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ORIGINAL ARTICLE
Effect of Amblyopia on the Developmental Eye
Movement Test in Children
Ann L. Webber*, Joanne M. Wood†
, Glen A. Gole‡
, and Brian Brown†
ABSTRACT
Purpose. To investigate the functional impact of amblyopia in children, the performance of amblyopic and age-matched
control children on a clinical test of eye movements was compared. The influence of visual factors on test outcome
measures was explored.
Methods. Eye movements were assessed with the Developmental Eye Movement (DEM) test, in a group of children with
amblyopia (n ϭ 39; age, 9.1 Ϯ 0.9 years) of different causes (infantile esotropia, n ϭ 7; acquired strabismus, n ϭ 10;
anisometropia, n ϭ 8; mixed, n ϭ 8; deprivation, n ϭ 6) and in an age-matched control group (n ϭ 42; age, 9.3 Ϯ 0.4
years). LogMAR visual acuity (VA), stereoacuity, and refractive error were also recorded in both groups.
Results. No significant difference was found between the amblyopic and age-matched control group for any of the
outcome measures of the DEM (vertical time, horizontal time, number of errors and ratio(horizontal time/vertical time)). The DEM
measures were not significantly related to VA in either eye, level of binocular function (stereoacuity), history of
strabismus, or refractive error.
Conclusions. The performance of amblyopic children on the DEM, a commonly used clinical measure of eye movements,
has not previously been reported. Under habitual binocular viewing conditions, amblyopia has no effect on DEM
outcome scores despite significant impairment of binocular vision and decreased VA in both the better and worse eye.
(Optom Vis Sci 2009;86:760–766)
Key Words: amblyopia, eye movements, DEM, binocular vision, strabismus
A
pproximately 3% of the population develop amblyopia,1,2
which is generally defined as poor vision resulting from ab-
normal visual experience during early childhood. Children
with amblyopia may have poorer visual acuity (VA) in both affected
and fellow eye, little or no stereopsis or binocular fusion, and poorer
efficiency in their accommodation and oculo-motor control.3
Al-
though much has been reported regarding the visual characteristics of
amblyopia and the neurological adaptations that underlie these ef-
fects,3–5
there is little published evidence of the disability associated
withamblyopia.6
Inparticular,therehasbeenonlylimitedresearchon
the impact of amblyopia on the ability to complete activities of daily
living that impact on career opportunities or career choices for am-
blyopes,6
or on tasks pertinent to the activities of amblyopic children
and their educational achievement.7
Persons with a history of ambly-
opia are reported to feel that it has affected their school and career
choices;8–10
however, a recent birth cohort study, involving 8861
participants, reported that amblyopia did not significantly impact on
educational, health, or social outcomes.11
In addition to having reduced VA, contrast sensitivity and hyper-
acuity,3
amblyopes have poorer control of fixation in both the ambly-
opic and non-amblyopic eye,12
and binocular coordination of
saccades is impaired in strabismic amblyopes, particularly those with
large angle strabismus.13
Although a causal relationship between
“poor” eye movements and reading has not been confirmed,14
assessment of eye movements in poor readers is routine in clin-
ical pediatric optometry practice,15
and recommended in opto-
metric clinical guidelines for the evaluation of learning-related
vision problems.16
Although the visual anomalies known to be
associated with amblyopia, such as reduced VA in both the
affected and fellow eye, reduced or absent stereopsis, and poor
fixation control may be expected to have an impact on fluency
of eye movements under habitual binocular viewing conditions,
the performance of amblyopic children on clinical tests of eye
movements has not previously been reported.
The most common assessment of eye movements in optometric
practice is direct observation of fixation ability, saccadic eye move-
*BAppSc (Optom), MSc
†
PhD, FAAO
‡
MD, FRANZCO
School of Optometry and Institute of Health and Biomedical Innovation, Queens-
land University of Technology (ALW, JMW, BB), and Department of Paediatrics and
Child Health, University of Queensland (GAG), Brisbane, Australia.
1040-5488/09/8606-0760/0 VOL. 86, NO. 6, PP. 760–766
OPTOMETRY AND VISION SCIENCE
Copyright © 2009 American Academy of Optometry
Optometry and Vision Science, Vol. 86, No. 6, June 2009
ments and pursuit eye movements, and grading of these eye move-
ments for smoothness and accuracy on a 1 to 4 scale.15
Although
the grading scales are simple to administer, the inter-rater reliabil-
ity of direct observation tests has been questioned.15
Although less
common in clinical practice, objective infrared recording of eye
movements during reading for comprehension can be provided by
the Visagraph III Eye-Movement recording system (Taylor Asso-
ciates, NY).15
Although the highly detailed description of eye move-
ments provided by the Visagraph is comprehensive, the relatively high
equipment costs, significantly longer time required for testing, and
relativelyhighdegreeoftechnicalknowledgerequiredtoobtainavalid
recording may have limited its use in clinical practice.
An alternative clinical test of saccadic eye movements is the
Developmental Eye Movement Test (DEM),17
which provides a
measure of visual-verbal oculomotor skills and rapid automatized
naming (RAN).18
The DEM is considered a standardized clinical
test of saccadic eye movements and is recommended for use in
optometric practice for the evaluation of learning-related vision
problems in children.16
Although the test–retest reliability of the
DEM has been questioned,19
in a more controlled setting test-
retest reliability has been shown to be relatively high.18
We have previously reported that amblyopia impacts on
outcomes of fine motor skills tests of visual motor control and upper-
limbspeedanddexterity,andthatpoorerfinemotorskillperformance
was associated with a history of strabismus.20
The deficits in motor
performance were greatest on timed manual dexterity tasks reflecting
both speed and accuracy. The outcomes of the DEM test are also
judged on speed and accuracy; hence, we examined whether they may
be similarly affected in a group of amblyopic children.
In addition to a history of strabismus, the visual anomalies as-
sociated with amblyopia that we hypothesize may influence DEM
test outcomes include the level of VA in the better eye, as this
predicts VA under binocular conditions,21
level of stereoacuity as a
measure of binocular fusion and inter-ocular VA difference as a
measure of depth of amblyopia. Hyperopia is also considered as it
has been linked with poor performance compared with controls on
several spatial cognitive and motor tests,22,23
and hyperopic chil-
dren have poor reading performance compared with emmetropic
and myopic children.24
In this study, performed under habitual binocular viewing con-
ditions, we used the DEM to obtain a clinical assessment of sac-
cadic eye movements in a sample of children with amblyopia of
differing aetiologies and compared outcome measures with those
of an age-matched group of control children. The influences of
etiology and measured visual characteristics on the outcome mea-
sures of the DEM were also explored.
