The Richard G.

Scobee Memorial Lecture

Preverbal Assessment for Amblyopia

Pamela J. Kutschke, C.O.

ABSTRACT Purpose: To describe and compare the different methods of preverbal assessment of amblyopia. Results: Each method of visual assessment has its plusses and minuses. Conclusion: There is no best method for assessment for amblyopia. The best method may be a combination of the various described tests.

INTRODUCTION When looking for an idea for this lecture, I tried to think of something that we, as orthoptists, do every day and that makes a great impact on our work lives. The area of preverbal assessment of amblyopia is a subject of ongoing debate. Each clinician has their own method of determining visual ability and a strong opinion on which
From the Department of Ophthalmology and Visual Sciences, University of Iowa, Iowa City, Iowa. Presented as the 35th annual Richard G. Scobee Memorial Lecture at the annual meeting of the American Association of Certied Orthoptists, New Orleans, Louisiana, October 25, 2005. Requests for reprints should be addressed to: Pamela J. Kutschke, C.O., 11254 PFP, Dept. of Ophthalmology and Visual Sciences, University of Iowa Health Care, Iowa City, IA 52242. e-mail: pamela-kutschke@uiowa.edu

method is best. However, the diagnosis of amblyopia in the preverbal child is often a difcult and challenging task. Testing focuses either on determining an actual visual acuity value for each eye or on determining a preference for one eye over the other. Various methods have been described and compared in the literature. TESTS Three tests were designed for laboratory use to determine an actual visual acuity value. These include optokinetic nystagmus, forced preferential looking, and visually evoked potentials. OKN Optokinetic nystagmus (OKN) occurs when objects pass across the eld of vision

2005 Board of Regents of the University of Wisconsin System, American Orthoptic Journal, Volume 55, 2005, ISSN 0065-955X, E-ISSN 1553-4448

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and produce pursuit eye movements followed by a rexation saccade. OKN is physiologic and involuntary, requiring only that the subject is awake with his eyes open. The classic OKN study was published by Gorman and associates in 1957.1 One hundred infants, aged less than six days, were placed under a canopy of moving black and white stripes. An observer subjectively noted the smallest stripe width that elicited OKN. In keeping with the standard, that 1 minute of arc is equal to 20/20 Snellen visual acuity, a stripe width of 20 minutes would equal 20/400. In this way, Gorman determined the visual acuity of the newborn to be 20/200 to 20/400. Dayton and associates took this concept farther and employed an electro-oculogram to determine the presence or absence of OKN.2 This study found similar results concluding that newborn acuity is at least 20/400 and improves with the advancing age of the infant. This consistency suggested that OKN could be useful in determining the visual acuity of infants. In the clinical setting, Enoch and Rabinowicz reported on the use of the handheld OKN drum presented at different distances to follow visual acuity in an infant with monocular cataract.3 Although testing time for OKN is short, patient cooperation is required. Due to size and complexity, the type of equipment used by Gorman and Dayton and their associates is not suitable for clinical use. A handheld OKN drum is good for clinical use. However, variations can occur as the speed of movement of the target, eyetarget distance, and target characteristics are not standardized. To reduce outside interference, the visual eld needs to be lled with the testing stripes, limiting the ability to use different testing distances to vary the stimulus size. OKN is quite different from Snellen-type tasks as it requires visual detection, not resolution of the target. This may be why some investigators have shown a poor correla-

tion between the visual acuity determined by OKN and Snellen visual acuity.4,5,6 Absence of OKN has uncertain signicance. Some apparently normal infants do not demonstrate OKN, probably due to inattention. OKN response depends on an intact ocular motor system, from pursuit and saccade centers to the brainstem to the cranial nerves and extraocular muscles. Disturbance anywhere in this chain will result in an abnormal OKN response despite intact visual processing. Although intact OKN has been elicited from infants with no visual cortex, a positive OKN response usually corresponds to visual function.7 It does not seem to correlate accurately to a specic visual acuity level. Catford and Oliver developed a handheld OKN device for clinical testing (Figure 1).8 The apparatus consists of a screen with a central aperture and a motorized drum with oscillating black dots of various sizes placed around it on a white background. Smaller and smaller targets are viewed

FIGURE 1: Catford-Oliver drum. (Courtesy of Amy McCarthy, C.O.)

