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 7° 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 2°
to 3° 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 visual acuity in an otherwise normal, healthy eye. Causes
of amblyopia include refractive error and ocular misalignment.' 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 amblyogenic factors as early as possible. A screening test recommended 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 compares 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.
Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5
Copyright © Association for Research in Vision and Ophthalmology
fraction. The changes in the red reflex arising from
ocular misalignment in the accommodating, focused
eye, however, are less well understood. Roe and Guyton'1 described observations obtained with a beamsplitter 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 ophthalmoscope. They also observed a color change with
a fixation eccentricity greater than 5°.
More recently, Carrera et al5 used a photographic
technique6 to measure the ability of observers to detect the presence of significant asymmetry of pupillary
brightness. They found high sensitivity (82%), specificity (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 brightness as ocular rotation occurs. The obvious application
would be to automate the manual Bruckner test and
compare the light reflexes for asymmetry. A more intriguing application would be the dynamic examination of the binocular reflex as the subject views in the
direction of a fixation target, as proposed by Cibis et
897
898
Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5
7
al. If the variation in pupil brightness reliably changes
in an individual eye with ocular rotation and the minimum always occurs with fixation on the light source, it
may be possible to determine the presence of bilateral
central fixation by the simultaneous presence of pupillary light reflex minima. Our test was performed monocularly. Strabismus was simulated by displacing a
finely detailed "accommodative" fixation target perpendicular to the common axis used for illumination
and viewing of the pupil.
METHODS
The Bruckner Test
The Bruckner, or red reflex, test examines and compares the bright pupils with a paraxial light source
illuminating the eyes. If an eye is focused on the
source, a minified image of the source will be located
on the retina. This image on the retina then serves as
a source for a second pass through the optical system.
The retroreflection at the retina is partly diffuse8 and
partly specular.9 Rays pass back through the pupil and
are refracted by the lens and the cornea. Rays of light
leaving the eye will retrace the paths of the light rays
entering the eye (Fig. 1A).
Photorefraction is the analysis of light distribution
across the pupil when the image formed on the retina
is perturbed by refractive error. Instead of a focused
image forming on the retina, a blurred image forms.
The second pass through the eye further perturbs the
image (Fig. IB), but several methods1011 have been
used to analyze the two-pass system.
The changes in the bright pupil arising from ocular rotation are less well described in the literature.
Again, a two-pass analysis is involved, but the image is
assumed to be perturbed from ocular rotation rather
than from simple refractive error. Four mechanisms
may play a role in the change in pupillary image with
ocular rotation: the specular reflection at the retina
from the internal limiting membrane that changes
slope with ocular rotation (Fig. 1C); changes arising
from variation in retinal pigment density, with the
retina displaying the characteristics of a diffuse reflector (Fig. ID); backscattering of light by the retinal
nerve fiber layer proportional to the thickness of the
layer (Fig. ID); and off-axis aberration12 resulting in
poor image formation on the retina, with further perturbation on the second pass (Fig. ID). We wanted to
evaluate the first three causes; the literature suggests
that off-axis aberrations are not significant over the
range of 0° to 7° used in our experiment.13 As the eye
rotates and the source remains fixed, the image of the
source will fall on different portions of the retina. This
is what occurs in the deviated eye in ocular misalignment.
Nerve fiber layer thickness
Off-axis source points
Image point is blurred
due to aberrations
FIGURE l. (A) Eye focused on point source: By diffuse reflection at the retina, the image on the retina is reimaged back
to the location of the source. The rays retrace themselves
through the system. (B) Eye with refractive error: The first
pass through the eye produces a blurred image of the point
source. The second pass blurs the image more, and the rays
do not retrace themselves. (C) Specular reflection from the
internal limiting membrane (ILM): Rays reflected by the
sloped region of the fovea may be diverted away from the
pupil on the second pass. Rays that miss the pupil on the
second pass are not observed. (D) Off-axis source: Source
is imaged to various regions of the retina that exhibit variation in pigment density and thickness, causing a different
amount of reflection. The eye has increasing aberrations,
with distance of source from axis causing blurred images on
the retina.