METHODS
Participants
Thirty-nine children (age, 9.1 Ϯ 0.9 years; range, 8.0 to 11.2
years) who had been diagnosed and treated for amblyopia or am-
blyogenic conditions and 42 control children (age, 9.3 Ϯ 0.4 years;
range, 8.6 to 10.0 years) participated in this study. Potential am-
blyopic subjects were recruited from the private practice of a pedi-
atric ophthalmologist (GG) and control subjects were recruited
from a local primary (elementary) school. Details of participant
recruitment and clinical characteristics have been previously re-
ported.20,25
Amblyopia in our subjects resulted from a range of
causes: seven had a history of infantile esotropia, ten had history of
acquired strabismus, eight had history of anisometropia, eight had
history of both strabismus and anisometropia, and six had a history
of disturbance of monocular image clarity causing deprivation am-
blyopia (five from monocular cataract and one from persistent
monocular primary vitreous requiring lensectomy and vitrec-
tomy). All had received ophthalmological treatment for the under-
lying amblyogenic condition (surgery or refractive correction), and
had concluded occlusion or penalisation treatment. The group
included both children with a successful treatment outcome and
children who still had clinically significant amblyopia (Ͼ0.2 log-
MAR difference in VA between eyes). The current refractive cor-
rection based on a cycloplegic refraction (1.0% cyclopentolate)
within the previous 12 months was worn for all testing.
Vision Assessment
Visual acuity was measured in each eye using a 3-m Bailey-Lovie
logMAR chart26
while the child wore their current refractive cor-
rection. The resultant VA for each eye was scored on a letter by
letter basis. The level of binocular function was assessed with the
Randot Preschool Stereoacuity Test,27
chosen for its established
validity and normative data.28
Suppression was confirmed by the
Mirror-Pola technique29
if no stereoscopic response was obtained
on the Randot Preschool Stereoacuity Test.
Developmental Eye Movement Test
Saccadic eye movements were assessed with the Developmental
Eye Movement test,17
in which the time taken for a series of num-
bers (single digits) to be seen, recognized, and spoken with accu-
racy was measured. The test consisted of two subtests with 40
numbers arranged in vertical columns (Tests A and B), and a
subtest with 80 irregularly spaced numbers arranged in 16 hori-
zontal rows (Test C). Participants were asked to name aloud the
single digit numbers as quickly and accurately as possible and the
times taken to read aloud the 80 numbers in both the four vertical
columns (vertical time) and the 16 line horizontal array (horizontal
time) were recorded. The number of omission and addition errors
was recorded and test times were adjusted for errors made. Upon
completion of the test, a ratio was calculated by dividing the time
taken to read the 80 numbers in the horizontal array by the total
time for reading the 80 numbers in vertical subsets. The outcomes
from the DEM test were vertical time, horizontal time, number of
errors and ratio(horizontal time/vertical time). Results were converted to
standard scores and percentile ranks based on published age-
normative data for this test.30
Amblyopic and control subjects also completed a self-esteem
questionnaire and tests of fine motor skills performance during the
experimental session; the findings of these tests have been pub-
lished elsewhere.20,25
Complete assessment of vision, fine motor
skills, perceived self-esteem, and DEM took about 45 min per
subject and were completed within one test session by all subjects.
All participants were given a full explanation of the experimental
procedures and the option to withdraw from the study at any time
was explained to the parent and child. Written informed consent
was obtained from the parent prior to participation in the study.
Developmental Eye Movement Test in Children with Amblyopia—Webber et al. 761
Optometry and Vision Science, Vol. 86, No. 6, June 2009
The study was conducted in accordance with the requirements of
the Queensland University of Technology Human Research Eth-
ics Committee and all protocols concurred with the guidelines of
the Declaration of Helsinki.
Statistical Analysis
All data were tested for normality using the Kolmogorov-Smirnov
test. Where the data were normally distributed, the results from the
amblyopes were compared with those of the control group using in-
dependent samples t-test and results between amblyopic subgroups
were compared with a one-way ANOVA (Statistical Package for the
Social Sciences–SPSS V14), using a significance level of 0.05. When
statistically significant differences were found between means, Bonfer-
roniposthoctestswereused.Non-parametrictestswereusedwherethe
data were not normally distributed. Pearson’s correlation coefficients
were calculated to explore the relationships between DEM measures
and subject vision characteristics.
RESULTS
No significant differences in age or gender were found between
the amblyopic and control groups. On average, the subjects with
amblyopia had a VA of 0.06 logMAR in the better eye (range,
Ϫ0.18 to 0.30 logMAR) and 0.44 logMAR in the worse eye
(range, 0.00 to 2.00 logMAR). Ten amblyopic subjects had cor-
rected VA of logMAR 0.20 or better in their worse eye, and 19
amblyopic subjects had a difference in acuity between eyes that was
less than or equal to 0.20 logMAR. In the control group, there was
little difference between eyes (Ϫ0.03 logMAR in the better eye;
Ϫ0.01 logMAR in the worse eye). All control subjects had VA
better than 0.20 logMAR in their worse eye and all had Ͻ0.20
logMAR difference in VA between eyes.
A hyperopic refractive correction was worn by 29 of the ambly-
opic subjects (73%) [range, ϩ0.50 diopter (D) to ϩ9.50 D] and
three control subjects (7%) (range, ϩ1.00 D to ϩ3.00 D). Refrac-
tive correction was spherical in the three control subjects and in 19
of the amblyopic group. Astigmatic correction varied between 1.00
D and 2.25 D in 10 of the amblyopic subjects. In the amblyopic
group, 16 subjects had refractive corrections that were different
between eyes by more than 1.00 D. The spherical equivalent of
refractive correction, averaged between right and left eyes, is re-
ported in Table 1.
When compared with age-matched control children, the am-
blyopic children had a greater inter-ocular difference in VA,
poorer VA in both their better and worse eyes, and were less
likely to have normal stereopsis (40 sec arc) (p Ͻ 0.05). Table 1
summarizes the mean and standard errors for the age, gender,
refractive and vision characteristics of the amblyopic and con-
trol groups and presents the results of the statistical analysis for
differences between groups.
Subjects were grouped according to their stereopsis level; “nil” if
no stereoscopic response could be measured, “reduced” if the re-
sponse indicated stereopsis between 800 and 60 sec arc, and “nor-
mal” if the response indicated stereopsis better than or equal to
40 sec arc. The level of stereopsis varied significantly both between
the amblyopic and control groups (␹2
(dF ϭ 2) ϭ 66.08; p Ͻ 0.001)
and between subgroups (␹2
(dF ϭ 8) ϭ 18.87; p Ͻ 0.001) (Table 1).
The majority of the control subjects (98%) had normal stereopsis
(Յ40Љ)31
compared with only 8% of the amblyopic group. No
subject with infantile esotropia had measurable stereopsis, 75% of
TABLE 1.
