Summary
Eye muscle surgery for the treatment of nystagmus has a long history, but today remains a small part of the treatment tools of a strabismus surgeon. Its use is largely confined to one operation in those rare older children who have constant large angle anomalous head postures. Knowledge gained from the last 30 years of animal and human research has resulted in the development of a comprehensive system for planning and executing eye muscle surgical treatment of nystagmus. This is utilized in infants, children, and adults with nystagmus, with or without associated sensory system abnormalities. New understanding of the physiology of nystagmus in infancy and childhood supports the clinically documented beneficial effects of eye muscle surgery on eye position, nystagmus characteristics and visual function.
This chapter covers a modern classification of nystagmus; a more complete method of clinical and electrophysiologic evaluation of the patient with nystagmus; specific eye muscle surgical procedures to treat combinations of nystagmus, strabismus, and anomalous head posturing; and expected outcomes and complications of surgery.
17 Nystagmus Surgery
17.1 Introduction
Before considering eye muscle surgery, the exact type of nystagmus must be diagnosed. Here, the use of accurate ocular motor recordings is essential. Key waveform characteristics pathognomonic for all forms of nystagmus are easily distinguishable. 1 “Nystagmus” alone is no longer an acceptable diagnosis. Eye movement recordings can identify many different types of nystagmus and differentiate them from clinically similar appearing saccadic oscillations. 1 Also, evaluation and comparison of therapies require a quantitative measure of visual system changes, which translate to clinical outcomes. Although one of the goals of nystagmus therapy may be to improve visual “acuity,” this should not be considered the primary outcome. Measured visual acuity is not always a good measure of real-world visual function. 2 , 3 Acuity is the result of several variables, such as stress, afferent deficits, medications, illness, fatigue, attention, head position, and eye position. The relation of these variables to nystagmus is idiosyncratic. Although nystagmus amplitude most directly impacts cosmetic appearance, it is not a good predictor of acuity or other visual function. A therapy that reduces amplitude may not improve acuity, and one that does improve acuity may not reduce amplitude. The eye movement characteristic related to overall visual function is that period during each beat of nystagmus when the eye’s velocity is < 4 degrees/second and its position is within 1 to 5 degrees of the target. 4 , 5 , 6 , 7 , 8 These “foveation” periods are easily measured and their changes directly relate to many visual functions. 4 , 5 , 6 , 7 , 8
Planning for eye muscle surgery in the nystagmus patient requires a thorough history, clinical evaluation, and testing. Special testing may include neuroimaging, serologic (blood, urine, spinal fluid) evaluation, electrophysiology (eye movement recordings, electroretinography, visual evoked responses, dark adaptation), optical coherence tomography, photography, and angiography. Once it is determined that the ocular motor abnormality cannot be treated with coincidental therapy of an underlying systemic condition, eye muscle surgery is considered. There is a twofold purpose of eye muscle surgery in patients with nystagmus. One is to improve the position of the eye(s) and/or head, and the other is to improve the oscillation’s beat-to-beat characteristics. There is a frequent association of strabismus with nystagmus, allowing the surgeon to treat both at the same time. The two conditions often affect each other, so correcting the strabismus may favorably affect the nystagmus and vice versa. The presence of an anomalous head posture (AHP) may be seen in infantile as well as acquired forms of nystagmus, and in both, surgery serves to move gaze (or the eye) into the straight-ahead position.
