent nystagmus typically appeared, or the manifest latent nystagmus worsened, when either eye was covered and always became damped as the DVD developed, as indicated by decreasing velocity of the slow phases.1,2 Occasionally, however, patients with DVD showed no clinically apparent latent nystagmus upon covering either eye. We believe this was because in these patients the DVD was so efficient that it anticipatorily occurred and blocked the latent nystagmus from developing in the first place. Some patients with DVD could voluntarily fix with one eye or the other and even could “imagine” doing so in total darkness. When these patients imagined taking up “fixation” with one eye in total darkness, typical DVD still occurred, recorded with the scleral search coils.4 These
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recordings were consistent with DVD’s being a learned, anticipatory, reflexive eye movement that occurs on taking up fixation with one eye. This type of learned, anticipatory eye movement is somewhat analogous to the “bounce” or “rebound” phenomenon often seen during prism and cover testing of strabismic patients. We thus find strong evidence that DVD serves to improve visual acuity in the fixing eye by helping damp latent or manifest latent nystagmus. This insight should prove useful to us in developing techniques, surgical or otherwise, to treat this vexing form of misalignment. DLG
What is DVD? What can explain this innate, involuntary, unconscious, stereotypical eye movement, in which either eye rotates dorsally in patients with infantile strabismus? I believe that DVD is an atavism. An atavism refers to the reappearance in an individual of characteristics of some remote ancestor that have been absent in intervening generations. What kind of atavism could produce DVD? DVD corresponds to a human dorsal light reflex, a balancing reflex that was first identified in lower lateraleyed animals such as fish over a century ago.6,7 When you turn off the room lights and illuminate the left side of a fish this luminance disparity will cause the fish to tilt leftward toward the light.6,7 Why does luminance disparity induce a body tilt? Maintaining vertical orientation is a critical evolutionary function. In nature, the sky provides a space-stable luminance hemisphere that is always in alignment with the gravitational vertical. In lateral-eyed animals, the balance of luminance input from the two eyes feeds binocular information into the vestibular nucleus and vestibulocerebellum to calibrate tilt position.8 These visuo-vestibular pathways try to maintain equal luminance input to assist the vestibular system in maintaining an upright body position.8 When the system is tricked by illumination of the left eye in a dark room, the system registers the body as tilted toward the right (with its left eye facing the sky) and tries to reequilibrate luminance input by tilting to the left.6,7 When the body is stabilized vertically and the left eye is illuminated, the unilluminated right eye rotates dorsally and the illuminated eye rotates ventrally in an attempt to reequilibrate the balance of luminance to the two eyes.7 It is this binocular component of the dorsal light reflex that is recapitulated in humans with DVD. When cortical binocular vision fails to develop in infancy, this innate subcortical reflex is again expressed in the form of DVD.8 When either eye is covered, the covered eye rotates toward the top of the head (dorsally, as in fish).9 Unlike in fish, however, humans have binocular visual cortex grafted atop lower subcortical centers so that this visual reflex is now triggered by a spontaneous cortical suppression of one eye rather than binocular luminance disparity.10 When a patient with infantile strabismus fixes with one eye, this subcortical visual reflex manifests as a
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Volume 18 Number 4 / August 2014 Finally, you would expect to see remnants of this primitive visual reflex in normal binocular humans.15 All of these findings have been documented. MCB
The Reversed Fixation Test
FIG 1. Video-oculography in a patient with bilateral DVD and latent nystagmus (upper panel) showing a brief true vertical divergence of the eyes, causing them to initially rotate in opposite directions when either eye is occluded (lower panel). OD, right eye; OS, left eye.
