Quantification of the Bruckner Test for Strabismus · Quantification of the Bruckner Test 899...

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Quantification of the Bruckner Test for Strabismus Joseph M. Miller*^ Heidi Leising Hall,\ John E. Greivenkamp,*-\ and David L. Guyton% Purpose. To measure quantitatively the change in the coaxial fundus reflex with varying degrees of ocular misalignment. Methods. The coaxial fundus reflex was imaged with a charge coupled device camera under conditions of simulated ocular misalignment ranging from 0° to offixationeccentricity. The effects of refractive error and pupil size were controlled. Average gray scale brightness values were calculated for each bright pupil image after some image processing was performed on the raw images. Results. A reliable, sharply delineated, minimum brightness at fovealfixationwas observed. Conclusions. It is estimated that this technique can be automated to detect the presence of to of ocular misalignment based on the difference in brightness of the bright pupil images between the two eyes. Invest Ophthalmol Vis Sci. 1995;36:897-905. A Amblyopia ("lazy eye") is described as decreased vi- sual acuity in an otherwise normal, healthy eye. Causes of amblyopia include refractive error and ocular mis- alignment.' In patients in which the problem is found at an early age, the problem is often correctable. Thus, it is of utmost importance to detect possibly amblyo- genic factors as early as possible. A screening test rec- ommended for use by primary care providers is the red reflex, or Bruckner, test. 23 In this test, a bright paraxial light source such as a direct ophthalmoscope is used to illuminate both eyes of the subject from a distance of approximately 1 m. The examiner com- pares the brightness of the two red fundus reflexes for evidence of asymmetry. If the subject is fixating on the light, any asymmetry of the pupil brightness indicates the presence of a potentially amblyogenic factor, be that cataract, anisometropia, or strabismus. In the case of anisometropia or strabismus, the brighter reflex is said to indicate the problematic eye. Changes in the red reflex with refractive error have been well studied and are the basis of photore- From the "Department of Ophthalmology, Optical Sciences Center, University of Arizona, Tucson, Arizona, and lhe%Wilmer Ophlhalmological Institute, Johns Hopkins University, Baltimore, Maryland. Supported by the Whitaker Foundation for Biomedical Research, Washington, DC, and by The Sensory Research Foundation, Phoenix, Arizona. Submitted for publication September 7, 1994; revised November 9, 1994; accepted November 11, 1994. Proprietary interest category: N. Reprint requests; Josejih Miller, Department of Ophthalmology, 1801 N. Campbell Ave, Tucson, AZ 85719. fraction. The changes in the red reflex arising from ocular misalignment in the accommodating, focused eye, however, are less well understood. Roe and Guy- ton' 1 described observations obtained with a beamsplit- ter ophthalmoscope, in which a true coaxial light source was used for fundus illumination. The change in the red reflex with ocular rotation was described but not measured. The reflex was said to dim with fixation, although not as much as with a regular oph- thalmoscope. They also observed a color change with a fixation eccentricity greater than 5°. More recently, Carrera et al 5 used a photographic technique 6 to measure the ability of observers to de- tect the presence of significant asymmetry of pupillary brightness. They found high sensitivity (82%), speci- ficity (91%), and accuracy (84%) in the screening of groups of subjects with small angle esotropia, large angle esotropia, anisometropia of 3 D, and normal subjects (26 subjects each group). This study used the simple judgment of asymmetry by a skilled or unskilled observer rather than a quantitative measure of the red reflex. We wanted to quantify the change in pupil bright- ness as ocular rotation occurs. The obvious application would be to automate the manual Bruckner test and compare the light reflexes for asymmetry. A more in- triguing application would be the dynamic examina- tion of the binocular reflex as the subject views in the direction of a fixation target, as proposed by Cibis et Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5 Copyright © Association for Research in Vision and Ophthalmology 897

Transcript of Quantification of the Bruckner Test for Strabismus · Quantification of the Bruckner Test 899...

Quantification of the Bruckner Test for Strabismus

Joseph M. Miller*^ Heidi Leising Hall,\ John E. Greivenkamp,*-\ and David L. Guyton%

Purpose. To measure quantitatively the change in the coaxial fundus reflex with varying degreesof ocular misalignment.