Infantile nystagmus syndrome (INS) is the most common type of nystagmus diagnosis that responds to eye muscle surgery, and it will therefore be the main focus of this chapter. INS is an ocular motor disorder of unknown etiology, which usually presents in early infancy (not congenitally) and is clinically characterized by involuntary oscillations of the eyes. The Leicestershire nystagmus survey recently reported a prevalence of 24.0 per 10,000 in the general population. 9 The most common forms of nystagmus were neurologic nystagmus (6.8 per 10,000 population) and INS associated with low vision (3.4–4.2 per 10,000). 9 Nystagmus is significantly more common in the white European population than in the Indian, Pakistani, and other Asian populations. 10 , 11 Other estimates of the incidence of INS vary enormously from 1 in 350 to 1 in 20,000, but the most commonly quoted figure is 1 in 6,550 or 0.015%. 10 , 11
These movements usually have a slow and fast phase, although they may be purely pendular. They are usually clinically horizontal with a small torsional component but always have a vertical component on eye movement recordings. 4 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 The intensity of nystagmus increases on eccentric gaze. INS may “disobey” Alexander’s law under binocular conditions, and this is often useful in distinguishing it from horizontal peripheral vestibular nystagmus. Alexander’s law states that, in peripheral vestibular nystagmus, the nystagmus increases in the direction of the fast phase and decreases, but never reverses, in the direction of the slow phase. Other clinical characteristics of INS 4 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 can include the following:
It remains horizontal in upgaze (in contrast to acquired and/or vestibular nystagmus, which changes direction in vertical gaze).
Increased intensity with fixation and decreased intensity with sleep or inattention.
Variable intensity in different positions of gaze (about a null position).
Changing direction in different positions of gaze (about a neutral position).
Decreased intensity (damping) with convergence.
Anomalous head posturing.
Strabismus.
Increased incidence of significant refractive errors.
These features are useful in further distinguishing INS from peripheral vestibular nystagmus, which becomes worse with occlusion and is damped by fixation. Anxiety, fatigue, stress, some medications, and systemic illness all increase nystagmus intensity and degrade visual function. 4 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19
Estimates of the prevalence of strabismus in INS range from 16 to 70%. Latent nystagmus is now termed fusion maldevelopment nystagmus syndrome (FMNS) by the Classification of Eye Movement Abnormalities and Strabismus (CEMAS) working group (Table 17‑1, Table 17‑2, Table 17‑3). Strabismus is essential for latent nystagmus, but incidental to INS. 16 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 The term sensory nystagmus has been applied to patients whose INS is attributable to an underlying sensory visual disorder. Cogan originally proposed that, in sensory nystagmus, the poor visual acuity interrupts sensory afferent input to the oculomotor control system, which causes fixation to become unstable and leads to a pendular oscillation of the eyes. 19 By contrast, motor nystagmus was attributed to signal errors intrinsic to the ocular motor control centers, leading to a jerk nystagmus with relatively good visual acuity. The myth that the presence or absence of a primary sensory deficit can be predicted on the basis of clinical presentation (i.e., pendular versus jerk nystagmus) has long been dispelled. 14 , 19 , 30 , 31 Pendular and jerk waveforms often coexist in the same individual with INS. Waveform analysis alone can therefore not be used to predict the presence or absence of afferent visual pathway dysfunction. 14 , 19 , 30 , 31 In INS, all of the known waveforms have been recorded in patients with and without sensory visual deficits. 14 , 19 , 30 , 31 INS has also been diagnosed in patients with visual acuities ranging from 20/20 to no light perception. Thus, infantile nystagmus does not “result” from poor acuity. Similarly, the age of onset for the nystagmus cannot be used to predict the presence or absence of an underlying sensory visual deficit. The neurophysiologic mechanism by which abnormal sensory visual input from both eyes precipitates, or “unhinges,” INS is unknown. These facts render obsolete the terms congenital, sensory, and motor when describing INS.