Experimental Setup
A 486 personal computer that included a frame grabber board (Dipix, Montreal, Canada) was used to
gather images from adult volunteers. Figure 2 shows
the experimental layout. The light source was a halogen light bulb emitting white light that was fed into
an endoilluminator through an optical fiber. The endoilluminator had a diameter of 50 /im and an angular
subtense at the subject's eye of 0.5 arcmin, which
closely approximated a point source. Based on the
Gullstrand eye model for an accommodated eye,H the
size of the point source on the retina was approxi-
Quantification of the Bruckner Test
899
Calibration
FIGURE 2. Experimental layout for imaging pupil brightness.
Subjectfixateson movable target that simulates ocular misalignment relative to illumination axis. Light source, fixation target, and camera aperture are conjugate to retina. BS
= beamsplitter.
mately 2.26 ^m. The diffraction spot size was calculated to be approximately 4 //m in diameter. The maximum image size for HF, Hed) and H c lines (wavelengths 486 nm, 587 nm, 656 nm) was calculated to
be 2.66 fim diameter, which is smaller than the diffraction spot size. The fixation target was a square 9 pixel
X 9 pixel "happy face" picture on a laptop computer
with a liquid crystal display. This target had an angular
subtense at the eye of 0.4° horizontally and 0.47° vertically. The picture was J1+ print size and could be
centered at any position in the laptop screen. The
fixation distance was 33 cm.
A mechanical shutter was placed between the light
source and the subject. This allowed the illumination
to be flashed briefly (approximately '/ 8 seconds) to
avoid the pupil constriction and retinal bleaching that
occur with constant illumination of the eye by a bright
source. When the shutter was activated by a cable release, a light-emitting diode emitter-receiver pair detected the shutter opening and signaled the computer
to initiate image capture.
Two beamsplitters were used in the optical path.
One beamsplitter combined light from the point
source and the fixation target. The other beamsplitter
reflected the combined target and light source into
the subject's eye and allowed imaging of the pupil by
a charge coupled device (CCD) camera. The camera,
light source, and target appeared coaxial to the subject without any one component occluding either of
the other two.
A 6.6 mm X 8.8 mm format CCD array was used
to image the pupil of the subjects. An 8-mm focal
length iens focused the pupil of the subject onto the
CCD array. An adjustable chin rest was used to achieve
alignment with the subject's pupil.
After the system was assembled, test images were obtained from several subjects. Settings of electronic
gain and offset were established that allowed the
bright pupil to be imaged at camera apertures ranging
from f/1.4 to f/2.8 without saturation of the electronics, while preserving the noise floor from clipping. At
this point, electronic gain and offset were fixed.
At these reference settings, 10 images were obtained without any ambient illumination. These
"dark" images were then analyzed pixel by pixel, and
the average and standard deviation were computed
for each pixel. In the region of the CCD used for
imaging, there was systematic variation in the dark
offset values, but the standard deviation indicated all
pixels were active. The average dark value for each
pixel could then be subtracted from the subject data
to reduce systematic error introduced by the nonuniform response of the CCD.
An artificial bright pupil was then constructed in
which a 9.525-mm diameter aperture, masked by
frosted tape, was retroilluminated uniformly by a yellow light-emitting diode. Images were obtained at various retroillumination levels until a bright pupil could
be 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/2
and f/4. Linear regression was performed, and a linear system response was verified by the linear increase
in brightness with increase in aperture.
The absolute value of the light incident on the
subject's eye, after transit through two beamsplitters,
was measured with a light meter. It was found that 1.3
lux was incident at 33 cm from the source. An absolute
measure of a typical value for light reflected back to
the CCD array was found by using a model eye with a
mirror at the location of the retina. By careful adjustment of the mirror, approximately 90% of the light
entering the pupil could be made to pass out of the
pupil to the CCD camera. Neutral density filters were
added to the path until the light hitting the CCD array
had a value similar to that obtained for a volunteer
(maximum pixel value, 200). The result indicated that
a typical light return from the human eye was approximately 0.02%.
A scale factor was required to calculate the actual
size of features in the captured images based on their
sizes in pixels. The scale factor was determined by
imaging a circle with a diameter of 9.525 mm, which
was found to contain 371 pixels.