Methods. The coaxial fundus reflex was imaged with a charge coupled device camera underconditions of simulated ocular misalignment ranging from 0° to 7° of fixation eccentricity.The effects of refractive error and pupil size were controlled. Average gray scale brightnessvalues were calculated for each bright pupil image after some image processing was performedon the raw images.

Results. A reliable, sharply delineated, minimum brightness at foveal fixation was observed.

Conclusions. It is estimated that this technique can be automated to detect the presence of 2°to 3° of ocular misalignment based on the difference in brightness of the bright pupil imagesbetween the two eyes. Invest Ophthalmol Vis Sci. 1995;36:897-905.

A

Amblyopia ("lazy eye") is described as decreased vi-sual acuity in an otherwise normal, healthy eye. Causesof amblyopia include refractive error and ocular mis-alignment.' In patients in which the problem is foundat an early age, the problem is often correctable. Thus,it is of utmost importance to detect possibly amblyo-genic factors as early as possible. A screening test rec-ommended for use by primary care providers is thered reflex, or Bruckner, test.23 In this test, a brightparaxial light source such as a direct ophthalmoscopeis used to illuminate both eyes of the subject from adistance of approximately 1 m. The examiner com-pares the brightness of the two red fundus reflexesfor evidence of asymmetry. If the subject is fixatingon the light, any asymmetry of the pupil brightnessindicates the presence of a potentially amblyogenicfactor, be that cataract, anisometropia, or strabismus.In the case of anisometropia or strabismus, thebrighter reflex is said to indicate the problematic eye.

Changes in the red reflex with refractive errorhave been well studied and are the basis of photore-

From the "Department of Ophthalmology, Optical Sciences Center, University ofArizona, Tucson, Arizona, and lhe%Wilmer Ophlhalmological Institute, JohnsHopkins University, Baltimore, Maryland.Supported by the Whitaker Foundation for Biomedical Research, Washington, DC,and by The Sensory Research Foundation, Phoenix, Arizona.Submitted for publication September 7, 1994; revised November 9, 1994; acceptedNovember 11, 1994.Proprietary interest category: N.Reprint requests; Josejih Miller, Department of Ophthalmology, 1801 N. CampbellAve, Tucson, AZ 85719.

fraction. The changes in the red reflex arising fromocular misalignment in the accommodating, focusedeye, however, are less well understood. Roe and Guy-ton'1 described observations obtained with a beamsplit-ter ophthalmoscope, in which a true coaxial lightsource was used for fundus illumination. The changein the red reflex with ocular rotation was describedbut not measured. The reflex was said to dim withfixation, although not as much as with a regular oph-thalmoscope. They also observed a color change witha fixation eccentricity greater than 5°.

More recently, Carrera et al5 used a photographictechnique6 to measure the ability of observers to de-tect the presence of significant asymmetry of pupillarybrightness. They found high sensitivity (82%), speci-ficity (91%), and accuracy (84%) in the screening ofgroups of subjects with small angle esotropia, largeangle esotropia, anisometropia of 3 D, and normalsubjects (26 subjects each group). This study used thesimple judgment of asymmetry by a skilled or unskilledobserver rather than a quantitative measure of the redreflex.

We wanted to quantify the change in pupil bright-ness as ocular rotation occurs. The obvious applicationwould be to automate the manual Bruckner test andcompare the light reflexes for asymmetry. A more in-triguing application would be the dynamic examina-tion of the binocular reflex as the subject views in thedirection of a fixation target, as proposed by Cibis et

Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5Copyright © Association for Research in Vision and Ophthalmology 897

898 Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5

al.7 If the variation in pupil brightness reliably changesin an individual eye with ocular rotation and the mini-mum always occurs with fixation on the light source, itmay be possible to determine the presence of bilateralcentral fixation by the simultaneous presence of pupil-lary light reflex minima. Our test was performed mon-ocularly. Strabismus was simulated by displacing afinely detailed "accommodative" fixation target per-pendicular to the common axis used for illuminationand viewing of the pupil.