hyperdeviation of the other eye. Cortical suppression can also be triggered by occlusion, suffusion with light, blurring, or otherwise degrading the visual image presented to the eye.10 This is why DVD can occur spontaneously and why a binocular luminance disparity need not be present to evoke this reflex in humans. What are the defining features of a dorsal light reflex that characterize DVD? First, DVD is atavistic insofar as it recapitulates a subcortical visual reflex, which is expressed in humans only when higher cortical functions are disabled.8-10 Second, it is accompanied by other reflex binocular movements, such as latent nystagmus, which also are known to arise from subcortical visual reflexes (Figure 1).11 Third, some patients with DVD maintain a head tilt toward the side of the fixing eye that is not compensatory for single binocular vision.12,13 Finally, DVD is modulated by binocular luminance disparity once fixation is established, as demonstrated by the Bielschowsky phenomenon.14 What are some clinical tests of this hypothesis? First, if DVD is a human dorsal light reflex, you would expect it to produce a dorsal rotation of the nonfixing eye. Second, although this dorsal rotation appears to be monocular on clinical examination, DVD should produce a brief vertical divergence movement of the two eyes, that should be detectable on eye movement recordings (Figure 1). Third, the torsional component of the dorsal rotation should not cause a subjective visual tilt but should compensate for one because the movement of DVD is compensatory for an altered internal sense of vertical. Fourth, the incursion of this primitive subcortical reflex should cause the uncovered eye to briefly descend below fixation on alternate cover testing. Fifth, if cortical suppression is the trigger, then DVD should be fundamentally incompatible with diplopia.
Dissociated horizontal deviation (DHD) is a variable horizontal deviation of the eyes that can manifest as an asymmetrical exotropia. It usually follows bimedial recession for infantile esotropia but can also occur in isolation.16 Not all asymmetrical exodeviations result from DHD. A patient with uncorrected anisometropia may have the appearance of a dissociated deviation due to different degrees of accommodative convergence when fixating with either eye. It is therefore important for patients to be wearing their full cycloplegic refraction in order to avoid this measurement error. Asymmetrical deviations can occur from a variety of reasons. After bimedial recessions, for example, patients can simply have unequal exodeviations with each eye fixating due to unequal adduction force in the two eyes. Rare patients with straight eyes may even have a unilateral esodeviation when fixing with the nonpreferred eye.17 Conversely, some patients can have a consecutive exotropia and equal deviations with each eye fixating and still have a DHD. A patient with symmetrical DHD can rarely have equal deviations with either eye fixating. Thus asymmetry of exodeviation in the primary position is neither necessary nor sufficient to establish the diagnosis of DHD. How then can the diagnosis be confirmed? The reversed fixation test (RFT) is a technique that was originally described by Mattheus and colleagues18 to clinically visualize small degrees of DVD. It was later adapted for DHD by Gr€af, who described it as the “decisive diagnostic tool for DHD.”17 The purpose of the RFT is to enable you to detect and accurately measure dissociated horizontal movements. (See Table 1 for a description of how to perform the RFT.) Although DHD was classically thought to be a horizontal expression of the same divergence innervation that characterizes DVD, Brodsky and Fray19 found that DHD arises from dissociated esotonus that is usually superimposed by monocular fixation on a baseline exodeviation (usually resulting from strabismus surgery). Fixation with the nonpreferred eye exerts a much greater esotonus than fixation with the preferred eye, which explains the occasional conversion of an exotropia to an esotropia when the nonpreferred eye takes up fixation. By using the RFT, they found that that DHD lies buried away within a consecutive exotropia in 50% of patients who have a history of infantile esotropia. In addition, they found the RFT to be especially useful in distinguishing DHD from the secondary effects of asymmetric postoperative medial rectus muscle weakness. Finally, the RFT confirmed the presence of a DHD in consecutive exotropia that was symmetrical when either eye was fixating. This effect was due to a fixation duress created by greater medial rectus weakness from strabismus
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Volume 18 Number 4 / August 2014 Table 1. Performing the RFT in a consecutive, left exodeviation 1. Perform prism and alternate cover testing and neutralize the left exodeviation with a prism. 2. Shift the occluder to the right eye and ensure no movement of the left eye through neutralizing prism. 3. Patient fixates with the left eye through prism for at least 5 seconds; RFT is performed by shifting the occluder back to the left eye. 4. Right eye observed for any refixation movement: a. No movement seen 5 negative RFT (no dissociated component) b. Movement seen 5 positive RFT (dissociated component present)
Table 2. Common clinical presentation of DHD using the RFT Fixation through neutralizing prism with eye that exerts greater esotonus (eye with larger exodeviation) induces an abduction movement of the contralateral eye. Fixation through neutralizing prism with eye that exerts less esotonus (eye with smaller exodeviation) induces an equal adduction movement of the contralateral eye.
