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Frequency of Visual Deficits in Children
With Developmental Dyslexia
Aparna Raghuram, OD, PhD; Sowjanya Gowrisankaran, PhD; Emily Swanson, BS;
David Zurakowski, MS, PhD; David G. Hunter, MD, PhD; Deborah P. Waber, PhD
IMPORTANCE Developmental dyslexia (DD) is a specific learning disability of neurobiological
origin whose core cognitive deficit is widely believed to involve language (phonological)
processing. Although reading is also a visual task, the potential role of vision in DD has been
controversial, and little is known about the integrity of visual function in individuals with DD.
OBJECTIVE To assess the frequency of visual deficits (specifically vergence, accommodation,
and ocular motor tracking) in children with DD compared with a control group of typically
developing readers.
DESIGN, SETTING, AND PARTICIPANTS A prospective, uncontrolled observational study was
conducted from May 28 to October 17, 2016, in an outpatient ophthalmology ambulatory
clinic among 29 children with DD and 33 typically developing (TD) children.
MAIN OUTCOMES AND MEASURES Primary outcomes were frequencies of deficits in vergence
(amplitude, fusional ranges, and facility), accommodation (amplitude, facility, and accuracy),
and ocular motor tracking (Developmental Eye Movement test and Visagraph eye tracker).
RESULTS Among the children with DD (10 girls and 19 boys; mean [SD] age, 10.3 [1.2] years)
and the TD group (21 girls and 12 boys; mean [SD] age, 9.4 [1.4] years), accommodation
deficits were more frequent in the DD group than the TD group (16 [55%] vs 3 [9%];
difference = 46%; 95% CI, 25%-67%; P< .001). For ocular motor tracking, 18 children in the
DD group (62%) had scores in the impaired range (in the Developmental Eye Movement test,
Visagraph, or both) vs 5 children in the TD group (15%) (difference, 47%; 95% CI, 25%-69%;
P< .001). Vergence deficits occurred in 10 children in the DD group (34%) and 5 children in
the TD group (15%) (difference, 19%; 95% CI, –2.2% to 41%; P= .08). In all, 23 children in the
DD group (79%) and 11 children in the TD group (33%) had deficits in 1 or more domain of
visual function (difference, 46%; 95% CI, 23%-69%; P< .001).
CONCLUSIONS AND RELEVANCE These findings suggest that deficits in visual function are far
more prevalent in school-aged children with DD than in TD readers, but the possible cause
and clinical relevance of these deficits are uncertain. Further study is needed to determine
the extent to which treating these deficits can improve visual symptoms and/or reading
parameters.
JAMA Ophthalmol. 2018;136(10):1089-1095.doi:10.1001/jamaophthalmol.2018.2797
Published online July 19, 2018.
Invited Commentary
page 1096
Supplemental content
CME Quiz at
jamanetwork.com/learning
and CME Questions page 1212
Author Affiliations: Author
affiliations are listed at the end of this
article.
Corresponding Author: Aparna
Raghuram, OD, PhD,Depar tment of
Ophthalmology, Boston Children’s
Hospital, 300 Longwood Ave,
Boston, MA 02115 (aparna.raghuram
@childrens.harvard.edu).
Research
JAMA Ophthalmology | Original Investigation
(Reprinted) 1089
© 2018 American Medical Association. All rights reserved.
Downloaded From: by a Harvard University User on 10/12/2018
Developmental dyslexia (DD) is a reading disorder that
emerges in childhood. The primary deficit involves im-
paired single-word decoding, word recognition, and
spelling, which may affect the a child’s reading rate, compre-
hension, and written expression later on. The disorder is gen-
erally viewed as stemming from a core linguistic deficit in pho-
nological processing; the recommended interventions are
educational and are theoretically guided by this premise.
1
Al-
though experts have historically dismissed claims that visual
processing might contribute meaningfully to the deficits
present in DD,
2,3
vision therapy has been recommended for
decades by behavioral optometrists to improve purported
visual symptoms.
4-6
Vision therapy is based on the premise that correctingperiph-
eral visual deficits (specifically vergence, accommodation, and
ocular motor tracking) will improve reading performance, yet
there is a dearth of controlled studies documenting that such defi-
cits are more common in children with DD, much less whether
treating them could improve reading. A well-documented ac-
counting of whether visual deficits are more prevalent in chil-
dren with DD is thus a necessary prerequisite to any controlled
evaluation of interventions to correct such deficits.