METHODS

The Bruckner Test

The Bruckner, or red reflex, test examines and com-pares the bright pupils with a paraxial light sourceilluminating the eyes. If an eye is focused on thesource, a minified image of the source will be locatedon the retina. This image on the retina then serves asa source for a second pass through the optical system.The retroreflection at the retina is partly diffuse8 andpartly specular.9 Rays pass back through the pupil andare refracted by the lens and the cornea. Rays of lightleaving the eye will retrace the paths of the light raysentering the eye (Fig. 1A).

Photorefraction is the analysis of light distributionacross the pupil when the image formed on the retinais perturbed by refractive error. Instead of a focusedimage forming on the retina, a blurred image forms.The second pass through the eye further perturbs theimage (Fig. IB), but several methods1011 have beenused to analyze the two-pass system.

The changes in the bright pupil arising from ocu-lar rotation are less well described in the literature.Again, a two-pass analysis is involved, but the image isassumed to be perturbed from ocular rotation ratherthan from simple refractive error. Four mechanismsmay play a role in the change in pupillary image withocular rotation: the specular reflection at the retinafrom the internal limiting membrane that changesslope with ocular rotation (Fig. 1C); changes arisingfrom variation in retinal pigment density, with theretina displaying the characteristics of a diffuse reflec-tor (Fig. ID); backscattering of light by the retinalnerve fiber layer proportional to the thickness of thelayer (Fig. ID); and off-axis aberration12 resulting inpoor image formation on the retina, with further per-turbation on the second pass (Fig. ID). We wanted toevaluate the first three causes; the literature suggeststhat off-axis aberrations are not significant over therange of 0° to 7° used in our experiment.13 As the eyerotates and the source remains fixed, the image of thesource will fall on different portions of the retina. Thisis what occurs in the deviated eye in ocular misalign-ment.

Nerve fiber layer thickness

Off-axis source points

Image point is blurreddue to aberrations

FIGURE l. (A) Eye focused on point source: By diffuse reflec-tion at the retina, the image on the retina is reimaged backto the location of the source. The rays retrace themselvesthrough the system. (B) Eye with refractive error: The firstpass through the eye produces a blurred image of the pointsource. The second pass blurs the image more, and the raysdo not retrace themselves. (C) Specular reflection from theinternal limiting membrane (ILM): Rays reflected by thesloped region of the fovea may be diverted away from thepupil on the second pass. Rays that miss the pupil on thesecond pass are not observed. (D) Off-axis source: Sourceis imaged to various regions of the retina that exhibit varia-tion in pigment density and thickness, causing a differentamount of reflection. The eye has increasing aberrations,with distance of source from axis causing blurred images onthe retina.

Experimental SetupA 486 personal computer that included a frame grab-ber board (Dipix, Montreal, Canada) was used togather images from adult volunteers. Figure 2 showsthe experimental layout. The light source was a halo-gen light bulb emitting white light that was fed intoan endoilluminator through an optical fiber. The en-doilluminator had a diameter of 50 /im and an angularsubtense at the subject's eye of 0.5 arcmin, whichclosely approximated a point source. Based on theGullstrand eye model for an accommodated eye,H thesize of the point source on the retina was approxi-

Quantification of the Bruckner Test 899

FIGURE 2. Experimental layout for imaging pupil brightness.Subject fixates on movable target that simulates ocular mis-alignment relative to illumination axis. Light source, fixa-tion target, and camera aperture are conjugate to retina. BS= beamsplitter.

mately 2.26 ^m. The diffraction spot size was calcu-lated to be approximately 4 //m in diameter. The maxi-mum image size for HF, Hed) and Hc lines (wave-lengths 486 nm, 587 nm, 656 nm) was calculated tobe 2.66 fim diameter, which is smaller than the diffrac-tion spot size. The fixation target was a square 9 pixelX 9 pixel "happy face" picture on a laptop computerwith a liquid crystal display. This target had an angularsubtense at the eye of 0.4° horizontally and 0.47° verti-cally. The picture was J1+ print size and could becentered at any position in the laptop screen. Thefixation distance was 33 cm.