Age, gender, refractive and vision characteristics of samples
Control
(N ϭ 42)
Total amblyopia
group
(N ϭ 39)
Statistical significance
between amblyopia and
control group
Amblyopic subgroups
Statistical significance
one-way ANOVA
between amblyopic
aetiology groups
t(dF ϭ 79)
␹2
(dF ϭ 2)
p
Infantile
esotropia
(N ϭ 7)
Acquired
strabismus
(N ϭ 10)
Anisometropia
(N ϭ 8)
Mixed
(N ϭ 8)
Deprivation
(N ϭ 6) F or ␹2 p
Age (years) 9.34 (0.38) 9.12 (0.96) Ϫ1.214c 0.228 9.51 (1.26) 8.90 (0.83) 9.64 (0.79) 8.56 (0.82) 9.26 (0.86) 1.888a 0.135
Gender (% female) 20 (48%) 17 (43%) 0.664d 0.404 29% 50% 38% 38% 50% ␹2
(dF ϭ 4)
1.564
0.815
Stereopsis
Nil 0 (0%) 23 (59%) 66.08d Ͻ0.001 7 (100%) 7 (70%) 0 (0%) 5 (63%) 4 (67%) ␹2
(dF ϭ 8)
18.87
0.016
800Љ–60Љ 1 (2%) 13 (33%) 0 (0%) 2 (20%) 6 (75%) 3 (38%) 2 (29%)
Յ40Љ 41 (98%) 3 (8%) 0 (0 %) 1 (10%) 2 (25%) 0 (0%) 0 (0%)
Inter ocular
difference in VA
(logMAR)
0.02 (0.03) 0.38 (0.52) 4.475c Ͻ0.001 0.51 (0.72) 0.11 (0.10)b 0.22 (0.18)b 0.21 (0.16)b 1.09 (0.69)b 6.254a 0.001
VA in better eye
(logMAR)
Ϫ0.03 (0.05) 0.06 (0.11) 4.726c Ͻ0.001 0.06 (0.12) 0.09 (0.10) 0.05 (0.10) 0.08 (0.13) 0.00 (0.10) 0.748a 0.566
VA in worse eye
(logMAR)
Ϫ0.01 (0.05) 0.44 (0.50) 5.710c Ͻ0.001 0.57 (0.68) 0.21 (0.13)b 0.27 (0.12)b 0.28 (0.21)b 1.09 (0.73)b 5.180a 0.002
Refractive error
(diopters)
0.16 (0.63) 2.92 (2.49) 6.941c Ͻ0.001 1.17 (1.21) 4.23 (3.20)b 2.75 (1.66) 4.59 (1.56)b 0.79 (1.50)b 5.044a 0.003
Mean (standard deviation) of data presented. Italics indicate significant differences between groups.
a
One-way ANOVA F(4,39).
b
Post hoc tests indicate significant differences between subgroups.
c
(dF ϭ 79).
d
␹2
(dF ϭ 2).
762 Developmental Eye Movement Test in Children with Amblyopia—Webber et al.
Optometry and Vision Science, Vol. 86, No. 6, June 2009
anisometropic amblyopes had reduced levels of stereopsis, and
25% of the anisometropes had normal stereopsis.
In addition to significant differences between the amblyopia and
control groups, significant differences were measured between am-
blyopic etiology subgroups in VA in the worse eye, intra-ocular VA
difference, level of stereoacuity, and average refractive error (Table
1). Post hoc testing indicated that those with an etiology of depri-
vation had significantly poorer VA in the worse eye and a greater
inter-ocular VA difference than the other subgroups, and the dif-
ference in refractive error was significant between the deprivation
and mixed etiology subgroups.
Mean and standard deviation of DEM outcome measures vertical
time, horizontal time, number of errors and ratio(horizontal time/vertical time)
are shown for the amblyopic and control groups in Table 2. No
significant differences in any of the outcome measures of the DEM
were found between the amblyopic and age-matched control
group, and the data for each group were comparable with pub-
lished DEM normative data for children aged between 9 and 10
years of age (n ϭ 84).30
Outcome measures of the DEM did not
differ significantly between amblyopic subgroups (Table 2); how-
ever, the small sample sizes in the etiological subgroups limit the
statistical power of this analysis.
An indication of the clinical significance of the DEM outcomes
was derived by referring to published normative data.30
As well as
presenting mean and standard deviation values for normative
groups, the DEM handbook provides a calculation of a standard
score and an indication of percentile rank of performance against
the normative data. Where a subject scored in the 15th percentile
or below, their results are considered abnormal and outside the
normal range by standardized and validated testing of the DEM.32
The number of subjects in either the amblyopia or the control
group whose result was outside the range of published normative
data30
is shown in Table 3. No significant difference was seen
between amblyopic and control groups in the number of subjects
who met this clinical criterion for an abnormal result.
Visual Determinants of DEM Outcome Measures
Pearson correlation coefficients were calculated for the total
sample (n ϭ 81) between the DEM outcome measures and the
visual characteristics of the subjects that we considered might in-
fluence oculo-motor control (history of strabismus, VA in better
eye, VA in worse eye, inter-ocular VA difference, average refractive
error, and level of stereopsis). As expected, there were a number of
significant intercorrelations between the visual characteristics of
the participants (p Ͻ 0.05) and also between the different DEM
outcome measures (p Ͻ 0.05). However, there were no significant
correlations between the DEM outcome measures and participant
visual characteristics.
Impact of Treatment Success
The amblyopic children were grouped for this analysis accord-
ing to whether their treatment was considered to have been suc-
cessful. Nineteen children (49%) had Յ0.20 logMAR
difference in acuity between eyes and had 0.20 logMAR or better
VA in their worse eye and were allocated to the successful outcome
group. No significant differences in DEM outcomes were found
between those children who would be clinically described as having
successful vs. unsuccessful treatment outcomes (Table 4).
The influence of binocular function was explored by testing for
differences in DEM outcomes between stereopsis groups. Al-
TABLE 2.
DEM outcomes
Outcome measure
Control
(N ϭ 42)
Total
amblyopia
group
(N ϭ 39)
Normative
data30 (age
9.0–9.99)
(N ϭ 84)
Statistical
significance
between amblyopia
and control group
Amblyopic subgroups
Statistical
significance
between
amblyopic
aetiology groups
T(dF ϭ 79) p
Infantile
esotropia
(N ϭ 7)
Acquired
strabismus
(N ϭ 10)
Anisometropia
(N ϭ 8)
Mixed
(N ϭ 8)
Deprivation
(N ϭ 6) F(4,39) p
Vertical adjusted time (s) 41.12 (6.79) 42.13 (9.05) 42.33 (8.20) 0.570 0.570 39.29 (6.85) 42.90 (9.22) 37.38 (3.96) 42.50 (5.68) 50.00 (14.93) 2.098 0.103
Horizontal adjusted time (s) 52.71 (11.54) 53.18 (16.96) 51.13 (13.30) 0.145 0.885 47.29 (8.75) 52.80 (13.68) 46.63 (6.61)a 56.38 (19.77) 65.17 (29.03)a 1.386 0.260
Number of errors 0.98 (2.42) 1.62 (3.60) 2.17 (4.10) 0.944 0.348 2.71 (5.62) 0.60 (1.35) 0.38 (0.52) 1.50 (3.51) 3.83 (5.23) 1.198 0.329
Ratio (horz time/vert time) 1.27 (0.19) 1.25 (0.20) 1.21 (0.19) Ϫ0.551 0.583 1.21 (0.17) 1.23 (021) 1.25 (0.15) 1.31 (0.28) 1.26 (0.17) 0.264 0.899
Mean (standard deviation) of data presented.
a
Post hoc tests indicate significant differences between subgroups.
TABLE 3.
Number of subjects with DEM scores below 15th percentile
Total N
(% of subjects)
Amblyopic
group
Control
group
␹2
(dF ϭ 1) p
Horizontal time Ն53 s 6 (7%) 4 (10%) 2 (5%) 0.890 0.345
Vertical time Ն64 s 12 (15%) 6 (15%) 6 (14%) 0.032 0.858
Number of errors Ն4 11 (14%) 6 (15%) 5 (12%) 0.209 0.648
Ratio Ն1.40 15 (19%) 7 (18%) 8 (19%) 0.016 0.899
Developmental Eye Movement Test in Children with Amblyopia—Webber et al. 763
Optometry and Vision Science, Vol. 86, No. 6, June 2009
though those with no measurable stereopsis recorded the highest
mean number of errors, these differences did not reach significance
as shown in Table 5.