Procedure
The 18 subjects were young adults 20 to 40 years of
age, 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
Subject
Number
Age
(years)
1
28
28
25
30
23
39
25
28
28
26
29
23
28
27
25
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
31
24
Gender
Ethnic Group
Eye Color
Refractive
Correction
White
White
White
White
White
White
White
White
White
Asian
White
White
Wliite
White
White
White
White
Asian
Hazel
Hazel
Brown
Brown
Blue
Blue
Blue-green
Brown
Brown
Brown
Brown
Brown
Blue
Blue-green
Brown
Brown
Brown
Brown
Contacts
Contacts
Contacts
None
None
None
None
Contacts
Glasses
Glasses
Contacts
Contacts
Contacts
None
Glasses
Contacts
None
Glasses
F
M
M
M
F
M
M
M
M
M
M
F
M
M
M
M
M
M
of 33 cm, either without correction or with contact
lenses (Table 1). They were healthy volunteers from
the Optical Sciences Center. Informed consent was
obtained from each subject, and the study was approved by the Human Subjects Committee. The tenets
of the Declaration of Helsinki were followed in this
research, and institutional human experimentation
committee approval was granted. The mean age was
27.1 years. Of the subjects, 89% were white and 11%
were Asian. The distribution of eye color among subjects was: 27.8% blue eyes, 61.6% brown eyes, and
11.1% hazel eyes. Five subjects had 20/20 uncorrected
vision. Four subjects had myopia but were able to fixate on the target without glasses. Nine subjects wore
contact lenses to enable fixation during the experiment.
The subject was instructed to set her or his head
in the chin rest and to adjust the chin rest to be able
to see all parts of a rectangle that bordered the area
within which the target was to be placed throughout
the experiment. Final head position was verified by
setting the fixation target at (0,0), triggering the shutter, and asking the subject if the light appeared coincident with the target.
The target was positioned to simulate central fixation and then moved radially outward. Images of the
pupil were taken with the subject gazing 0° (foveal
fixation), 0.25°, 0.5°, 1°, 2°, 3°, 4°, and 5° in eight
different radial directions evenly spaced every 45°. In
six of the radial directions, images also were gathered
at 6° and 7°. Figure 3 illustrates the positions at which
images 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 image, and a 50 X 50 pixel area that included the bright
pupil was extracted from each image. The gray-scale
histogram of the image was computed (Fig. 4A). Figure 4 shows the intermediate results of the processing
performed on the raw data gathered. First, the mean
dark image was subtracted from the raw image to reduce interpixel variation as described in the calibration section. Figure 4B shows a typical flat-field-corrected image and corresponding histogram. The histograms show that by subtracting the dark image from
the raw data, as described in the calibration, the noise
45°
315°
225°'
H
N135
FIGURE 3. Direction of gaze for data points indicated by intersections of circles and lines. Degrees of fixation eccentricity
are indicated and are the same along each of the eight radial
directions.
B
C
D
E
FIGURE 4. (A) A sample 50 X 60 pixel image of a bright pupil and a corresponding grayscale histogram. (B) The image after subtraction of the mean dark image (flat fielding)
and corresponding gray-scale histogram. (C) The binary representation of pixels determined
to be in the pupil. (D) Binary result of a dilation operator to fill in holes and smooth the
edges of the pupil. (E) Final gray-scale representation of the pupil area.
the data is reduced from about 14 parts in 256
MS to about 12 parts in 256 RMS. The initial binary
eshold was then determined by finding the gray
ale threshold value corresponding to the brightest
% of the image pixels. A value of 5% was chosen
cause it represented a maximally dilated pupil size
10 mm diameter. Figure 4C demonstrates the biry output after thresholding. Next, the pupillary reon was located using a connected components algohm and processed with a dilation operator to fill in
ged or missing areas. The results are shown in Fige 4D. The final result was a gray-scale image of the
pil shown in Figure 4E, Figure 5 demonstrates a
l set of data for a single subject. The change in
ghtness with fixation eccentricity is readily appart. Figure 3 shows the direction of gaze for these
ages.
The pixels in the pupil were counted, and, from
s, the area of the pupil in mm2 was determined. If
wer than 20 pixels were detected by the thresholding
ogram, the image was not used. Of the 1334 total
ages captured, 4% were discarded for this reason.
These discarded images represented data at var
values of fixation eccentricity.
It was assumed that the pupil size remained
same for a single subject throughout that subj
data. This assumption was made because the
rounding light level and accommodative effort, w
would influence pupil size, were controlled. The e
ronmental light level was held constant through
the experiment, and the point light source was flas
briefly (% second) with the image gathered (wi
33 msec) before the pupil had a chance to const
Accommodative demand remained fixed through
the experiment. Foreshortening of the area of
pupil as the eye rotated, with a maximum angl
rotation of 7°, was not corrected because it resu
in less than 1 % variation.