A mechanical shutter was placed between the lightsource and the subject. This allowed the illuminationto be flashed briefly (approximately '/8 seconds) toavoid the pupil constriction and retinal bleaching thatoccur with constant illumination of the eye by a brightsource. When the shutter was activated by a cable re-lease, a light-emitting diode emitter-receiver pair de-tected the shutter opening and signaled the computerto initiate image capture.

Two beamsplitters were used in the optical path.One beamsplitter combined light from the pointsource and the fixation target. The other beamsplitterreflected the combined target and light source intothe subject's eye and allowed imaging of the pupil bya charge coupled device (CCD) camera. The camera,light source, and target appeared coaxial to the sub-ject without any one component occluding either ofthe other two.

A 6.6 mm X 8.8 mm format CCD array was usedto image the pupil of the subjects. An 8-mm focallength iens focused the pupil of the subject onto theCCD array. An adjustable chin rest was used to achievealignment with the subject's pupil.

Calibration

After the system was assembled, test images were ob-tained from several subjects. Settings of electronicgain and offset were established that allowed thebright pupil to be imaged at camera apertures rangingfrom f/1.4 to f/2.8 without saturation of the electron-ics, while preserving the noise floor from clipping. Atthis point, electronic gain and offset were fixed.

At these reference settings, 10 images were ob-tained without any ambient illumination. These"dark" images were then analyzed pixel by pixel, andthe average and standard deviation were computedfor each pixel. In the region of the CCD used forimaging, there was systematic variation in the darkoffset values, but the standard deviation indicated allpixels were active. The average dark value for eachpixel could then be subtracted from the subject datato reduce systematic error introduced by the nonuni-form response of the CCD.

An artificial bright pupil was then constructed inwhich a 9.525-mm diameter aperture, masked byfrosted tape, was retroilluminated uniformly by a yel-low light-emitting diode. Images were obtained at vari-ous retroillumination levels until a bright pupil couldbe imaged at camera aperture f/1.4 without clipping.The light-emitting diode power level was then fixed,and images were obtained at camera apertures f/2and f/4. Linear regression was performed, and a lin-ear system response was verified by the linear increasein brightness with increase in aperture.

The absolute value of the light incident on thesubject's eye, after transit through two beamsplitters,was measured with a light meter. It was found that 1.3lux was incident at 33 cm from the source. An absolutemeasure of a typical value for light reflected back tothe CCD array was found by using a model eye with amirror at the location of the retina. By careful adjust-ment of the mirror, approximately 90% of the lightentering the pupil could be made to pass out of thepupil to the CCD camera. Neutral density filters wereadded to the path until the light hitting the CCD arrayhad a value similar to that obtained for a volunteer(maximum pixel value, 200). The result indicated thata typical light return from the human eye was approxi-mately 0.02%.

A scale factor was required to calculate the actualsize of features in the captured images based on theirsizes in pixels. The scale factor was determined byimaging a circle with a diameter of 9.525 mm, whichwas found to contain 371 pixels.

Procedure

The 18 subjects were young adults 20 to 40 years ofage, each able to read Jl + (3-point) print at a distance

900 Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5

TABLE l. Summary of Subject Data

SubjectNumber

123456789

101112131415161718

Age(years)

282825302339252828262923282725193124

Gender

FMMMFMMMMMMFMMMMMM

Ethnic Group

WhiteWhiteWhiteWhiteWhiteWhiteWhiteWhiteWhiteAsianWhiteWhiteWliiteWhiteWhiteWhiteWhiteAsian

Eye Color

HazelHazelBrownBrownBlueBlueBlue-greenBrownBrownBrownBrownBrownBlueBlue-greenBrownBrownBrownBrown

RefractiveCorrection

ContactsContactsContactsNoneNoneNoneNoneContactsGlassesGlassesContactsContactsContactsNoneGlassesContactsNoneGlasses

of 33 cm, either without correction or with contactlenses (Table 1). They were healthy volunteers fromthe Optical Sciences Center. Informed consent wasobtained from each subject, and the study was ap-proved by the Human Subjects Committee. The tenetsof the Declaration of Helsinki were followed in thisresearch, and institutional human experimentationcommittee approval was granted. The mean age was27.1 years. Of the subjects, 89% were white and 11%were Asian. The distribution of eye color among sub-jects was: 27.8% blue eyes, 61.6% brown eyes, and11.1% hazel eyes. Five subjects had 20/20 uncorrectedvision. Four subjects had myopia but were able to fix-ate on the target without glasses. Nine subjects worecontact lenses to enable fixation during the experi-ment.