The primary goal of this study, therefore, was to assess the
prevalence and nature of visual deficits in children with dys-
lexia and compare them with a control group of typically devel-
oping (TD) readers. Wesought to provide initial estimates of what
visual functions specifically are affected in children with DD, the
frequency and magnitude of any abnormal findings, and whether
these deficits cluster in a subgroup of readers with dyslexia or
are more evenly distributed across the population.
Methods
Study Design and Participants
A prospective, uncontrolled, group comparison observational
study was conducted from May 28 to October 17, 2016. Chil-
dren who received a diagnosis of DD were recruited from a hos-
pital-based clinic, and a control group of TD readers were re-
cruited from patients receiving standard eye examinations in
the same hospital, as well as by flyers and word of mouth. In-
formed written assent was obtained from each participant, and
informed written consent was obtained from each parent or
guardian. The ethics committee of Boston Children’s Hospital
approved the research protocol. The entire study was con-
ducted according to the principles of the Declaration of Helsinki.
7
Inclusion criteria for the DD group were diagnosis of DD, 7
to 11 years of age, best-corrected visual acuity better than or equal
to 20/25 in each eye, and residing within 120 km (75 miles) of
the research site. Exclusion criteria were diagnosis of attention-
deficit/hyperactivity disorder documented by questionnaires,
IQ less than 70, diagnosis of a comorbid neurodevelopmental
disorder (eg, autism spectrum disorder, brain malformation,or
neurogenetic disorder) or medical illness, history of eye sur-
gery, structural anomalies of the anterior or posterior segment
of the eye or medical condition that could affect the ability to
participate in the study, or other ocular pathologic conditions.
The inclusion and exclusion criteria for the TD group were the
same except that the child must not have received a diagnosis
of DD or extra reading support within either general or special
education. Of 50 potentially eligible children identified with
DD, 29 agreed to participate and completed the evaluation.
Thirty-three children participated in the TD group.
Procedure
Participants were invited to the laboratory for a visit of ap-
proximately 2 hours, during which psychoeducational test-
ing, a comprehensive eye examination, and visual function
measures were performed as detailed herein.
Measures
Psychoeducational Testing
Psychoeducational testing included documentation of IQ
(2-subtest version of the Wechsler Abbreviated Scale of Intel-
ligence–II) and of single-word reading and spelling (Wood-
cock Reading Mastery Test, Word Identification and Word
Attack subtests, and Test of Written Spelling).
Vision Testing
Vision testing included a standard eye examinationincluding
pupil dilation and cycloplegic refraction. A detailed descrip-
tion of the assessments of visual function—vergence, accom-
modation, and ocular motor tracking—is provided in the
eAppendix in the Supplement. In brief, vergence was as-
sessed for amplitude, fusional ranges, and facility. Accommo-
dation was assessed for amplitude, facility, and accuracy.
Ocular motor tracking was assessed using 2 methods: a printed
test involving numbers oriented vertically and horizontally(D e-
velopmental Eye Movement [DEM] test) and an infrared eye
tracking test performed during reading activities (Visa-
graph). These assessments were performed with appropriate
refractive correction in place and in free space.
eTable 1 in the Supplement details the diagnoses for ver-
gence and accommodation deficits and their corresponding
criteria.
8-11
For the ocular motor tracking parameters, DEM and
Visagraph, scores below the 25th percentile for the TD group
were considered abnormal in the absence of well-established
criteria in the literature. Formeasures of accommodation per-
formed monocularly, the value from the eye with the lowest
performance was used for analysis.
Statistical Analysis
Group differences in demographic characteristics, psychoedu-
cational performance, vision, and visual function assessments
Key Points
Question Are deficits in visual function more frequent in children
with developmental dyslexia than in typically developing readers?
Findings In this cohort study, school-aged children with
developmental dyslexia exhibited more deficits in visual function—
vergence, accommodation, and/or ocular motor tracking—than did
a nonrandomized control group of typically developing children.
Meaning These findings suggest that visual function deficits contribute
to reading acquisition in children with developmental dyslexia.