DISCUSSION
This is the first study to report the performance of a group of
amblyopic children on a clinical measure of saccadic eye move-
ments and to compare that performance to an age-matched control
group with normal vision. Our findings indicate that, despite
significantly reduced VA in both the affected and fellow eyes,
reduced or absent stereopsis, and significantly greater hyperopic
refractive errors, the scores of the amblyopic children were sim-
ilar to those of control children for the outcome measures of the
DEM test: vertical time, horizontal time, number of errors and
ratio(horizontal time/vertical time).
In addition to determining that the ability of amblyopic chil-
dren to quickly execute saccades to fixate, identify, and name single
digits was not significantly different from that of their age-matched
peers, we found that the outcome measures of the DEM did not
significantly relate to measures of VA in either eye, levels of binoc-
ular function, or magnitude of refractive correction.
The prevalence of clinically unacceptable performance on the
DEM was equivalent in the amblyopic and control groups and
agreed with published normative data for the DEM test, suggesting
that under habitual binocular viewing conditions amblyopia does
not result in a functionally relevant reduction in saccadic eye move-
ment speed and accuracy.
The DEM provides an indirect, quantitative evaluation of sac-
cadic eye movements based on the speed with which a series of
numbers can be seen, recognized, and verbalized with accuracy.18
It is thus purported to detect oculomotor dysfunction and is
recommended in optometric clinical practice guidelines for the
quantitative evaluation of saccadic eye movements in children for
learning-related vision problems.33
The horizontal subtest mimics
the eye movements made during reading, with saccades of variable
length required to fixate on the irregularly spaced single digits
(N10 font size) along horizontal rows, whereas the vertical subtests
give a base measure of how quickly the child can name 80 numbers
without having to make the saccadic eye movements along rows.
The time to complete the task and the number of errors are the
clinical outcomes, with significantly slower and/or error prone
performance on the horizontal task than the vertical task, that is a
higher Ratio score, indicating poor saccadic eye movement con-
trol.17
Poor performance on both the vertical and horizontal
subtests would indicate slow automatic naming ability.17
A clinical purpose of the DEM is to help practitioners determine
whether poor saccadic tracking may contribute to poor reading
behavior.17
Indeed, a sustained and prevalent controversy in read-
ing eye movement research is whether fluent reading is controlled
by low-level eye movement efficiency, as would be measured by the
DEM, or whether it is influenced by the more moment-to-
moment cognitive processes.14
The DEM has been found to pre-
dict students with below-average reading performance,34
and to
relate to parental observation of errors during reading, such as
losing place or omitting words when reading or copying and re-
reading lines unknowingly.18
However, despite recognition of
reading as an important vision dependent ability that contributes
to an individual’s quality of life,35
few studies have evaluated the
reading performance of amblyopes under habitual binocular view-
ing conditions. Specific reading disability was found to be rela-
tively rare in a small sample of children with amblyopia (n ϭ 20),36
and not more prevalent than reported in the general population.
Conversely, Stifter et al.37
recently reported functionally relevant
reading impairment (reduced maximum reading speed under binoc-
ular viewing conditions) in micro-strabismic children (n ϭ 20; age,
11.5 Ϯ 1.1 years). Our finding that amblyopia had no effect on eye
movements when assessed with the DEM indicates that the deficit
in binocular reading speed reported in amblyopic children37
is not
TABLE 5.
Difference in DEM results between binocular function groups
DEM outcome measure
Nil stereopsis
N ϭ 23
Reduced
stereopsis
N ϭ 14
Normal
stereopsis
N ϭ 44
F(2,78) p
Vertical time (s) 43.52 (10.60) 40.29 (6.56) 41.02 (6.59) 0.985 0.378
Horizontal time (s) 55.78 (20.73) 49.29 (9.46) 52.61 (11.21) 0.919 0.403
Number of errors 2.43 (4.04) 0.50 (0.76) 0.93 (2.38) 2.495 0.089
Ratio(horizontal time/vertical time) 1.26 (0.24) 1.22 (0.13) 1.27 (0.16) 0.416 0.661
TABLE 4.
Difference in DEM results between amblyopic VA groups
DEM outcome measure
VA in worse eye Յ0.20
logMAR N ϭ 19
VA in worse eye Ͼ0.20
logMAR N ϭ20
T(dF ϭ 37) p
Vertical time (s) 41.26 (6.69) 42.95 (10.95) Ϫ0.5777 0.568
Horizontal time (s) 53.37 (14.26) 53.00 (19.63) 0.067 0.947
Number of errors 1.89 (4.04) 1.35 (3.20) 0.468 0.642
Ratio(horizontal time/vertical time) 1.29 (0.23) 1.21 (0.15) 1.314 0.197
764 Developmental Eye Movement Test in Children with Amblyopia—Webber et al.
Optometry and Vision Science, Vol. 86, No. 6, June 2009
explained by poor saccadic eye movement efficiency. Stifter et al.37
also reported that better binocular reading speed in the amblyopic
group was associated with more central and steady fixation and
better sensory binocular function, but did not relate to age, VA,
accommodative impairment, strabismic angle, or refractive error.
In this study, timed outcome measures on the DEM were not
associated with history of strabismus, VA in either eye, level of
binocular function, or magnitude of refractive error.
It has been reported that the reading speed of well-corrected
fluent observers reading ordinary text under adequate lighting con-
ditions is limited by letter spacing (crowding) and is independent
of text size, contrast, and luminance, provided that text contrast is
at least four times the threshold contrast for an isolated letter.38
Levi et al.39
recently demonstrated that crowding rather than acu-
ity limits reading in amblyopic observers, as well as in normal
observers, in both central and peripheral vision. Crowding should
not influence performance on the DEM because the test targets
consist of 3 mm tall, high-contrast single digits (approximately
N10) with 5 mm between rows of numbers and spacing of 10 to 25
mm between numbers. The extent to which crowding may explain
the reduction in reading speed measured under binocular condi-
tions as reported by Stifter et al.37
remains unclear.
Amblyopia is the most common cause of reduced vision in chil-
dren and young people, with significant costs to both the individual
and community for screening and treatment. Although a number of
functionally relevant deficits in tasks that contribute to quality of
life have now been reported,40
the educational, health, and social
life outcomes of amblyopes do not appear to be affected.11
In
addition to determining the extent of functionally relevant deficits
in performance that may accompany amblyopia, it is important to
have an understanding of how children with amblyopia perform
on clinical tests commonly used in pediatric practice. Our present
findings demonstrate that under habitual binocular viewing con-
ditions, amblyopia does not impact on clinical measures of sac-
cadic eye movement efficiency. Although our finding suggests that
reports of reduced reading speed in amblyopia are not due to poor
eye movement control, further studies employing more direct and
objective measures of eye movements during reading are required
to further explore this relationship.