Although the pupillary size was assumed to rem
constant throughout the experiment, the obser
size of the bright image varied from image to im
for an arbitrary threshold. The maximum obser
bright pupil for each subject was found, and all o
images were normalized to this size by including b
Degrees of Fixation Eccentricity
0
0.25 0.5
1.0 2.0 3.0 4.0 5.0
6.0
7.0
0
•2
45
S
8
S
U
FIGURE 5. Complete data set gathered for subject 10 before image processing. Degrees of
fixation eccentricity are indicated for the columns. Degrees from horizontal (clockwise) are
indicated for the rows and correspond to Figure 3.
und pixel values with the bright area. The padding
he pupil size with background values ranged from
pixels to 0 pixels, with the maximum pupil size
he subjects varying from 310 pixels (8.7 mm diam) to 110 pixels (5.18 mm diameter). The detected
of the pupil ranged from 42 pixels to 310 pixels.
average brightness per pixel for each image was
n calculated. Any images that contained more than
saturated pixels (gray-scale value 255) in the
ht pupil were discarded.
SULTS
minimum brightness for all subjects was observed
in 0.5° of central fixation. The maximum brightoften appeared at approximately 5° eccentricity.
normalize the data within each subject's set, the
mest gray scale average value was assigned a value
, the brightest 1, and the remaining data were
ed accordingly.
The data for all subjects are summarized in Figure
he normalized data were averaged over all radial
ctions for each amount of fixation eccentricity.
95% confidence intervals were found, and Figure
ows these results.
For the pooled observations, it was determined
0
1
Z
3
4
S
6
7
0
1
2
3
4
5
6
Fixation Eccentricity (Degrees)
FIGURE 6. Summary of data by subject. Data have been a
aged for a given fixation eccentricity over the eight rad
directions. Data have been normalized for each subject
the range of 0 to 1. The standard deviation is shown.
SO
100
ISO
250
200
Thickness of Retinal Layer (microns)
220 T
=• 200 • •
3 180I 160 ••
80Fixation Eccentricity (Degrees)
GURE 7. Summary of normalized results averaged for all
bjects. The 95% confidence intervals for the data are
own.
hat the brightness from 2° to 7° could be distinuished from the brightness from 0° to 0.5°. Figure
gives a graphic representation of the variation in
rightness observed with varying degrees of ocular
misalignment. The brightness values correspond to
hose illustrated in Figure 7 along the left-hand side
f the graph.
We observed that the shape of our graph of pupil
rightness versus distance from the center of the fovea
esembles the variation in thickness of the retina in
hat region. A plot of observed pupil brightness versus
etinal thickness15 is shown in Figure 9. The plot has
n r2 value of 0.96,
ISCUSSION
nterpretation of these data is somewhat speculative.
n the present experiment, neither defocus nor varia-
GURE 8. Gray-scale representation of the average brightess observed versus fixation eccentricity.
i f 60"
40- •
It
I 140-
20 •
0
0.2
0.4
% 120'
| 100"
80 40
0.6
0.2
0.4
Distance Iran Fixation (mm)
FIGURE 9. (A) Observed brightness versus thickness of r
nerve fiber layer.15 (B) Comparison of observed brigh
and retinal thickness versus distance from fixation.
tion in pupil size can be responsible for the obse
variation of pupillary brightness. Only the effect
duced by ocular rotation are observed. Does the
reflex brighten with eccentric fixation because o
axis aberrations, decreased absorption by pigm
away from the fovea, more specular reflection
the internal limiting membrane returning thro
the pupil, or simply increased backscattering of
from the thicker retinal layers as the image m
away from the fovea centralis?
Off-axis aberrations are unlikely to be the c
given that the fovea itself is off-axis, and the minim
is observed with foveal fixation. Off-axis aberra
may play a role with larger angles,13 but over our r
of data the results are remarkably symmetric a
the fovea.
Increased pigment density may be responsibl
the observed diminution at fixation. The incre
pigment density would have to increase as the fov
is approached. This increase in pigment would c
less light to be reflected, and the reflex would ass
the color of the pigment. We used white light and
not analyze the returned spectra so we cannot exc
this mechanism, but the sharpness of the minim
observed is not in keeping with clinical observa
of macular pigment density.