INS often occurs in association with congenital or early onset (first 6 months of life) defects in the visual sensory system such as systemic and ocular albinism, achromatopsia, aniridia, congenital retinal dystrophies and degenerations, visual cortex anomalies, and congenital cataracts, glaucoma, and corneal diseases. 1 , 4 , 13 , 14 , 32 , 33 , 34 , 35 All children with INS have an eye position in the orbit where the INS intensity is the least (“null” position), which is in the primary position in about 40% of patients and in an eccentric orbital position in 60%. Those with an eccentric null position adopt a head turn to maintain the eyes in that position. This is particularly prominent when the child is concentrating on a distant object, since INS tends to worsen with attempted fixation. 1 , 4 , 13 , 14 , 32 , 33 , 34 , 35 The head turn is an attempt to improve visual function under these conditions. Some individuals with INS utilize extreme head turns to place their eyes in maximum side gaze and actively block their nystagmus. Unlike positioning the eyes in a null zone, in which foveation is optimum, the mechanism of this active blockage is uncertain. It is our hypothesis that by using the vestibulo-ocular reflex (VOR) or voluntary gaze to place the globe near the orbital walls, a mechanical damping effect on the oscillation is obtained. Head oscillations are common in INS (30–40%) and are the result of a parallel, anomalous neural instability to the neck muscles. 1 , 4 , 13 , 14 , 32 , 33 , 34 , 35 The head oscillations are not used as a strategy to improve vision, except in those rare patients with abnormal gain of their VOR.
Oscillopsia is almost never constantly present in INS. 1 , 4 , 13 , 14 , 32 , 33 , 34 , 35 In rare patients with intermittent oscillopsia, it tends to occur at gaze angles in which the nystagmus is maximal or a new ocular motor or sensory system defect develops. 36 Absence of oscillopsia is usually not helpful in distinguishing congenital from acquired nystagmus in children. Children with acquired nystagmus in the first decade of life rarely have a continuation of this complaint. 36 Adults and older children with acquired nystagmus retain oscillopsia.
17.2 Evaluation
Although not routinely available, eye movement recordings are useful to identify many different types of nystagmus and saccadic intrusions and oscillations. An integral part of waveform analysis is the identification of the portions of each cycle (beat of nystagmus) during which the image of the target was on the fovea (foveation periods). 37 Documentation of these important characteristics of nystagmus waveforms by accurate ocular motor recordings provides the data needed for diagnosis and treatment. 37
17.2.1 Visual Acuity
Visual acuity is best measured with refraction in place binocularly and monocularly using one of three methods: the Teller Acuity Cards (TAC; University of Washington) or Lea Symbols (Lea-Test Ltd.) procedure (preverbal children), the Amblyopia Treatment Study (ATS) single, surrounded, HOTV optotype protocol (under 7 years of age), or the Early Treatment Diabetic Retinopathy Study (ETDRS) chart protocol (7 or more years of age). 38 Measurements are obtained in the patient’s null position, which is determined by clinical evaluation, a head posture measuring system, and/or eye movement recordings. Due to nystagmus, TAC visual acuity is tested with the cards held vertically so that the gratings are horizontally oriented. It is important to note that since the ocular motor oscillation of INS is almost uniformly horizontal (with horizontal intensity changes seen even in those patients with torsional and vertical head postures), the testing of acuity with vertically held TAC is valid for all these patients.
17.2.2 Ocular Motor and Standard Clinical Evaluations
Ocular motor examination includes a precise determination of alignment at distance (3–6 m) and near (33 cm) in all diagnostic positions of gaze. Associated sensory system abnormalities are confirmed by history, complete ophthalmic evaluation, and special testing. In patients with INS, an AHP is not the “abnormality” that needs to be treated. If it were, surgery on the neck muscles would be in order, not surgery on the extraocular muscle (EOM). An AHP is an adaptive strategy that is deliberately employed in the service of improved visual function. Also, an AHP is under the direct control of the patient and, therefore, may not be the most accurate or repeatable measure of the real problem, which is the gaze position in which the INS waveforms have the most well-developed foveation periods. Although various methods of measuring the AHP can be employed, data from eye movement recordings plotted over all gaze angles provide the most precise method for planning EOM surgery to reposition the gaze angle to the best foveation. Eye movement recordings and visual acuities measured at different gaze angles are both acceptable clinical methods. If neither is available, measuring head position will yield an approximate value upon which to base EOM surgery. 12 , 14 , 19 , 39 , 40 Head posture testing should be repeated at multiple intervals over a continuous 15-minute time frame to help rule out infantile aperiodic/periodic alternating nystagmus (APAN).