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through the screen until no eye movement is elicited. One study by Khan and associates tested this device and found that while the nystagmus response was a good qualitative indicator, it could not be used to determine the exact level of vision.5 Another study by Atkinson and associates came to a similar conclusion.4 Because the Catford drum uses circular targets, no detail resolution is needed, as is required for optotype visual acuity. In addition, the dots correspond to the overall size of a Snellen letter, not the stroke width of each segment of the letter. FPL The second method for visual acuity assessment, forced preferential looking (FPL) has been extensively researched. In 1958, Fantz9 and Berlyne7 independently reported the behavior of infants to preferentially xate patterned stimuli more than homogeneous ones. Using this premise, Fantz and colleagues10 described the preferential looking technique using a test chamber where the infant was exposed to black and white stripes versus a gray eld while an observer watched the infants corneal reections to determine both the number of times the infant xated on a stimulus and the duration of xation on each stimulus. The width of the stripes was reduced until no preference to xate the pattern stimulus was shown. At this point, both objects presumably appeared the same to the infant. The acuity estimate for a particular age was designated as the smallest stripe width for which 75% or more of the infants of that age showed longer xation of the striped pattern than the homogeneous eld. The results were recorded in terms of spatial frequency or cycles per degree. A spatial frequency difference of one octave corresponds to a doubling or a halving of the spatial frequency. For example, a one octave difference exists between 30 and 60 cycles per degree. By convention, a 20/20 Snellen E subtends

5 minutes of arc at 20 feet. A complete cycle would correspond to two stroke widths, or 2/60 or 1/30 degrees of arc. Therefore, 20/20 corresponds to 30 cycles per degree. In the 1970s, Teller and colleagues developed the forced preferential looking technique, a modied version of Fantzs procedure.11,12 The apparatus consists of a gray cardboard screen with a rectangular window through which is shown two placards, one striped black and white and one a homogeneous gray corresponding to the mean luminance of the stimuli. The observer is blind to the location of the stimulus and the corneal reection cannot be seen. A peephole in the center of the apparatus allows the observer to judge whether the stripe is on the left or the right, based on behavioral cues from the infant such as facial expression, or head or eye movement. Each infant was tested with a variety of different width gratings. The optimum age for testing was found to be 2 to 3 months. Younger infants tired easily and older infants were too interested in their surroundings. FPL was found to be useful in the laboratory setting. Statistical limitations required a large number of trials, as many as 60 to 100, to produce a reasonably accurate assessment of visual acuity, necessitating lengthy testing time of up to an hour. Testing required the use of three adults, one each to hold the child, observe the response, and record the data. Conventional FPL is reportedly possible only up to 12 months of age. Beyond this, behavioral factors limit testing ability. Using operant techniques from audiometry studies to introduce positive visual and auditory reinforcement, the testing age of FPL was broadened to the most difcult age group, 1224 month olds. Mayer and Dobson used an apparatus incorporating two identical animated toy animals, one to each side of the FPL screen, as reinforcement for correct responses.13 Birch and colleagues used food to increase cooperation in these older children.14

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FIGURE 2: Teller acuity cards.