The subject was instructed to set her or his headin the chin rest and to adjust the chin rest to be ableto see all parts of a rectangle that bordered the areawithin which the target was to be placed throughoutthe experiment. Final head position was verified bysetting the fixation target at (0,0), triggering the shut-ter, and asking the subject if the light appeared coinci-dent with the target.

The target was positioned to simulate central fixa-tion and then moved radially outward. Images of thepupil were taken with the subject gazing 0° (fovealfixation), 0.25°, 0.5°, 1°, 2°, 3°, 4°, and 5° in eightdifferent radial directions evenly spaced every 45°. Insix of the radial directions, images also were gatheredat 6° and 7°. Figure 3 illustrates the positions at whichimages were gathered.

The initial images gathered were 640 X 480 pixels.Image processing software, written in the C language,

was used to detect the bright pupil section in the im-age, and a 50 X 50 pixel area that included the brightpupil was extracted from each image. The gray-scalehistogram of the image was computed (Fig. 4A). Fig-ure 4 shows the intermediate results of the processingperformed on the raw data gathered. First, the meandark image was subtracted from the raw image to re-duce interpixel variation as described in the calibra-tion section. Figure 4B shows a typical flat-field-cor-rected image and corresponding histogram. The his-tograms show that by subtracting the dark image fromthe raw data, as described in the calibration, the noise

315°

H225°'

45°

N135

FIGURE 3. Direction of gaze for data points indicated by inter-sections of circles and lines. Degrees of fixation eccentricityare indicated and are the same along each of the eight radialdirections.

Quantification of the Bruckner Test 901

B

C D EFIGURE 4. (A) A sample 50 X 60 pixel image of a bright pupil and a corresponding gray-scale histogram. (B) The image after subtraction of the mean dark image (flat fielding)and corresponding gray-scale histogram. (C) The binary representation of pixels determinedto be in the pupil. (D) Binary result of a dilation operator to fill in holes and smooth theedges of the pupil. (E) Final gray-scale representation of the pupil area.

in the data is reduced from about 14 parts in 256RMS to about 12 parts in 256 RMS. The initial binarythreshold was then determined by finding the grayscale threshold value corresponding to the brightest5% of the image pixels. A value of 5% was chosenbecause it represented a maximally dilated pupil sizeof 10 mm diameter. Figure 4C demonstrates the bi-nary output after thresholding. Next, the pupillary re-gion was located using a connected components algo-rithm and processed with a dilation operator to fill injagged or missing areas. The results are shown in Fig-ure 4D. The final result was a gray-scale image of thepupil shown in Figure 4E, Figure 5 demonstrates afull set of data for a single subject. The change inbrightness with fixation eccentricity is readily appar-ent. Figure 3 shows the direction of gaze for theseimages.

The pixels in the pupil were counted, and, fromthis, the area of the pupil in mm2 was determined. Iffewer than 20 pixels were detected by the thresholdingprogram, the image was not used. Of the 1334 totalimages captured, 4% were discarded for this reason.

These discarded images represented data at variousvalues of fixation eccentricity.

It was assumed that the pupil size remained thesame for a single subject throughout that subject'sdata. This assumption was made because the sur-rounding light level and accommodative effort, whichwould influence pupil size, were controlled. The envi-ronmental light level was held constant throughoutthe experiment, and the point light source was flashedbriefly (% second) with the image gathered (within33 msec) before the pupil had a chance to constrict.Accommodative demand remained fixed throughoutthe experiment. Foreshortening of the area of thepupil as the eye rotated, with a maximum angle ofrotation of 7°, was not corrected because it resultedin less than 1 % variation.