Understanding the influence of amblyopia on performance is
important for clinicians when interpreting test results and for pro-
viding advice to parents of the consequences of amblyopia. Clinical
treatment plans for amblyopia aim to improve VA and binocular
function outcomes. However, the relationship between degraded
vision and performance both on clinical tests of visual efficiency
and on visually directed tasks relevant to children is yet to be fully
established and warrants further study.
Received July 8, 2008; accepted August 20, 2008.
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Ann L. Webber
School of Optometry
Queensland University of Technology
Herston Road
Kelvin Grove, 4058 Queensland
Australia
e-mail: al.webber@qut.edu.au
766 Developmental Eye Movement Test in Children with Amblyopia—Webber et al.
Optometry and Vision Science, Vol. 86, No. 6, June 2009

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Effect of amblyopia_on_the_developmental_eye.37

  • 1. ORIGINAL ARTICLE Effect of Amblyopia on the Developmental Eye Movement Test in Children Ann L. Webber*, Joanne M. Wood† , Glen A. Gole‡ , and Brian Brown† ABSTRACT Purpose. To investigate the functional impact of amblyopia in children, the performance of amblyopic and age-matched control children on a clinical test of eye movements was compared. The influence of visual factors on test outcome measures was explored. Methods. Eye movements were assessed with the Developmental Eye Movement (DEM) test, in a group of children with amblyopia (n ϭ 39; age, 9.1 Ϯ 0.9 years) of different causes (infantile esotropia, n ϭ 7; acquired strabismus, n ϭ 10; anisometropia, n ϭ 8; mixed, n ϭ 8; deprivation, n ϭ 6) and in an age-matched control group (n ϭ 42; age, 9.3 Ϯ 0.4 years). LogMAR visual acuity (VA), stereoacuity, and refractive error were also recorded in both groups. Results. No significant difference was found between the amblyopic and age-matched control group for any of the outcome measures of the DEM (vertical time, horizontal time, number of errors and ratio(horizontal time/vertical time)). The DEM measures were not significantly related to VA in either eye, level of binocular function (stereoacuity), history of strabismus, or refractive error. Conclusions. The performance of amblyopic children on the DEM, a commonly used clinical measure of eye movements, has not previously been reported. Under habitual binocular viewing conditions, amblyopia has no effect on DEM outcome scores despite significant impairment of binocular vision and decreased VA in both the better and worse eye. (Optom Vis Sci 2009;86:760–766) Key Words: amblyopia, eye movements, DEM, binocular vision, strabismus A pproximately 3% of the population develop amblyopia,1,2 which is generally defined as poor vision resulting from ab- normal visual experience during early childhood. Children with amblyopia may have poorer visual acuity (VA) in both affected and fellow eye, little or no stereopsis or binocular fusion, and poorer efficiency in their accommodation and oculo-motor control.3 Al- though much has been reported regarding the visual characteristics of amblyopia and the neurological adaptations that underlie these ef- fects,3–5 there is little published evidence of the disability associated withamblyopia.6 Inparticular,therehasbeenonlylimitedresearchon the impact of amblyopia on the ability to complete activities of daily living that impact on career opportunities or career choices for am- blyopes,6 or on tasks pertinent to the activities of amblyopic children and their educational achievement.7 Persons with a history of ambly- opia are reported to feel that it has affected their school and career choices;8–10 however, a recent birth cohort study, involving 8861 participants, reported that amblyopia did not significantly impact on educational, health, or social outcomes.11 In addition to having reduced VA, contrast sensitivity and hyper- acuity,3 amblyopes have poorer control of fixation in both the ambly- opic and non-amblyopic eye,12 and binocular coordination of saccades is impaired in strabismic amblyopes, particularly those with large angle strabismus.13 Although a causal relationship between “poor” eye movements and reading has not been confirmed,14 assessment of eye movements in poor readers is routine in clin- ical pediatric optometry practice,15 and recommended in opto- metric clinical guidelines for the evaluation of learning-related vision problems.16 Although the visual anomalies known to be associated with amblyopia, such as reduced VA in both the affected and fellow eye, reduced or absent stereopsis, and poor fixation control may be expected to have an impact on fluency of eye movements under habitual binocular viewing conditions, the performance of amblyopic children on clinical tests of eye movements has not previously been reported. The most common assessment of eye movements in optometric practice is direct observation of fixation ability, saccadic eye move- *BAppSc (Optom), MSc † PhD, FAAO ‡ MD, FRANZCO School of Optometry and Institute of Health and Biomedical Innovation, Queens- land University of Technology (ALW, JMW, BB), and Department of Paediatrics and Child Health, University of Queensland (GAG), Brisbane, Australia. 1040-5488/09/8606-0760/0 VOL. 86, NO. 6, PP. 760–766 OPTOMETRY AND VISION SCIENCE Copyright © 2009 American Academy of Optometry Optometry and Vision Science, Vol. 86, No. 6, June 2009
  • 2. ments and pursuit eye movements, and grading of these eye move- ments for smoothness and accuracy on a 1 to 4 scale.15 Although the grading scales are simple to administer, the inter-rater reliabil- ity of direct observation tests has been questioned.15 Although less common in clinical practice, objective infrared recording of eye movements during reading for comprehension can be provided by the Visagraph III Eye-Movement recording system (Taylor Asso- ciates, NY).15 Although the highly detailed description of eye move- ments provided by the Visagraph is comprehensive, the relatively high equipment costs, significantly longer time required for testing, and relativelyhighdegreeoftechnicalknowledgerequiredtoobtainavalid recording may have limited its use in clinical practice. An alternative clinical test of saccadic eye movements is the Developmental Eye Movement Test (DEM),17 which provides a measure of visual-verbal oculomotor skills and rapid automatized naming (RAN).18 The DEM is considered a standardized clinical test of saccadic eye movements and is recommended for use in optometric practice for the evaluation of learning-related vision problems in children.16 Although the test–retest reliability of the DEM has been questioned,19 in a more controlled setting test- retest reliability has been shown to be relatively high.18 We have previously reported that amblyopia impacts on outcomes of fine motor skills tests of visual motor control and upper- limbspeedanddexterity,andthatpoorerfinemotorskillperformance was associated with a history of strabismus.20 The deficits in motor performance were greatest on timed manual dexterity tasks reflecting both speed and accuracy. The outcomes of the DEM test are also judged on speed and accuracy; hence, we examined whether they may be similarly affected in a group of amblyopic children. In addition to a history of strabismus, the visual anomalies as- sociated with amblyopia that we hypothesize may influence DEM test outcomes include the level of VA in the better eye, as this predicts VA under binocular conditions,21 level of stereoacuity as a measure of binocular fusion and inter-ocular VA difference as a measure of depth of amblyopia. Hyperopia is also considered as it has been linked with poor performance compared with controls on several spatial