From 9 to 33% of patients with INS will have an inherent rhythmic, periodic, or aperiodically changing nystagmus intensity and/or direction over time. 3 , 41 , 42 , 43 , 44 , 45 Most clinicians diagnose this oscillation as acquired periodic alternating nystagmus (PAN). 3 , 41 , 42 , 43 , 44 , 45 Acquired PAN has a specific pattern identified by the presence of spontaneous nystagmus in the primary position, which beats horizontally in one direction for 1 or 2 minutes, followed by a quiet period, and then reappearance of the nystagmus in the opposite direction for a similar length of time. 3 , 41 , 42 , 43 , 44 , 45 It is usually seen in association with vestibular-cerebellar disease and neurodegenerative conditions. 3 , 41 , 42 , 43 , 44 , 45 APAN has all the characteristics of INS except that the null point shifts position in a regular (periodic) or irregular (aperiodic) pattern, and is usually also asymmetrical, with unequal intervals of jerk nystagmus in each direction. This results in changes of intensity and/or direction of nystagmus within seconds to minutes.
The occurrence of IPAN is not as rare as previously suggested and can be missed due to long or irregular cycles and the patient’s preference for only one AHP. 3 , 41 , 42 , 43 , 44 , 45 The changing null period is easier to recognize with eye movement recordings, which are not available in all clinical environments. The clinician may be able to diagnose this disorder if an INS patient is examined in the following way: occlude the nonpreferred eye and examine the preferred eye with the head straight and gaze in primary position over at least 5 to 10 minutes. The examiner looks for a regular or irregular changing oscillation intensity and/or direction. Identification of IPAN is essential if surgical or medical treatment is being considered for strabismus, nystagmus, and/or an associated AHP.
Although INS is a lifelong condition, it remains variable over time. This includes minute-to-minute variability as well as long-term age-associated changes and other ocular and systemic conditions. There are few data about the effect of aging on INS, but we do know that changes can occur in INS oscillation over time. Medications, along with degenerative and neurologic illnesses, may contribute to these changes. Understanding INS as a dynamic disease process is important to the lifelong evaluation and care of these patients.
17.3 Surgery of the Eye Muscles in the Treatment of Nystagmus
17.3.1 Background
There are quantitative data showing that if the slow foveation periods occurring during each beat of nystagmus can be lengthened or increased, then some of the patient’s visual functions may improve. 36 , 46 , 47 , 48 , 49 This can be achieved by the patient, or by therapeutic interventions, including medicines, surgery, contact lenses, acupuncture, and biofeedback. In Anderson’s textbook Ocular Vertical Deviations and the Treatment of Nystagmus (2nd ed., 1959), he states: “It has been found that such operation not only may greatly lessen torticollis, but may also improve vision by lessening the nystagmus itself.” 50 The idea that eye muscle surgery has visual system beneficial effects beyond the “mechanical” repositioning of the muscles or globe was a novel concept that was initially predicted after post-Kestenbaum eye movement data analysis. This was only successfully demonstrated however, after years of careful analysis of patients and their eye movement nystagmus recordings, and hypothesis-driven animal and human trials.
Although two goals of nystagmus therapy may be reconstructive and visual acuity improvements, they are not the primary outcome measures. Measured visual acuity is the result of several variables, such as stress, afferent deficits, head position, and eye position. The relationship between these variables and the nystagmus waveform are idiosyncratic and therefore not always a good measure of real-world visual function. 51 Nystagmus amplitude is the characteristic most directly related to cosmetic appearance, but amplitude is not a good predictor of acuity, oscillopsia, visual recognition time, gaze-dependent visual acuity, or contrast sensitivity. 51
17.3.2 Indications for Surgery
Indication for eye muscle surgery in any patient with nystagmus results from a thorough history, clinical evaluation, and special testing. Once it is determined that the ocular motor abnormality cannot be improved by treatment of an underlying systemic condition, eye muscle surgery may be considered. There are three goals of eye muscle surgery in nystgmus patients: (1) improve a compensatory AHP due to an eccentric gaze null position, (2) improve strabismic deviation, and (3) improve the oscillation’s beat-to-beat characteristics (foveation periods). There is a high association of strabismus with nystagmus, which often allows the surgeon to treat both at the same time. 52 , 53 The two conditions often affect each other. Correction of strabismus can improve binocular fusion, which may favorably affect the nystagmus, and vice versa. An AHP may be present in infantile and acquired forms of nystagmus, and surgery serves to move gaze (or the eyes) into the straight-ahead position in both.