Research Original Investigation Frequency of Visual Deficits in Children With Developmental Dyslexia
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were assessed by ttests for continuous variables and χ
2
tests for
categorical variables. For continuous variables, Ftests based on
univariate analysis of variance and 2-way analysis of covari-
ance (ANCOVA) were performed to evaluate group differences,
adjusting for age, sex, and IQ differences as appropriate.All 95%
CIs were calculated using the Wilson method.
12
A 2-sided P<.01
was used to address type I errors due to multiple outcome analy-
ses and testing.
13
Statistical analysis was performed using SPSS
Statistics, version 23.0 (IBM Corp).
Results
Participant Characteristics
The Table shows the demographic and psychometric charac-
teristics of the participants in both groups. The DD group was
somewhat older (mean [SD] age, 10.3 [1.2] years vs 9.4 [1.4]
years) and had a higher proportion of boys than the TD group
(19 [66%] vs 12 [36%]), as is typical; the TD group had a higher
proportion of Asian children than the DD group (17 [52%] vs
0). The mean (SD) IQ for the DD group was in the average range
(104.97 [12.05]), but the mean (SD) IQ for the TD group was in
the high average range (117.88 [10.83]). There were group dif-
ferences in reading and spelling (Word Identification, t= 12.32;
WordAttack, t= 9.2; and Spelling, t= 8.45; all P< .001), which
remained highly significant after adjusting for IQ (WordIden-
tification, F= 101.07; Word Attack, F= 48.92; and Spelling,
F= 39.65; all P< .001). All parametric analyses for the vision
measures were adjusted for age and sex. Using ANCOVA, we
did not find IQ to be a significant covariate or to change the
findings in a meaningful way, so it was not included as a co-
variate for the vision measures.
Vision Measures
Refractive Error and Eye Alignment
The median cycloplegic refractive error did not differ between
the 2 groups (DD group: 0.75 diopters [D] [range, 2.25 to –4.75
D]; TD group: 0.50 D [range, 1.75 to –3.75 D]). The distribution
of eye alignment (based on the cover test) did not differ by
group for distance or near (eTable 2 in the Supplement).
Vergence
Individual vergence measures, including the near point of con-
vergence test and near fusional convergenceranges, were sig-
nificantly reduced in the DD group (eTable 3 in Supplement).
Furthermore, full criteria for a diagnosis of vergence deficit
were met in twice as many children in the DD group (10 [34%];
7 convergence excess and 3 convergence insufficiency) as in
the TD group (5 [15%]; 4 convergence excess and 1 conver-
gence insufficiency). This latter difference did not reach sta-
tistical significance (χ
2
= 3.15; difference, 19%; 95% CI, –2.2%
to 41%; P= .08).
Accommodation
The proportion of children who met the criteria for a diagno-
sis of accommodation deficiency was higher in the DD group
(16 [55%]; 9 accommodative insufficiency, 6 accommodative
dysfunction, and 1 accommodative infacility) than in the TD
group (3 [9%]; all accommodative insufficiency) (χ
2
= 15.42;
difference, 46%; 95% CI, 25%-67%; P< .001). An uncor-
rected refractive error greater than 0.75 D was present in 5 of
9 children in the DD group and 2 of 3 children in the TD group
with accommodative insufficiency. The amplitude of accom-
modation (F= 13.67) and monocular accommodative facility
(F= 18.11) also differed by group (P< .001 for both; eTable 4
in the Supplement). Overall, the number of children who had
vergence and/or accommodation deficits was substantially
higher in the DD group than in the TD group (18 [62%] vs 7
[21%]), as detailed in Figure 1.
14
Ocular Motor Tracking
DEM Test|One child with DD was overwhelmed by the DEM task
and could not complete it. For the DEM parameters (horizon-
tal and errors), the DD group performed more poorly than the
TD group, as seen from results of 2-way ANCOVA (Figure 2).