cognitive and motor tests,22,23 and hyperopic chil- dren have poor reading performance compared with emmetropic and myopic children.24 In this study, performed under habitual binocular viewing con- ditions, we used the DEM to obtain a clinical assessment of sac- cadic eye movements in a sample of children with amblyopia of differing aetiologies and compared outcome measures with those of an age-matched group of control children. The influences of etiology and measured visual characteristics on the outcome mea- sures of the DEM were also explored. METHODS Participants Thirty-nine children (age, 9.1 Ϯ 0.9 years; range, 8.0 to 11.2 years) who had been diagnosed and treated for amblyopia or am- blyogenic conditions and 42 control children (age, 9.3 Ϯ 0.4 years; range, 8.6 to 10.0 years) participated in this study. Potential am- blyopic subjects were recruited from the private practice of a pedi- atric ophthalmologist (GG) and control subjects were recruited from a local primary (elementary) school. Details of participant recruitment and clinical characteristics have been previously re- ported.20,25 Amblyopia in our subjects resulted from a range of causes: seven had a history of infantile esotropia, ten had history of acquired strabismus, eight had history of anisometropia, eight had history of both strabismus and anisometropia, and six had a history of disturbance of monocular image clarity causing deprivation am- blyopia (five from monocular cataract and one from persistent monocular primary vitreous requiring lensectomy and vitrec- tomy). All had received ophthalmological treatment for the under- lying amblyogenic condition (surgery or refractive correction), and had concluded occlusion or penalisation treatment. The group included both children with a successful treatment outcome and children who still had clinically significant amblyopia (Ͼ0.2 log- MAR difference in VA between eyes). The current refractive cor- rection based on a cycloplegic refraction (1.0% cyclopentolate) within the previous 12 months was worn for all testing. Vision Assessment Visual acuity was measured in each eye using a 3-m Bailey-Lovie logMAR chart26 while the child wore their current refractive cor- rection. The resultant VA for each eye was scored on a letter by letter basis. The level of binocular function was assessed with the Randot Preschool Stereoacuity Test,27 chosen for its established validity and normative data.28 Suppression was confirmed by the Mirror-Pola technique29 if no stereoscopic response was obtained on the Randot Preschool Stereoacuity Test. Developmental Eye Movement Test Saccadic eye movements were assessed with the Developmental Eye Movement test,17 in which the time taken for a series of num- bers (single digits) to be seen, recognized, and spoken with accu- racy was measured. The test consisted of two subtests with 40 numbers arranged in vertical columns (Tests A and B), and a subtest with 80 irregularly spaced numbers arranged in 16 hori- zontal rows (Test C). Participants were asked to name aloud the single digit numbers as quickly and accurately as possible and the times taken to read aloud the 80 numbers in both the four vertical columns (vertical time) and the 16 line horizontal array (horizontal time) were recorded. The number of omission and addition errors was recorded and test times were adjusted for errors made. Upon completion of the test, a ratio was calculated by dividing the time taken to read the 80 numbers in the horizontal array by the total time for reading the 80 numbers in vertical subsets. The outcomes from the DEM test were vertical time, horizontal time, number of errors and ratio(horizontal time/vertical time). Results were converted to standard scores and percentile ranks based on published age- normative data for this test.30 Amblyopic and control subjects also completed a self-esteem questionnaire and tests of fine motor skills performance during the experimental session; the findings of these tests have been pub- lished elsewhere.20,25 Complete assessment of vision, fine motor skills, perceived self-esteem, and DEM took about 45 min per subject and were completed within one test session by all subjects. All participants were given a full explanation of the experimental procedures and the option to withdraw from the study at any time was explained to the parent and child. Written informed consent was obtained from the parent prior to participation in the study. Developmental Eye Movement Test in Children with Amblyopia—Webber et al. 761 Optometry and Vision Science, Vol. 86, No. 6, June 2009
  • 3. The study was conducted in accordance with the requirements of the Queensland University of Technology Human Research Eth- ics Committee and all protocols concurred with the guidelines of the Declaration of Helsinki. Statistical Analysis All data were tested for normality using the Kolmogorov-Smirnov test. Where the data were normally distributed, the results from the amblyopes were compared with those of the control group using in- dependent samples t-test and results between amblyopic subgroups were compared with a one-way ANOVA (Statistical Package for the Social Sciences–SPSS V14), using a significance level of 0.05. When statistically significant differences were found between means, Bonfer- roniposthoctestswereused.Non-parametrictestswereusedwherethe data were not normally distributed. Pearson’s correlation coefficients were calculated to explore the relationships between DEM measures and subject vision characteristics. RESULTS No significant differences in age or gender were found between the amblyopic and control groups. On average, the subjects with amblyopia had a VA of 0.06 logMAR in the better eye (range, Ϫ0.18 to 0.30 logMAR) and 0.44 logMAR in the worse eye (range, 0.00 to 2.00 logMAR). Ten amblyopic subjects had cor- rected VA of logMAR 0.20 or better in their worse eye, and 19 amblyopic subjects had a difference in acuity between eyes that was less than or equal to 0.20 logMAR. In the control group, there was little difference between eyes (Ϫ0.03 logMAR in the better eye; Ϫ0.01 logMAR in the worse eye). All control subjects had VA better than 0.20 logMAR in their worse eye and all had Ͻ0.20 logMAR difference in VA between eyes. A hyperopic refractive correction was worn by 29 of the ambly- opic subjects (73%) [range, ϩ0.50 diopter (D) to ϩ9.50 D] and three control subjects (7%) (range, ϩ1.00 D to ϩ3.00 D). Refrac- tive correction was spherical in the three control subjects and in 19 of the amblyopic group. Astigmatic correction varied between 1.00 D and 2.25 D in 10 of the amblyopic subjects. In the amblyopic group, 16 subjects had refractive corrections that were different between eyes by more than 1.00 D. The spherical equivalent of refractive correction, averaged between right and left eyes, is re- ported in Table 1. When compared with age-matched control children, the am- blyopic children had a greater inter-ocular difference in VA, poorer VA in both their better and worse eyes, and were less likely to have normal stereopsis (40 sec arc) (p Ͻ 0.05). Table 1 summarizes the mean and standard errors for the age, gender, refractive and vision characteristics of the amblyopic and con- trol groups and presents the results of the statistical analysis for differences between groups. Subjects were grouped according to their stereopsis level; “nil” if no stereoscopic response could be measured, “reduced” if the re- sponse indicated stereopsis between 800 and 60 sec arc, and “nor- mal” if the response indicated stereopsis better than or equal to 40 sec arc. The level of stereopsis varied significantly both between the amblyopic and control groups (␹2 (dF ϭ 2) ϭ 66.08; p Ͻ 0.001) and between subgroups (␹2 (dF ϭ 8) ϭ 18.87; p