Another hypothesis is that the internal lim
membrane of the retina acts as a source of signif
specular reflection.4'9 The foveola subtends
Along the edges of the foveal pit, the steep angle
result in significant light being reflected away from
pupil and may account for the decrease in pup
brightness observed within 1° of fixation. This hy
esis would also account for the decrease in obse
904
Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5
brightness from reflection farther out in the periphery
of the retina. On the other hand, such a mechanism
would predict maximum brightness from reflection
from the very center of the foveal pit where the incident ray is normal to the surface. Such a "hot spot"
at the center of fixation was never seen. Our subjects
were older (mean age, 27.1 years) than the young
children routinely screened using the Bruckner test.
It is possible that the internal limiting membrane reflectivity decreases significantly with increasing age,
perhaps blunting the effect observed. However, none
of our subjects was likely to have a posterior vitreous
detachment on the basis of age.
If the retinal layers act as scattering medium, more
light would be backscattered in the thicker regions
than in the thinner regions. In thinner regions, where
pigment density is also greatest, more light would
reach the pigment epithelium and be absorbed. In
thicker regions of the retina, more backscatter would
occur, resulting in more light returning through the
pupil. Such backscattering would correlate with our
observations as shown in Figure 9, with clinical observations of the nerve fiber layer. Thick nerve fiber layers
partially obscure the outlines of underlying vessels because of the light scattering that occurs.16
We suspect that all the above factors play a role
over the range of angles observed. Artal and Navarro17
examined the two-pass point spread function simultaneously at fixation and at 1° of eccentricity. Within
this region, the specular component dominated the
changes observed. As the eccentricity increases, the
slope 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 the
response that is observed allows predictions to be
made about binocular changes in the red reflex with
strabismus. We have begun work to model the expected results of using this technique in a binocular
setting. The model assumes one eye fixating on a target while the other eye is deviated a constant amount.
The fixating eye is modeled to have fixation instability
less than 1°. Figure 10A shows the expected correlation of right and left eye pupil brightness with no
strabismus present and with symmetric responses between the eyes. Brightness values are assigned based
on the results from Figure 7. The brightness of the
"fixating" eye versus the fellow eye is plotted for 200
simulations with no strabismus. The model thus predicts that for binocular, foveal fixation, the data points
form a line with a slope of 1. Figure 10B predicts how
pupil brightness changes in the presence of 2 prism
diopters (1.15°) of strabismus with the same fixation
instability.
300-,-
200-CD
LLJ
100-.
0
A
o
100
200
300
Right Eye
250
•Hi
1
.il 1 '
200
<» 1 5 0
ai
% 100
^ i . ] !••'
_J
50
50
B
100
150 200
Right Eye
250
FIGURE 10. Computer simulation results of the brightness
detected for each eye. One eyefixateson a target with some
gaze instability, and the second eye has some misalignment
relative to the first eye of (A) 0 prism diopters and (B) 2
prism diopters.
Comparison of Figures 10A and 10B reveals that
if many repeated measures of simultaneous pupil
brightness can be obtained, it may be possible to detect bifoveal fixation on a statistical basis. The method
would require recognizing the line of unity present in
Figure 10A under bifoveal fixation that is transformed
into a locus of points that largely excludes the line of
unity in Figure 10B in the presence of strabismus. It
is likely that 2 prism diopters or more of strabismus
could be detected, but the determination of the exact
amount would be difficult, and differentiation be-
Quantification of the Bruckner Test
tween esotropia and exotropia would probably not be
possible without additional data.
A significant limiting factor in the present data is
CCD camera noise. Our system was limited by how
bright a point source could be achieved. To image
the pupil, camera gain was maximal, resulting in interpixel background noise of approximately 16 parts in
256 RMS. Addition of noise of this magnitude renders
the distinction between Figure 10A and Figure 10B
patterns more difficult. This problem may be addressed by increasing the point source illumination
and reducing camera noise.
In summary, we have documented the monocular
change in pupil image brightness, from fundus reflection of coaxial illumination, with fixation eccentricity
of up to 7°. This phenomenon, although widely observed as part of the Bruckner or red reflex test, has
not been systematically used in a screening instrument
for strabismus. Our results suggest that asymmetry of
the red reflex may reliably be detected with ocular
misalignment as small as 2°.
Key Words
amblyopia, image analysis, strabismus, retinal reflectivity, optics
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