surgery being offset by the greater dissociated esotonus that is simultaneously exerted during fixation with the nonpreferred eye. The RFT permits a shift in visual fixation from one eye to the other, while the subject maintains the eyes in their prism-neutralized position. Any movement in the uncovered eye is purely driven by a shift in the balance of visual inputs derived from the right and left eyes. Thus corrective refixation movements are only seen in the presence of dissociated deviations. To measure a DHD, simply have the patient hold the neutralizing prism over the exodeviated eye. The examiner neutralizes the additional movement noted with a positive RFT. The size of the refixation movement is usually small (approximately 2D-10D). This small movement represents the difference in esotonus that is being exerted by fixation with each eye. (See Table 2 for the common clinical presentation of DHD using the RFT.) The diagnostic utility of the RFT has inherent limitations. First, it must be performed with the cycloplegic refractive findings in place in a noncycloplegic state to eliminate the dissociated motor effects caused by anisometropia. Second, a positive RFT does not rule out coexistent paretic and restrictive conditions; it simply identifies the presence of a dissociated component. Third, in the setting of equal vision, DHD can be inherently symmetrical, making it impossible to distinguish from a garden variety intermittent exotropia using the RFT. This situation can be suspected when the amplitude of the horizontal deviation increases when the patient becomes distracted or inattentive and therefore ceases to fixate. If suspected (based on the
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associated findings of latent nystagmus or DVD), ask the patient to solve a difficult mathematical problem in their head and watch both eyes drift outward from their previously measured position. Finally, the RFT requires patient cooperation, visual attention, and central fixation. Despite these limitations, the RFT is quick, easy to perform, and diagnostic of DHD when found to be positive. KJF
DVD Measurement Techniques Dissociated vertical deviation (DVD) can be difficult to diagnose and even more difficult to measure. This part of the workshop explains two techniques that are useful in determining and neutralizing the deviation.20 The measurement of DVD can be complex, even for experienced examiners. DVD can vary from visit to visit and examiner to examiner.21 Neutralization of the DVD could have a poor endpoint because of latent nystagmus and redress. It is important to take into consideration the cooperation of the patient. Can you assess the patient with a true prism and alternate cover test (PACT)? Can you only estimate the deviation? Some examiners use the estimation technique for assessing DVD. This allows for not only a grading scale of how large the DVD is but also helps determine the control of DVD. On the grading scale of 1-4, DVD graded as 1 is a small angle, \5D, with excellent control. A DVD graded as 2 is a small angle with poorer control, maybe tropic, with several covers. Grade 3 indicates poorly controlled DVD .10D. A DVD graded as 4 is manifest and .15D. This technique is most useful in infants and/or uncooperative patients. The other measurement technique is an adapted prism and alternate cover test with each eye fixing. This technique is similar to the reversed fixation test described by Kommerell and Mattheus21 and Brodsky and Fray.22,23 First, the examiner holds base down prism over one eye and looks only at the eye behind the prism, adding base down prism until the eye behind the prism stops moving. The contralateral eye is ignored. Repeat the technique with the prism over the other eye. This should be performed in all fields of gaze with each eye fixing. Pay close attention to the presence of a true hypotropia of the nonfixing eye in primary position and side gazes. The hypotropia may only be present initially (during binocular viewing) and then build to a DVD with the PACT. This can occur with DHD as well. The examiner should also note control of the DVD as phoric, intermittent, or manifest. Performing the PACT with a slow, extended cover test allows the examiner to bring out the full amount of DVD. I may perform a Marlowe occlusion prior to measuring the DVD on the best controlled patients. The Marlowe is a prolonged occlusion that dissociates patients. The examiner places a patch over one eye for 45 minutes and then measures the strabismus without allowing the patient to be binocular.