However, the time involved in performing the test is still a predominant limitation. A modied approach, the diagnostic stripe-width method, employs a single grating that has been predetermined to be visible to approximately 95% of normal infants of that particular age.12 The infant must score a certain number of correct responses to a given number of trials. Vision is assessed on a pass or fail system with respect to the expected age norm. The benet of this system is the low number of trials and the reduced testing time. However, the test is used more as a screening tool as it does not determine an exact visual acuity value but identies those with an abnormal visual response. Another modication developed for use in clinical settings is the staircase method. By placing most of the preferential looking trials near the acuity threshold, this procedure attempts to minimize the number of trials needed to determine visual acuity. The stimuli are presented in a step-wise manner going from lowest to highest spatial frequency. One of the arguments against this type of testing is that it introduces a bias in determining the acuity threshold. The number of trials needed to

determine acuity still strains the ability of many children to cooperate. The FPL procedure became more clinically applicable with the advent of the commercially available Teller Acuity Cards (TAC). The cards measure 55cm by 25cm with black and white gratings on one side and a luminance matched homogeneous background on the other (Figure 2). The child sits on the parents lap while the examiner shows the cards to the child. The examiner is not masked as to the gratings location. Cards are shown in descending order starting with the coarsest grating. The card can be rotated 180 for retesting. The childs behavior is viewed through a peephole in the center of the card. A positive response may be noted by either head or eye movement, or in older children pointing, toward the graded stripes. Once the observer is certain that a grating has been seen, it need not be presented again. Although not required, a gray screen with an opening to view the cards is available to reduce distractions. This procedure was found to be faster and has been found to be as accurate as the laboratory FPL. The equipment needed for the acuity card procedure is inexpensive and minimal training is required to administer the test.

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The main difference between the acuity card procedure and the FPL procedure is in the judgment of the childs response by the observer. In FPL testing, the observer judges the response based on either a right or wrong basis. In the acuity card procedure, the observer notes the quality and correctness of the response. If there is a strongly correct response, the observer goes to the next higher frequency. As the threshold is reached, responses become less strong and multiple trials with a particular grating can be performed. This reduces the number of trials required for each frequency. The acuity card procedure has been reported to be successful up to 1224 months, although reports vary.13,1517 Visuomotor, interactive, and attentional factors have been reported to result in poor acuity card scores in developmentally challenged children.18 However, when an acuity is obtained, it appears to be based on developmental, rather than chronological age.15 A major difculty with FPL is that gratings typically provide falsely high acuities in patients with both anisometropic19 and strabismic20 amblyopia. One reason could be that patients with amblyopia typically have better near visual acuity, and the TAC procedure is a near test. Another is that one can still detect the grating on the Teller cards when the visual acuity is defocused enough to produce poor Snellen acuity. Kushner and colleagues compared TAC results with Snellen results in older patients with visual defects.21 They found better visual acuity results with TAC than Snellen. TAC often found normal visual acuity where Snellen visual acuity was abnormal. VEP The third test, visually evoked potential (VEP) is a summed cortical response that results from a temporal change in the intensity of the visual stimulus entering the eye. To record, electrodes are placed on the scalp over the occipital pole, the location of

the visual cortex, with grounding electrodes on the forehead, earlobe, or mastoid. The visual stimulus can be a ash of light or a pattern of rapidly alternating black and white checkerboard or stripes presented transiently or continuously. The recorded signals are amplied and averaged to produce a signal-to-noise ratio. Testing requires less cooperation than the two previously mentioned behavioral methods although accurate xation and accommodation to the stimulus are needed. Thirty to sixty second intervals for each stimulus size are tested resulting in a test time of about 20 minutes. Widespread clinical application is limited, as testing equipment is expensive and training is needed to record and interpret responses. Studies have found VEP to reach adult acuity levels by 4 to 6 months of age.22 The results of VEP in evaluating patients with possible visual cortex dysfunction must be interpreted with caution as VEP has been recorded in patients with absence of the occipital cortex23 and cortical blindness.24 This may be due to the contribution of the secondary visual cortices. The exact origin of the waveforms generated in VEPs is not clear. OKN and FPL acuities are typically lower than those found by VEP. Reports have cited the inability to correlate the visual acuity results found between tests.2527 Differences between the type of test and the method in which they are administered may account for the disparity. VEP does not require a motor response. This motor response, required for FPL, involves a higher level of processing, including the visual association cortex and nonvisual areas of the brain in addition to the primary visual cortex. These systems mature at different rates with early cortical VEP responses maturing more rapidly.28 Another difference is that VEP uses a temporally modulated target while FPL uses stationary targets. VEP also measures foveal function, while OKN and FPL stimuli are larger and