Ͻ 0.001) (Table 1). The majority of the control subjects (98%) had normal stereopsis (Յ40Љ)31 compared with only 8% of the amblyopic group. No subject with infantile esotropia had measurable stereopsis, 75% of TABLE 1. Age, gender, refractive and vision characteristics of samples Control (N ϭ 42) Total amblyopia group (N ϭ 39) Statistical significance between amblyopia and control group Amblyopic subgroups Statistical significance one-way ANOVA between amblyopic aetiology groups t(dF ϭ 79) ␹2 (dF ϭ 2) p Infantile esotropia (N ϭ 7) Acquired strabismus (N ϭ 10) Anisometropia (N ϭ 8) Mixed (N ϭ 8) Deprivation (N ϭ 6) F or ␹2 p Age (years) 9.34 (0.38) 9.12 (0.96) Ϫ1.214c 0.228 9.51 (1.26) 8.90 (0.83) 9.64 (0.79) 8.56 (0.82) 9.26 (0.86) 1.888a 0.135 Gender (% female) 20 (48%) 17 (43%) 0.664d 0.404 29% 50% 38% 38% 50% ␹2 (dF ϭ 4) 1.564 0.815 Stereopsis Nil 0 (0%) 23 (59%) 66.08d Ͻ0.001 7 (100%) 7 (70%) 0 (0%) 5 (63%) 4 (67%) ␹2 (dF ϭ 8) 18.87 0.016 800Љ–60Љ 1 (2%) 13 (33%) 0 (0%) 2 (20%) 6 (75%) 3 (38%) 2 (29%) Յ40Љ 41 (98%) 3 (8%) 0 (0 %) 1 (10%) 2 (25%) 0 (0%) 0 (0%) Inter ocular difference in VA (logMAR) 0.02 (0.03) 0.38 (0.52) 4.475c Ͻ0.001 0.51 (0.72) 0.11 (0.10)b 0.22 (0.18)b 0.21 (0.16)b 1.09 (0.69)b 6.254a 0.001 VA in better eye (logMAR) Ϫ0.03 (0.05) 0.06 (0.11) 4.726c Ͻ0.001 0.06 (0.12) 0.09 (0.10) 0.05 (0.10) 0.08 (0.13) 0.00 (0.10) 0.748a 0.566 VA in worse eye (logMAR) Ϫ0.01 (0.05) 0.44 (0.50) 5.710c Ͻ0.001 0.57 (0.68) 0.21 (0.13)b 0.27 (0.12)b 0.28 (0.21)b 1.09 (0.73)b 5.180a 0.002 Refractive error (diopters) 0.16 (0.63) 2.92 (2.49) 6.941c Ͻ0.001 1.17 (1.21) 4.23 (3.20)b 2.75 (1.66) 4.59 (1.56)b 0.79 (1.50)b 5.044a 0.003 Mean (standard deviation) of data presented. Italics indicate significant differences between groups. a One-way ANOVA F(4,39). b Post hoc tests indicate significant differences between subgroups. c (dF ϭ 79). d ␹2 (dF ϭ 2). 762 Developmental Eye Movement Test in Children with Amblyopia—Webber et al. Optometry and Vision Science, Vol. 86, No. 6, June 2009
  • 4. anisometropic amblyopes had reduced levels of stereopsis, and 25% of the anisometropes had normal stereopsis. In addition to significant differences between the amblyopia and control groups, significant differences were measured between am- blyopic etiology subgroups in VA in the worse eye, intra-ocular VA difference, level of stereoacuity, and average refractive error (Table 1). Post hoc testing indicated that those with an etiology of depri- vation had significantly poorer VA in the worse eye and a greater inter-ocular VA difference than the other subgroups, and the dif- ference in refractive error was significant between the deprivation and mixed etiology subgroups. Mean and standard deviation of DEM outcome measures vertical time, horizontal time, number of errors and ratio(horizontal time/vertical time) are shown for the amblyopic and control groups in Table 2. No significant differences in any of the outcome measures of the DEM were found between the amblyopic and age-matched control group, and the data for each group were comparable with pub- lished DEM normative data for children aged between 9 and 10 years of age (n ϭ 84).30 Outcome measures of the DEM did not differ significantly between amblyopic subgroups (Table 2); how- ever, the small sample sizes in the etiological subgroups limit the statistical power of this analysis. An indication of the clinical significance of the DEM outcomes was derived by referring to published normative data.30 As well as presenting mean and standard deviation values for normative groups, the DEM handbook provides a calculation of a standard score and an indication of percentile rank of performance against the normative data. Where a subject scored in the 15th percentile or below, their results are considered abnormal and outside the normal range by standardized and validated testing of the DEM.32 The number of subjects in either the amblyopia or the control group whose result was outside the range of published normative data30 is shown in Table 3. No significant difference was seen between amblyopic and control groups in the number of subjects who met this clinical criterion for an abnormal result. Visual Determinants of DEM Outcome Measures Pearson correlation coefficients were calculated for the total sample (n ϭ 81) between the DEM outcome measures and the visual characteristics of the subjects that we considered might in- fluence oculo-motor control (history of strabismus, VA in better eye, VA in worse eye, inter-ocular VA difference, average refractive error, and level of stereopsis). As expected, there were a number of significant intercorrelations between the visual characteristics of the participants (p Ͻ 0.05) and also between the different DEM outcome measures (p Ͻ 0.05). However, there were no significant correlations between the DEM outcome measures and participant visual characteristics. Impact of Treatment Success The amblyopic children were grouped for this analysis accord- ing to whether their treatment was considered to have been suc- cessful. Nineteen children (49%) had Յ0.20 logMAR difference in acuity between eyes and had 0.20 logMAR or better VA in their worse eye and were allocated to the successful outcome group. No significant differences in DEM outcomes were found between those children who would be clinically described as having successful vs. unsuccessful treatment outcomes (Table 4). The influence of binocular function was explored by testing for differences in DEM outcomes between stereopsis groups. Al- TABLE 2. DEM outcomes Outcome measure Control (N ϭ 42) Total amblyopia group (N ϭ 39) Normative data30 (age 9.0–9.99) (N ϭ 84) Statistical significance between amblyopia and control group Amblyopic subgroups Statistical significance between amblyopic aetiology groups T(dF ϭ 79) p Infantile esotropia (N ϭ 7) Acquired strabismus (N ϭ 10) Anisometropia (N ϭ 8) Mixed (N ϭ 8) Deprivation (N ϭ 6) F(4,39) p Vertical adjusted time (s) 41.12 (6.79) 42.13 (9.05) 42.33 (8.20) 0.570 0.570 39.29 (6.85) 42.90 (9.22) 37.38 (3.96) 42.50 (5.68) 50.00 (14.93) 2.098 0.103 Horizontal adjusted time (s) 52.71 (11.54) 53.18 (16.96) 51.13 (13.30) 0.145 0.885 47.29 (8.75) 52.80 (13.68) 46.63 (6.61)a 56.38 (19.77) 65.17 (29.03)a 1.386 0.260 Number of errors 0.98 (2.42) 1.62 (3.60) 2.17 (4.10) 0.944 0.348 2.71 (5.62) 0.60 (1.35) 0.38 (0.52) 1.50 (3.51) 3.83 (5.23) 1.198 0.329 Ratio (horz time/vert time) 1.27 (0.19) 1.25 (0.20) 1.21 (0.19) Ϫ0.551 0.583 1.21 (0.17) 1.23 (021) 1.25 (0.15) 1.31 (0.28) 1.26 (0.17) 0.264 0.899 Mean (standard deviation) of data presented. a Post hoc tests indicate significant differences between subgroups. TABLE 3. Number of subjects with DEM scores below 15th percentile Total N (% of subjects) Amblyopic group Control group ␹2 (dF ϭ 1) p Horizontal time Ն53 s 6 (7%) 4 (10%) 2 (5%) 0.890 0.345 Vertical time Ն64 s 12 (15%) 6 (15%) 6 (14%) 0.032 0.858 Number of errors Ն4 11 (14%) 6 (15%) 5 (12%) 0.209 0.648 Ratio Ն1.40 15 (19%) 7 (18%) 8 (19%) 0.016 0.899 Developmental Eye Movement Test in Children with Amblyopia—Webber et al. 763 Optometry and Vision Science, Vol. 86, No. 6, June 2009