17.3.3 History and Benefits of Eye Muscle Surgery for Nystagmus
The concept of a possible neurologic benefit from surgery on the EOMs has a long history. The origins of nystagmus surgical studies began with early clinical trials of the Anderson-Kestenbaum recession-resection surgery on humans, and studies of eye movements of animals with nystagmus. In a 1977 study of INS surgery, a profound change was noted in the shape of nystagmus intensity versus gaze-angle function. 54 Anderson-Kestenbaum surgery was shown to increase the breadth of the null region and decrease overall nystagmus intensity, in addition to shifting the plot toward primary position, as was expected. 54
An animal model for INS was used to test the hypothesis that something more was occurring to affect nystagmus than just the moving or resecting of the eye muscles. 47 , 55 , 56 Eye movement recordings verified profound and persistent nystagmus damping from disinsertion of the EOM followed by its immediate reattachment to its original insertion (tenotomy and reattachment [T&R]). 47 , 55 , 56 Other animal studies and human clinical trials demonstrated that T&R dampened the nystagmus with improved foveation characteristics and visual function. 8 , 39 , 40 , 49 , 51 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65
The physiology of ocular motor proprioception and its role in both involuntary ocular oscillations and normal ocular motor control has received renewed interest from the ocular motor basic science community. 66 , 67 The tendinoscleral segment of the global portion of the EOM is now called its “enthesis” and is where surgery is performed. Recently studies have identified enthesial neurons and shown them to have proprioceptive anatomy and physiology. 66 , 67 They probably provide feedback, which assists with alignment and stabilization of the eyes. These structures may relate to afferent central nervous system input, and their disruption during surgery could influence postoperative outcome. The neurophysiologic hypothesis for the “improvement” in nystagmus is that there is a reduction of small-signal gain of the ocular motor plant caused by interfering with enthesial, neural proprioceptive tension control. Enthesial nerve signals from palisade-type nontwitch fibers are likely involved in modulating the gain of sensory feedback from the eye muscles analogous to the gamma efferent loop that controls the gain of proprioceptive feedback in skeletal muscles. 66 , 67
17.3.4 Operation Classification
The types of operation used for nystagmus have only recently been classified systematically. In 1953, Anderson and Kestenbaum independently suggested that an abnormal head posture due to nystagmus could be alleviated by surgery. 68 , 69 , 70 In the following year Goto made similar suggestions. Anderson’s proposal was for recession of the pair of yoke rectus muscles whose action was in the direction of the face turn. 68 , 69 , 70 Goto suggested resection of the yoke antagonist muscles, and Kestenbaum favored surgery on all four horizontal rectus muscles (but recommended that the eyes be done sequentially). 70 The Kestenbaum strategy, with modifications, is most commonly performed today, and his name is usually attached to this surgical approach. A logical extension of these procedures was applied by Dermot Pierse of England in 1959. 71 He described two patients with nystagmus with the head held backward for maximum vision. He weakened both depressors (inferior rectus and superior oblique). Many authors subsequently have published their results with similar operations.