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their peripheral placement stimulates extrafoveal and central areas. EVALUATION VEP, OKN, and FPL were each designed to determine a visual acuity value that corresponds to Snellen visual acuity. However, most researchers caution a comparison of these values is often misleading. Each method uses a different level of visual and motor processing and Snellen equivalents are helpful only on a conceptual basis. Resolution tests using optotypes differ signicantly from the recognition tests such as FPL and OKN. The disparity between resolution and recognition may be insignicant in normal vision but becomes greater as the visual acuity decreases, such as in amblyopia. A recent survey of pediatric ophthalmologists and orthoptists showed that few rely on OKN, preferential looking, or VEP for amblyopia assessment in their preverbal patients. The majority, 93%, relies on xation and following ability and/or the induced tropia test. The evaluation of the monocular and binocular xation and following ability is an essential part of the clinical assessment of vision in the preverbal child. Any animated toys, movies, wiggle pictures, nger puppets, or other targets that require accommodation are appropriate. One eye is occluded and the child is presented with the target, preferably lighted. The position of the corneal light reex is noted. The letter C is indicated if the reex is centrally located and xation is assumed to be foveal. The letter S stands for steady and may be used to denote two qualities. Steady xation implies good xing and following movement. It also may be used to indicate the absence of nystagmus. The occluder is then removed and the examiner determines the M or maintenance of xation with either eye. This is also called the binocular xation pattern.

The binocular xation pattern is a commonly used test to detect the presence of amblyopia. This test is based on the assumption that patients will alternate xation, or hold xation well, with either eye during binocular viewing if the vision of the eyes is equal. In the presence of monocular decreased vision, the patient will xate with the eye with better vision and will not hold xation with the amblyopic eye. The presence of manifest strabismus makes this determination easy as the xating eye is readily apparent. If alternation is present, vision is equal. Knapp and Moore described xation pattern testing as early as 1962.29 They classied xation of the ability of the nonpreferred eye to hold xation. Zipf, in 1976, is credited as one of the rst to examine the reliability of xation pattern testing using this system of xation grading to enable monitoring of amblyopia therapy.30 Zipf noted that the binocular xation pattern was unreliable in testing patients with small angle strabismus of 10 or less. Wright and colleagues31,32 also found unacceptably high false positive rates in these patients and felt this was due to the retinal image falling within the facultative central suppression scotoma present in patients with monoxation.33 The use of a 10 prism to shift the object of regard to outside of this scotoma was suggested. Wright also noted that amblyopic patients would, at times, alternate with a prism when tested on a stationary target. It was found that xation should be held through smooth pursuit to ensure better testing reliability. With the prism and smooth pursuit, they showed a good correlation between xation preference testing and visual acuity. It is now accepted that in nonstrabismic patients or those with a small angle of deviation, it is necessary to create a strabismus using a prism placed base-down or base-in in front of either eye. Prisms of different powers, ranging from 10 to 25, have been described.31,32,3436 The same criteria for determining CSM are used.