Although the pupillary size was assumed to remainconstant throughout the experiment, the observedsize of the bright image varied from image to imagefor an arbitrary threshold. The maximum observedbright pupil for each subject was found, and all otherimages were normalized to this size by including back-

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Degrees of Fixation Eccentricity

0 0.25 0.5 1.0 2.0 3.0 4.0 5.0 6.0 7.0

J

FIGURE 5. Complete data set gathered for subject 10 before image processing. Degrees offixation eccentricity are indicated for the columns. Degrees from horizontal (clockwise) areindicated for the rows and correspond to Figure 3.

ground pixel values with the bright area. The paddingof the pupil size with background values ranged from263 pixels to 0 pixels, with the maximum pupil sizefor the subjects varying from 310 pixels (8.7 mm diam-eter) to 110 pixels (5.18 mm diameter). The detectedsize of the pupil ranged from 42 pixels to 310 pixels.The average brightness per pixel for each image wasthen calculated. Any images that contained more than10% saturated pixels (gray-scale value 255) in thebright pupil were discarded.

RESULTS

The minimum brightness for all subjects was observedwithin 0.5° of central fixation. The maximum bright-ness often appeared at approximately 5° eccentricity.To normalize the data within each subject's set, thedimmest gray scale average value was assigned a valueof 0, the brightest 1, and the remaining data werescaled accordingly.

The data for all subjects are summarized in Figure6. The normalized data were averaged over all radialdirections for each amount of fixation eccentricity.The 95% confidence intervals were found, and Figure7 shows these results.

For the pooled observations, it was determined

0 1 Z 3 4 S 6 7 0 1 2 3 4 5 6 7

Fixation Eccentricity (Degrees)

FIGURE 6. Summary of data by subject. Data have been aver-aged for a given fixation eccentricity over the eight radialdirections. Data have been normalized for each subject tothe range of 0 to 1. The standard deviation is shown.

Quantification of the Bruckner Test 903

Fixation Eccentricity (Degrees)

FIGURE 7. Summary of normalized results averaged for allsubjects. The 95% confidence intervals for the data areshown.

that the brightness from 2° to 7° could be distin-guished from the brightness from 0° to 0.5°. Figure8 gives a graphic representation of the variation inbrightness observed with varying degrees of ocularmisalignment. The brightness values correspond tothose illustrated in Figure 7 along the left-hand sideof the graph.

We observed that the shape of our graph of pupilbrightness versus distance from the center of the fovearesembles the variation in thickness of the retina inthat region. A plot of observed pupil brightness versusretinal thickness15 is shown in Figure 9. The plot hasan r2 value of 0.96,

DISCUSSION

Interpretation of these data is somewhat speculative.In the present experiment, neither defocus nor varia-

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Thickness of Retinal Layer (microns)

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0.2 0.4 0.6 0.2 0.4 0.6

FIGURE 8. Gray-scale representation of the average bright-ness observed versus fixation eccentricity.

Distance Iran Fixation (mm)

FIGURE 9. (A) Observed brightness versus thickness of retinalnerve fiber layer.15 (B) Comparison of observed brightnessand retinal thickness versus distance from fixation.

tion in pupil size can be responsible for the observedvariation of pupillary brightness. Only the effects in-duced by ocular rotation are observed. Does the redreflex brighten with eccentric fixation because of off-axis aberrations, decreased absorption by pigmentaway from the fovea, more specular reflection fromthe internal limiting membrane returning throughthe pupil, or simply increased backscattering of lightfrom the thicker retinal layers as the image movesaway from the fovea centralis?

Off-axis aberrations are unlikely to be the cause,given that the fovea itself is off-axis, and the minimumis observed with foveal fixation. Off-axis aberrationsmay play a role with larger angles,13 but over our rangeof data the results are remarkably symmetric aboutthe fovea.

Increased pigment density may be responsible forthe observed diminution at fixation. The increasedpigment density would have to increase as the foveolais approached. This increase in pigment would causeless light to be reflected, and the reflex would assumethe color of the pigment. We used white light and didnot analyze the returned spectra so we cannot excludethis mechanism, but the sharpness of the minimumobserved is not in keeping with clinical observationsof macular pigment density.