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DVD is often found in conjunction with a horizontal strabismus. I neutralize the larger deviation first.24 KM
Living with Dissociated Vertical Deviation My patients’ parents often ask me, “What is it like living with strabismus? Can you teach me how to help my child navigate through life with misaligned eyes?” Educating my patients and their parents on a life without binocularity is a profound part of my career as a certified orthoptist. Having strabismus allows me to better understand, empathize with, counsel, and treat my patients and their families. Living with dissociated vertical deviation (DVD) can certainly feel like a curse! Because my DVD can become manifest at any given time, I feel self-conscious about having no control of the deviation. As an adult, I worry about its presence more with stress, fatigue, illness, and anxiety. Occasionally, there are times (my wedding day!) when I am forced to plan around my strabismus. Unfortunately, I have not discovered a way to control DVD. However, ridding all visual input by closing my eyes for about 10 seconds seems to offer a reset on my eye alignment. Most of the time, this simple act eliminates the DVD and restores my microesotropic angle. The year is 1988 and my little sister and I are playing dolls on the living room floor when she looks up at me and innocently asks, “Does that hurt, when your eye floats up to the ceiling like that?” Yes, sometimes it does. The sensation is not necessarily pain but more discomfort, and there is greater discomfort with larger DVD. This feeling is extremely difficult to describe, but there is a slight tugging sensation and pressure in the superior orbit. If you have a patient with DVD complaining of obscure eye pain or pressure, consider the DVD as a possible cause. We are all aware that a breakthrough in suppression can lead to intractable diplopia. This is often a result of a life event causing enormous stress and anxiety. During preparation for orthoptic oral board examinations, I awoke one morning to intractable diplopia that brought my life to a halt! During this harrowing ordeal, I gleaned insight into how suppression really works. For me personally, suppression is easiest and best when DVD is manifest. When this is the case, I switch fixation to my nondominant left eye, causing a 25D DVD of the right eye, and the intractable diplopia is eliminated. This allows me to sense and experience good suppression. I then switch fixation back to my dominant right eye and attempt to feel suppression again. Can a person feel suppression? Absolutely! The inability to localize the diplopic image makes intractable diplopia more of a sensation. Rather than seeing the image, you feel its presence. When you are keenly aware of the way intractable diplopia feels, you soon realize the way good suppression feels. As you visually concentrate on the real image, you can watch the diplopic image slowly fade away. In my opinion, this makes relearning suppression a “mind over matter” situation.
Volume 18 Number 4 / August 2014 In summary, it is imperative that we show careful consideration and validation not only to a patient’s cosmetic insecurities but also to the sensory anomalies that are associated with strabismus. They can cause great discomfort and make life’s simple tasks challenging. I hope to have provided you with a better understanding of your patients’ abnormal sensory experiences and given you ideas on how to help your patients overcome them. CCH
Surgical Approach to DVD Nonsurgical management of DVD can sometimes be successful in mild cases. Amblyopia treatment for optimum visual acuity can help control DVD. Consider the possibility of an overminus prescription for a patient with DVD to stimulate accommodation and control of latent nystagmus and the overall control of the DVD. When a DVD is asymmetric in a visually mature patient with good vision in both eyes, refractive error correction can be designed to encourage fixation by the eye with the greater dissociated deviation. The surgical correction of DVD can be challenging. Despite the fact that the deviation can be lessened, patients should have adequate counseling that the deviation can never be truly “cured” because the root cause of the problem lies in the sensory system. Many DVD’s are small and inconspicuous. These deviations can be observed; however, when a deviation is large and frequently manifest, or when it is associated with an abnormal head posture, surgery is often the best course of action. As with all forms of strabismus, surgical planning begins with a complete examination, including visual acuity, sensory status, motility