17.3.5 Surgical Techniques
The mechanics of eye muscle surgery in patients with nystagmus are no different than in strabismus. The techniques of recession, resection, tenotomy, tenectomy, myectomy, myotomy, tuck, and transposition are familiar to strabismus surgeons. These procedures are discussed at length in other sections of this text, and the reader is referred to those chapters for their details. Our consolidated approach to eye muscle surgery in patients with nystagmus developed from a need to improve the multiple ocular motor and visual abnormalities in this patient population. These include, but may not be limited to, the nystagmus itself, anomalous head posturing, and strabismus, as well as deficiency of acuity, stereopsis, motion processing, gaze-dependent vision, visual reaction time, and contrast sensitivity. 2 , 72 , 73 , 74 The nine-operation system allows the clinician to optimize surgical intervention in INS patients with one procedure. In our experience, most patients (85–90%) with INS have, in addition to their oscillation, a clinically significant head posture, strabismus, or vergence damping, alone or in some combination. This requires that the surgical approach incorporate all the patient’s findings. The rationale for classification of surgical procedures into nine separate but related types was therefore necessary. In multiple series of over 1,000 nystagmus operations, the following types were observed 8 , 39 , 40 , 49 , 51 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 : 22% had operation 1 (eccentric horizontal head position alone), 16% had operation 2 (chin-down head posture ± strabismus), 15% had operation 3 (strabismus alone), 10% had operation 4 (horizontal head posture + strabismus), 10% had operation 5 (chin-up head posture ± strabismus), 9% had operation 6 (nystagmus alone, no head posture, vergence damping, or strabismus), 7% had operation 7 (multiplanar head posture ± strabismus), 6% had operation 8 (convergence damping alone with good binocular function), and 5% had operation 9 (torsional head posture alone).
A few observations can be made by using and analyzing this system. Most patients with infantile forms of nystagmus (91%) have strabismus with or without an AHP and will benefit from some removal or repositioning of the EOMs and not from T&R alone. The largest populations of patients have a combination of AHP (horizontal or vertical) and strabismus. There is also a large, under-recognized population of patients who benefit from surgical intervention for a chin-up or chin-down head posture. There is evidence that the presence of a vertical head posture with INS is more commonly associated with diagnosable diseases of the prechiasmal visual system, such as albinism, achromatopsia and other retinal dystrophies, optic nerve hypoplasia, and foveal hypoplasia. 29 , 57 Although clinicians may not have recognized these vertical null positions, or have less experience with their treatment, patients with a chin-down or chin-up posture should be as eligible for surgical treatment as those with horizontal head postures.
Some strabismus surgeons are reluctant to operate on seemingly normal-functioning oblique muscles due to the potential for cyclovertical motor and sensory complications. Unfortunately, nystagmus surgeons are often required to operate on nondysfunctional muscles, and this is especially true for chin-up and chin-down postures. Combined vertical rectus recession and resection procedures are prone to cause secondary alphabet (A and V pattern) and cyclotorsional deviations, and we therefore prefer bilateral oblique and rectus muscle operations for chin-up and chin-down postures. The key to surgical success in this group of patients is to perform equal oblique and rectus muscle surgery on each eye with attention to detail. 59 The only downside of this surgery is a usual 10% to 15% comitant limitation of vertical gaze with mild lid retraction.
17.3.6 Surgical Timing
The optimal timing of nystagmus surgery, with or without an associated AHP, is not fully established. It is the author’s opinion that early surgery (under 24 months of age) for INS may have a more profound effect on nystagmus and related visual development than later surgery. This is especially true for those INS patients with associated visual sensory deficits. We usually wait until the children are on their feet (about 10–14 months of age) unless there is an associated infantile strabismus that requires surgery. Early eye muscle surgery for eye movement disorders in not a new idea. 56 , 75 , 76 , 77 , 78 Human and animal studies conducted in the last 25 years support the clinical benefit of early ocular motor treatment. 56 , 75 , 76 , 77 , 78 Although there are data suggesting improved results with nystagmus surgery under 24 months of age, the total picture is not yet clear.
Stay updated, free articles. Join our Telegram channel
Full access? Get Clinical Tree