Another hypothesis is that the internal limitingmembrane of the retina acts as a source of significantspecular reflection.4'9 The foveola subtends <2°.Along the edges of the foveal pit, the steep angle mayresult in significant light being reflected away from thepupil and may account for the decrease in pupillarybrightness observed within 1° of fixation. This hypoth-esis would also account for the decrease in observed

904 Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5

brightness from reflection farther out in the peripheryof the retina. On the other hand, such a mechanismwould predict maximum brightness from reflectionfrom the very center of the foveal pit where the inci-dent ray is normal to the surface. Such a "hot spot"at the center of fixation was never seen. Our subjectswere older (mean age, 27.1 years) than the youngchildren routinely screened using the Bruckner test.It is possible that the internal limiting membrane re-flectivity decreases significantly with increasing age,perhaps blunting the effect observed. However, noneof our subjects was likely to have a posterior vitreousdetachment on the basis of age.

If the retinal layers act as scattering medium, morelight would be backscattered in the thicker regionsthan in the thinner regions. In thinner regions, wherepigment density is also greatest, more light wouldreach the pigment epithelium and be absorbed. Inthicker regions of the retina, more backscatter wouldoccur, resulting in more light returning through thepupil. Such backscattering would correlate with ourobservations as shown in Figure 9, with clinical obser-vations of the nerve fiber layer. Thick nerve fiber layerspartially obscure the outlines of underlying vessels be-cause of the light scattering that occurs.16

We suspect that all the above factors play a roleover the range of angles observed. Artal and Navarro17

examined the two-pass point spread function simulta-neously at fixation and at 1° of eccentricity. Withinthis region, the specular component dominated thechanges observed. As the eccentricity increases, theslope of the internal limiting membrane decreases,the incident ray is perpendicular to the retina surface,gross color changes become more clinically apparent,and brightness increases.

Regardless of the mechanism, the steepness of theresponse that is observed allows predictions to bemade about binocular changes in the red reflex withstrabismus. We have begun work to model the ex-pected results of using this technique in a binocularsetting. The model assumes one eye fixating on a tar-get while the other eye is deviated a constant amount.The fixating eye is modeled to have fixation instabilityless than 1°. Figure 10A shows the expected correla-tion of right and left eye pupil brightness with nostrabismus present and with symmetric responses be-tween the eyes. Brightness values are assigned basedon the results from Figure 7. The brightness of the"fixating" eye versus the fellow eye is plotted for 200simulations with no strabismus. The model thus pre-dicts that for binocular, foveal fixation, the data pointsform a line with a slope of 1. Figure 10B predicts howpupil brightness changes in the presence of 2 prismdiopters (1.15°) of strabismus with the same fixationinstability.

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FIGURE 10. Computer simulation results of the brightnessdetected for each eye. One eye fixates on a target with somegaze instability, and the second eye has some misalignmentrelative to the first eye of (A) 0 prism diopters and (B) 2prism diopters.

Comparison of Figures 10A and 10B reveals thatif many repeated measures of simultaneous pupilbrightness can be obtained, it may be possible to de-tect bifoveal fixation on a statistical basis. The methodwould require recognizing the line of unity present inFigure 10A under bifoveal fixation that is transformedinto a locus of points that largely excludes the line ofunity in Figure 10B in the presence of strabismus. Itis likely that 2 prism diopters or more of strabismuscould be detected, but the determination of the exactamount would be difficult, and differentiation be-

Quantification of the Bruckner Test 905

tween esotropia and exotropia would probably not bepossible without additional data.

A significant limiting factor in the present data isCCD camera noise. Our system was limited by howbright a point source could be achieved. To imagethe pupil, camera gain was maximal, resulting in inter-pixel background noise of approximately 16 parts in256 RMS. Addition of noise of this magnitude rendersthe distinction between Figure 10A and Figure 10Bpatterns more difficult. This problem may be ad-dressed by increasing the point source illuminationand reducing camera noise.

In summary, we have documented the monocularchange in pupil image brightness, from fundus reflec-tion of coaxial illumination, with fixation eccentricityof up to 7°. This phenomenon, although widely ob-served as part of the Bruckner or red reflex test, hasnot been systematically used in a screening instrumentfor strabismus. Our results suggest that asymmetry ofthe red reflex may reliably be detected with ocularmisalignment as small as 2°.

Key Words

amblyopia, image analysis, strabismus, retinal reflectivity, op-tics

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