  • 5. though those with no measurable stereopsis recorded the highest mean number of errors, these differences did not reach significance as shown in Table 5. DISCUSSION This is the first study to report the performance of a group of amblyopic children on a clinical measure of saccadic eye move- ments and to compare that performance to an age-matched control group with normal vision. Our findings indicate that, despite significantly reduced VA in both the affected and fellow eyes, reduced or absent stereopsis, and significantly greater hyperopic refractive errors, the scores of the amblyopic children were sim- ilar to those of control children for the outcome measures of the DEM test: vertical time, horizontal time, number of errors and ratio(horizontal time/vertical time). In addition to determining that the ability of amblyopic chil- dren to quickly execute saccades to fixate, identify, and name single digits was not significantly different from that of their age-matched peers, we found that the outcome measures of the DEM did not significantly relate to measures of VA in either eye, levels of binoc- ular function, or magnitude of refractive correction. The prevalence of clinically unacceptable performance on the DEM was equivalent in the amblyopic and control groups and agreed with published normative data for the DEM test, suggesting that under habitual binocular viewing conditions amblyopia does not result in a functionally relevant reduction in saccadic eye move- ment speed and accuracy. The DEM provides an indirect, quantitative evaluation of sac- cadic eye movements based on the speed with which a series of numbers can be seen, recognized, and verbalized with accuracy.18 It is thus purported to detect oculomotor dysfunction and is recommended in optometric clinical practice guidelines for the quantitative evaluation of saccadic eye movements in children for learning-related vision problems.33 The horizontal subtest mimics the eye movements made during reading, with saccades of variable length required to fixate on the irregularly spaced single digits (N10 font size) along horizontal rows, whereas the vertical subtests give a base measure of how quickly the child can name 80 numbers without having to make the saccadic eye movements along rows. The time to complete the task and the number of errors are the clinical outcomes, with significantly slower and/or error prone performance on the horizontal task than the vertical task, that is a higher Ratio score, indicating poor saccadic eye movement con- trol.17 Poor performance on both the vertical and horizontal subtests would indicate slow automatic naming ability.17 A clinical purpose of the DEM is to help practitioners determine whether poor saccadic tracking may contribute to poor reading behavior.17 Indeed, a sustained and prevalent controversy in read- ing eye movement research is whether fluent reading is controlled by low-level eye movement efficiency, as would be measured by the DEM, or whether it is influenced by the more moment-to- moment cognitive processes.14 The DEM has been found to pre- dict students with below-average reading performance,34 and to relate to parental observation of errors during reading, such as losing place or omitting words when reading or copying and re- reading lines unknowingly.18 However, despite recognition of reading as an important vision dependent ability that contributes to an individual’s quality of life,35 few studies have evaluated the reading performance of amblyopes under habitual binocular view- ing conditions. Specific reading disability was found to be rela- tively rare in a small sample of children with amblyopia (n ϭ 20),36 and not more prevalent than reported in the general population. Conversely, Stifter et al.37 recently reported functionally relevant reading impairment (reduced maximum reading speed under binoc- ular viewing conditions) in micro-strabismic children (n ϭ 20; age, 11.5 Ϯ 1.1 years). Our finding that amblyopia had no effect on eye movements when assessed with the DEM indicates that the deficit in binocular reading speed reported in amblyopic children37 is not TABLE 5. Difference in DEM results between binocular function groups DEM outcome measure Nil stereopsis N ϭ 23 Reduced stereopsis N ϭ 14 Normal stereopsis N ϭ 44 F(2,78) p Vertical time (s) 43.52 (10.60) 40.29 (6.56) 41.02 (6.59) 0.985 0.378 Horizontal time (s) 55.78 (20.73) 49.29 (9.46) 52.61 (11.21) 0.919 0.403 Number of errors 2.43 (4.04) 0.50 (0.76) 0.93 (2.38) 2.495 0.089 Ratio(horizontal time/vertical time) 1.26 (0.24) 1.22 (0.13) 1.27 (0.16) 0.416 0.661 TABLE 4. Difference in DEM results between amblyopic VA groups DEM outcome measure VA in worse eye Յ0.20 logMAR N ϭ 19 VA in worse eye Ͼ0.20 logMAR N ϭ20 T(dF ϭ 37) p Vertical time (s) 41.26 (6.69) 42.95 (10.95) Ϫ0.5777 0.568 Horizontal time (s) 53.37 (14.26) 53.00 (19.63) 0.067 0.947 Number of errors 1.89 (4.04) 1.35 (3.20) 0.468 0.642 Ratio(horizontal time/vertical time) 1.29 (0.23) 1.21 (0.15) 1.314 0.197 764 Developmental Eye Movement Test in Children with Amblyopia—Webber et al. Optometry and Vision Science, Vol. 86, No. 6, June 2009
  • 6. explained by poor saccadic eye movement efficiency. Stifter et al.37 also reported that better binocular reading speed in the amblyopic group was associated with more central and steady fixation and better sensory binocular function, but did not relate to age, VA, accommodative impairment, strabismic angle, or refractive error. In this study, timed outcome measures on the DEM were not associated with history of strabismus, VA in either eye, level of binocular function, or magnitude of refractive error. It has been reported that the reading speed of well-corrected fluent observers reading ordinary text under adequate lighting con- ditions is limited by letter spacing (crowding) and is independent of text size, contrast, and luminance, provided that text contrast is at least four times the threshold contrast for an isolated letter.38 Levi et al.39 recently demonstrated that crowding rather than acu- ity limits reading in amblyopic observers, as well as in normal observers, in both central and peripheral vision. Crowding should not influence performance on the DEM because the test targets consist of 3 mm tall, high-contrast single digits (approximately N10) with 5 mm between rows of numbers and spacing of 10 to 25 mm between numbers. The extent to which crowding may explain the reduction in reading speed measured under binocular condi- tions as reported by Stifter et al.37 remains unclear. Amblyopia is the most common cause of reduced vision in chil- dren and young people, with significant costs to both the individual and community for screening and treatment. Although a number of functionally relevant deficits in tasks that contribute to quality of life have now been reported,40 the educational, health, and social life outcomes of amblyopes do not appear to be affected.11 In addition to determining the extent of functionally relevant deficits in performance that may accompany amblyopia, it is important to have an understanding of how children with amblyopia perform on clinical tests commonly used in pediatric practice. Our present findings demonstrate that under habitual binocular viewing con- ditions, amblyopia does not impact on clinical measures of sac- cadic eye movement efficiency. Although our finding suggests that reports of reduced reading speed in amblyopia are not due to poor eye movement control, further studies employing more direct and objective measures of eye movements during reading are required to further explore this relationship. Understanding the influence of amblyopia on performance is important for clinicians when interpreting test results and for pro- viding advice to parents of the consequences of amblyopia. Clinical treatment plans for amblyopia aim to improve VA and binocular function outcomes. However, the relationship between degraded vision and performance both on clinical tests of visual efficiency and on visually directed tasks relevant to children is yet to be fully established and warrants further study. Received July 8, 2008; accepted August 20, 2008. REFERENCES 1. Attebo K, Mitchell P, Cumming R, Smith W, Jolly N, Sparkes R. Prevalence and causes of amblyopia in an adult population. Ophthal- mology 1998;105:154–9. 2. 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