The proportion of children from the DD group obtaining scores
Table. DemographicCharacteristics and Performance
of Psychoeducational Measures of Developmental Dyslexia
and Typical Reading Groups
Characteristic
Individuals With
Developmental
Dyslexia
(n = 29)
Typically
Developing
Readers
(n = 33)
Age, mean (SD), y 10.3 (1.2) 9.4 (1.4)
Male, No. (%) 19 (66) 12 (36)
Race, No. (%)
White 29 (100) 16 (48)
Asian 0 17 (52)
Psychoeducational Test Scores at Time of Study
WRMT Word Identification
Mean (SD) 87.55 (15.65) 122.58 (15.94)
Median (range) 89 (55-112) 127 (95-145)
WRMT Word Attack
Mean (SD) 87.55 (9.43) 111.33 (11.73)
Median (range) 86 (63-112) 110 (92-134)
Test of written spelling
Mean (SD) 80.93 (13.44) 110.91 (14.36)
Median (range) 82 (45-105) 111 (83-140)
WASI-II estimated IQ
Mean (SD) 104.97 (12.05) 117.88 (10.83)
Median (range) 105 (83-133) 118 (95-138)
Psychoeducational Test Scores at Time of Clinical Evaluation
Elapsed time since
evaluation, y
Mean (SD) 1.68 (1.17) NA
Median (range) 1.72 (0.16-4.15) NA
WRMT Word Identification
a
Mean (SD) 80.62 (10.68) NA
Median (range) 81.00 (55-102) NA
WRMT Word Attack
b
Mean (SD) 83.88 (7.11) NA
Median (range) 83.50 (70-98) NA
Abbreviations: NA, not applicable; WASI-II, Wechsler Abbreviated Scale of
Intelligence–second edition; WRMT,Woodcock Reading Mastery Test.
a
For 29 children.
b
For 26 children.
Frequency of Visual Deficits in Children With Developmental Dyslexia Original Investigation Research
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in the failing range for the DEM test was elevated for both the
error (66%; χ
2
=10.70;P= .001)and horizontal (55%; χ
2
= 6.22;
P= .01) scores (eFigure 1A and B in the Supplement). Nearly
half (13 of 29 [45%]) of the children in the DD group per-
formed in the failing range for both the error and horizontal
scores compared with only 1 child in the TD group (3%).
Visagraph |Data could not be obtained for 2 children in the DD
group (1 child reading below the first grade reading level; the
other owing to examiner error). The text was chosen based on
the grade equivalent level from the Woodcock Reading Mastery
Test Word Identification. Forall 33 children in the TD group, the
grade equivalent was at or abovetheir c urrentgrade placement.
Of the 27 children in the DD group, 16 had a grade equivalent at
least 1 year below their current grade placement, and 11 had a
grade equivalent at their current placement. Datawere retained
for analysis only if the reading comprehension questions were
answered at or above 60% accuracy; all children except 1 in the
DD group met this criterion. The mean (SD) reading comprehen-
sion was comparable across the groups (DD group below their
grade placement, 85% [13.6%]; DD group at their grade place-
ment, 81% [14.5%]; and TD group, 89% [10.1%]).
Both DD subgroups performed more poorly than the TD
group on all Visagraph parameters but did not differ from each
other as seen from the results of 2-way ANCOVA (Figure 3). Nine
children in the DD group also completed the task with a text 1
level below their grade equivalent; their readingrate (F= 16.97),
fixations (F= 18.40), and regressions (F= 13.65) werestill poorer
than those of controls (P< .01 with 2-way ANCOVA). As illus-
trated in eFigure 2A to C in the Supplement, the proportion of
individuals with Visagraph impairments was greater in the DD
group for reading rate (21 of 26 [81%]), fixations (16 of 26 [62%]),
and regressions (15 of 26 [58%]) (reading rate, χ
2
= 18.59; fixa-
tions, χ
2
= 8.38; regressions, χ
2
= 8.28; all P< .01). A total of 13
children (50%) in the DD group achieved scores in the impaired
range for both fixations and regressions compared with only 5
children (15%) in the TD group. The DEM Horizontal score had
a moderate correlation with all 3 Visagraph parameters (r= 0.49-
0.51; P<.001;eTable5intheSupplement). Overall, 18 children
in the DD group (62%) had scores in the impaired range on the
DEM and/or Visagraphcompared w ithonly 5 children in the TD
group (15%) (difference, 47%; 95% CI, 25%-69%; P< .001).
Distribution of Visual Function Deficits Within the DD Group
Of the 29 children with DD, 23 (79%) had a deficit in 1 or more
domain compared with only 11 (33%) in the TD group. Among
the children in the DD group, deficits were observed in more
than 1 domain in 15 children (52%) and in 1 domain in 8 chil-
dren (28%) (Figure 4).