examination, and measurement of the angle of deviation. The extraocular muscle chosen for initial surgery often depends on the presence or absence of inferior oblique overaction. In the absence of inferior oblique muscle overaction, vertical rectus surgery is generally performed. Several procedures have been evaluated in this treatment of DVD, including vertical recession/resection, inferior rectus resection alone, superior rectus recession with or without posterior fixation sutures, and supramaximal superior rectus recession.25-28 Currently, most ophthalmologists tend to favor large superior rectus recession. Fixed suture or hang-back techniques can be performed. Care should be taken to avoid scarring of the superior oblique complex with either surgical approach. Inferior oblique anterior transposition frequently becomes the first-line approach when inferior oblique muscle overaction is present, yet this approach has been reported successful even in patients lacking such dysfunction.29,30 When reinserting the inferior oblique, it is placed just temporal to the inferior rectus insertion. Many surgeons try to narrow the reinsertion and avoid placement anterior to the inferior rectus insertion. Nasal transposition of the inferior oblique tendon has also been described.31 Inferior oblique weakening without
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Volume 18 Number 4 / August 2014 anteriorization is less effective, although standard inferior oblique recession combined with simultaneous weakening of the superior oblique for DVD has been reported favorably.32 Most DVDs and their surgical correction are bilateral. In a case series by von Noorden,33 170 cases of DVD were reviewed and only 24 (14%) were found to be unilateral. However, most cases (91%) were asymmetric in presentation. When bilateral superior rectus surgery is performed, larger supramaximal surgical numbers are targeted. A 6–7 mm recession is recommended for a small deviation, 8–9 mm for a medium deviation, and 10–11 mm for a large deviation. Bilateral inferior oblique anterior transposition to the inferior rectus insertion is often advocated when inferior oblique overaction is present no matter the magnitude of preoperative DVD. Surgeons may opt for a unilateral procedure on a rectus or inferior oblique muscle when manifest DVD is found in an eye that is never used for fixation. Unilateral surgery should be approached with caution if the patient has good visual acuity in each eye because fixation switch may occur. When unilateral surgery is performed, the surgical dose can be highly variable. Superior rectus recessions are generally preferred, using at least 5 mm for a small deviation (10D), 6–7 mm for a medium deviation (15D-20D), and 8–9 mm for a large deviation (25D-30D). Asymmetric bilateral superior rectus surgery can be performed as well using similar recession amounts. Asymmetric placement or resection of the inferior oblique during anteriorization has been reported with varying efficacy for markedly asymmetric DVD.34,35 Postoperative complications can occur. Eyelid retraction is common immediately after superior rectus recession surgery because of the association of the superior rectus and the levator complex but rarely persists beyond the postoperative recover period.36 Asymmetric surgery may result in a true hypotropia of the eye having the greater muscle recession or transposition. Additionally, torsion due to superior oblique muscle scarring can also occur. Lower eyelid fullness is common after inferior oblique anterior transposition. Limitation of elevation on abduction, also termed the antielevation syndrome, is more common after the inferior oblique muscle is advanced anterior to the insertion of the inferior rectus muscle. The most common complication after DVD surgery is recurrence of the deviation. In this circumstance, re-recession of the superior rectus muscle or further advancing an inferior oblique muscle is possible, but results are difficult to predict. For a second operation, many surgeons choose to approach the unoperated elevator: if the first surgery was superior recession, an inferior oblique anterior transposition or weakening would be done; if inferior oblique surgery was first performed, a superior rectus recession could be chosen. An initial, combined surgery on both the inferior oblique and superior rectus has been found helpful to avoid postoperative recurrence of the DVD.37 Risks of this combined approach include limita-