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The binocular xation pattern/induced tropia test is a quick, reproducible, inexpensive, objective method of diagnosing amblyopia. Studies have compared the binocular xation pattern, with or without a prism, to Snellen visual acuity.34,35,37,38 Most agree that the test reliably documents those patients with amblyopia. Wright and colleagues found that by combining the test with the ability to hold xation through smooth pursuit, they were able to reduce the number of false negatives.32 The rate of over-diagnosis was found to be low. Others, have found a higher false positive rate.34,35,37 Due to the large number of clinicians using the BFP/ITT to diagnose amblyopia, it is assumed that most pediatric ophthalmologists and orthoptists nd the test reliable. However, there is always controversy. To my knowledge, only one purely negative article regarding the xation pattern method has been published in the English literature. This article by Attila and associates stated that use of the xation pattern to determine visual acuity and the possible presence of amblyopia is so insensitive, and so unspecic that it is virtually useless, if not medically hazardous.39 One explanation for these discrepancies may be found in the methodology of the various studies. Campos and Gulli found that patients with amblyopia who were rst treated after the age of three would not show alternate xation, even in the presence of equal visual acuity.40 Test subject age and past treatment data were often not listed for past studies concerning xation pattern. However, as all studies compared xation pattern to optotype visual acuity, patients needed to be old enough to perform standard visual acuity measurement. I have observed that the xation pattern in older patients is often unreliable. Older strabismic patients usually have a preferred eye, even with equal vision. Conversely, nonstrabismic patients with an acuity difference will often alter-

nate xation through a prism because they are aware of the diplopic image, even if one is not clear. The BFP has been compared to all three of the previously mentioned laboratory tests. Ellis and colleagues compared clinical evaluation by a pediatric ophthalmologist, including xation preferences, to Teller acuity cards.41 A tendency of the TAC to underestimate amblyopia with respect to clinical judgment was found. Mayer and Fulton compared FPL to the xation preference and found the two tests to correlate in anisometropic and deprivation amblyopia but not in strabismic amblyopia.42 It was hypothesized that the difference was due to the fact that anisometropic and deprivation amblyopia affect central and peripheral retina while strabismic amblyopia mainly affects the central, or foveal, retina. Wilcox and Sokol compared binocular xation pattern to VEP in esotropic patients.43 Both tests were able to diagnose amblyopia. However, the binocular xation pattern was not useful in following visual improvement during amblyopia treatment. This inability of the xation pattern to monitor visual acuity change has always caused the clinician difculty. Methods of grading are subjective and imprecise, and may vary greatly with the childs mood. The preferred response is always equal xation. This may not be possible, especially in the presence of a unilateral organic disorder that prevents normal vision. Cadera and associates used a neutral density rotary lter in combination with a xation preference test to calibrate the point at which a patient would switch xation from the fellow eye to the amblyopic eye.44 A dense neutral density lter was placed over the preferred eye to switch xation to the amblyopic eye. Fixation with the preferred eye resumed when, as the density of the lter was decreased, a point was reached where the dominant eye had a visual acuity equal to or better than the

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amblyopic eye. In this way, progress of amblyopia treatment could be monitored. Keech and Kutschke used a combination of 12 prism with calibrated photographic fog lters placed before the normal eye to degrade the vision to a point where xation switched to the amblyopic eye.45 A specic visual acuity level could not be assigned to a lter as levels for a particular lter varied among patients. However, denser prismlter lens combinations degraded visual acuity in a sequential fashion for each individual patient. The combined prism-lter lenses were able to accurately assess changes in visual acuity in control patients and those with amblyopia. Unfortunately, the gradient lters were costly to produce and the idea never caught on. Our newest endeavor to calibrate the xation test is the Iowa lter bar. Graduated Bangerter lters are paired with 12 Fresnel prisms to be used in much the same way as the gradient lters. The prism-lter combination is sandwiched between two clear, scratch-resistant plastic strips making the apparatus easy and inexpensive. The device can be held with the prism basein or base-down. Preliminary testing shows the lters to decrease visual acuity in a predictable fashion as the blur-levels on the bar increase. The Iowa Fixation Bar is currently undergoing further testing. CONCLUSION There is ultimately no correct way to determine amblyopia in the preverbal child. Behavioral responses of younger children differ from those of their older counterparts. Yet, we must study older children to compare the preverbal tests to the Snellen gold standard of visual acuity testing. Each test must be weighed for ease of clinical use, amount of training needed for personnel, and cost of equipment. The best method of assessing vision may be to use a combination of tests for corroboration.

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Key words: amblyopia, forced preferential looking, visually evoked potential, optokinetic nystagmus

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