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tion in elevation and upper eyelid retraction. Inferior rectus resection of 4–5 mm has also been advocated for recurrent DVD. Results of this technique are less predictable than with primary surgery.38 EDB, DGM References 1. Guyton DL, Cheeseman EW Jr, Ellis FJ, Straumann D, Zee DS. Dissociated vertical deviation: an exaggerated normal eye movement used to damp cyclovertical latent nystagmus. Trans Am Ophthalmol Soc 1998;96:389-429. 2. Cheeseman EW, Guyton DL. Vertical fusional vergence: the key to dissociated vertical deviation. Arch Ophthalmol 1999;117:1188-91. 3. Guyton DL. Dissociated vertical deviation: Etiology, mechanism, and associated phenomena. J AAPOS 2000;4:131-44. 4. Guyton DL. Dissociated vertical deviation: An acquired nystagmus blockage phenomenon. Am Orthoptic J 2004;54:77-87. 5. Zubcov AA, Reinecke RD, Calhoun JH. Asymmetric horizontal tropias, DVD, and manifest latent nystagmus: an explanation of dissociated horizontal deviation. J Pediatr Ophthalmol Strabismus 1990;27:59-64. € 6. Von Holst E. Uber den Lichtr€ uckenreflex bei Fische. Pubbl Stn Zool Ges 1935;37:109-14. 7. Graf W, Meyer D. Central mechanisms counteract visually induced tonus asymmetries: a study of ocular responses to unilateral illumination in goldfish. J Comp Physiol 1983;150:473-81. 8. Brodsky MC. Dissociated vertical divergence: a righting reflex gone wrong. Arch Ophthalmol 1999;117:1216-22. 9. Brodsky MC. Perceptual correlates of the human dorsal light reflex. Arch Ophthalmol 2002;120:1174-8. 10. Brodsky MC. Dissociated vertical divergence: cortical or subcortical in origin. Strabismus 2011;19:67-8. 11. Brodsky MC. Latent nystagmus: vestibular nystagmus with a twist. Arch Ophthalmol 2004;122:202-9. 12. Crone RA. Alternating hyperphoria. Brit J Ophthalmol 1954;38:591-604. 13. Lang J. Congenital convergent strabismus. Int Ophthalmol Clin 1972;4:88-92. 14. Bielschowsky A. Disturbances of the vertical motor muscles of the eyes. Arch Ophthalmol 1938;20:190-96. 15. van Rijn LJ, ten Tusscher MPM, de Jong I, Hendrikse F. Asymmetrical vertical phorias indicating dissociated vertical deviation in subjects with normal binocular vision. Vision Res 1998;38:2973-8. 16. Romero-Apis D, Castellanos-Bracamontes A. Dissociated horizontal deviation: clinical finings and surgical results in 20 patients. Binoc Vis Q 1992;7:173-8. 17. Gr€af M. Dissociated horizontal deviations (DHD): terminology, diagnosis, and etiology. In Faber TJ, ed. Transactions of the 26th Meeting of the European Strabismological Association, Florence, June 2001. Tokyo: Swets & Zeiinger; 2001:105–8. 18. Mattheus S, Deberitz I, Kommerell G. Differentialdiagnose zwischen inkomitierendem und dissoziiertem Schielen. Arbeitskreis Schielbehandung Berufsverband Augen€artze Deutschlands 1976;10:135-7. 19. Brodsky MC, Fray KJ. Dissociated horizontal deviation after surgery for infantile esotropia: Clinical characteristics and proposed pathophysiologic mechanisms. Arch Ophthalmol 2007;125:1683-92. 20. Strominger MB, Rogers GL, Wagner RS. Dissociated vertical deviation and inferior oblique overaction. J Pediatr Ophthalmol Starbismus 2008;46:132-6. 21. Kommerell G, Mattheus S. Reversed fixation test as a means to differentiate between dissociated and nondissociated strabismus. Strabismus 1996;4:3-9. 22. Brodsky M, Fray K. How to perform the reversed fixation test. Am Orthop J 2007;57:118-22. 23. Batra N. Evaluation of vertical deviations secondary to other causes. Am Orthop J 2011;61:49-52.
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Volume 18 Number 4 / August 2014 32. Gamio S. A surgical alternative for dissociative vertical deviation based on new pathologic concepts: weakening all four oblique eye muscles. Outcomes and results in 9 cases. Binocul Vis Strabismus Q 2002;17:15-24. 33. Von Noorden GK. Current concepts of infantile esotropia (Bowman lecture). Eye 1988;2:343. 34. Pineles SL, Velez G, Velez FG. Asymmetric inferior oblique anterior transposition for incomitant asymmetric dissociated vertical deviation. Graefes Arch Clin Exp Ophthalmol 2013;251:2639-42. 35. Farvardin M, Attarzadeh A. Combined resection and anterior transposition of the inferior oblique muscle for the treatment of moderate to large dissociated vertical deviation associated with inferior oblique muscle overaction. J Pediatr Ophthalmol Strabismus 2002;39:268-72. quiz 293-4. 36. Coats DK. Treatment of vertical deviations secondary to other causes. Am Orthoptic J 2011;61:53-7. 37. Varn MM, Saunders RA, Wilson ME. Combined bilateral superior rectus muscle recession and inferior oblique muscle weakening for dissociated vertical deviation. J AAPOS 1997;1:134-7. 38. Esswein Kapp MB, von Noorden GK. Treatment of residual dissociated vertical deviation with inferior rectus resection. J Pediatr Ophthalmol Strabismus 1994;31:262-4.
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