14
Discussion
The goals of this study were to determine whether deficits in
peripheral visual function (vergence, accommodation, and ocu-
lar motor tracking) are more prevalent in children with DD.Spe-
cifically, it addressed which functions were most promi-
nently affected, the frequency and magnitude of abnormal
findings, and whether deficits clustered in a subgroup or were
more evenly distributed across the DD group.
The prevalence of visual deficits was high among children
with DD; 23 (79%) met the criteria for a diagnosis of deficit in 1
or more domains of vergence, accommodation, and/or track-
ing compared with only 11 children in the TD group (33%). Ac-
commodation and ocular motor tracking were significantly im-
paired in children in the DD group, as were differences in 3
specific measures of vergence (but not in overall impairment
of vergence.) These deficits were not equally distributed across
the DD group. A total of 15 of the children in the DD group (52%)
had deficits in more than 1 domain, 8 (28%) had deficits in 1 do-
main, and 6 (21%) did not have deficits.
The potential role of vision deficits in DD has been con-
troversial, and it has been argued that specific vision-related
deficits are no more prevalent in individuals with DD than in
Figure 2. Mean (SE) Developmental EyeMovement Test Scores
for the Typically Developing(TD) Readers and Individuals
With Developmental Dyslexia (DD)
120
110
100
90
80
70
60
Standard Score
Vertical Horizontal Ratio Error
DD group
TD group
Vertical, F
1,61
=5.77;P= .02;horizontal, F
1,61
= 12.09; P= .001; ratio, F
1,61
= 4.72;
P= .03; and error, F
1,61
= 18.63; P< .001.
Figure 1. Distributionof Vergence and Accommodation Deficits Between
Individuals With Developmental Dyslexia and TypicallyDeveloping Readers
Vergence
4-Convergence
excess
1-Convergence
insufficiency
Accommodation
3-Accommodative insufficiency
Accommodation
9-Accommodative insufficiency
6-Accommodative dysfunction
1-Accommodative infacility
7-Convergence excess
3-Convergence
insufficiency
Vergence
2
1
4
2
8
8
Typically developing
readers (n
=
33)
Individuals with developmental dyslexia (n
=
29)
Overlapping circles indicate patients who had both vergence and
accommodation deficits. The numerals in the circles indicate number of
patients. The specific types of vergence and accommodation deficits are also
detailed (χ
2
= 15.6; difference, 41%; 95% CI, 18%-69%; P< .001).
Research Original Investigation Frequency of Visual Deficits in Children With Developmental Dyslexia
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the general population.
3
The lack of a control group in prior
clinical studies has also been criticized.
15
In the present pro-
spective controlled study, however, we documented a higher
prevalence of vision deficits in a well-characterized group of
children with DD. Nevertheless, the contribution of these
deficits remains uncertain.
Vergence
Although convergence insufficiency has been viewed as a po-
tential problem in children with reading deficits,
16,17
the fre-
quency of children who met the criteria for a diagnosis of ver-
gence deficit was unexpectedly similar in our DD and TD
groups. Moreover, in both groups, the deficit was much more
likely to involve convergence excess than convergence insuf-
ficiency, which was infrequent in our sample. Prior studies of
vergence in DD have mostly assessed performance on ver-
gence tests rather than documenting a clinical diagnosis; hence,
their findings are not directly comparable to ours.
18-20
Con-
sistent with such studies,
18,19,21,22
we did find statistically
significant differences on individual vergence tests, includ-
ing the near point of convergence, positive fusional ranges at
near, and vergence facility. Several studies reported a diagno-
sis of vergence deficit in children who had a generic learning
disability but not necessarily dyslexia.
22,23
Ygge et al,
20
how-
ever, did not document diagnoses of vergence deficit even on
individual tests for children with dyslexia.
Accommodation
More than half the children in the DD group (16 [55%]) met the
criteria for a diagnosis of accommodation deficit compared with
only 3 (9%) in the TD group. Approximately two-thirdsof these
children in the DD group had accommodative insufficiency, and
the rest had generalized accommodative dysfunction. At the
level of individual tests, the amplitude of accommodation was
lower in the DD group than in the TD group, consistent with
other studies.
18,24
Children in the DD group recorded fewer
cycles on the monocular and binocular accommodative facil-
ity test, indicating that their accommodation dynamics were
slower to react than those of the TD group.
Ocular Motor Tracking
More than half of the children in the DD group (18 [62%]) ex-
hibited ocular motor tracking deficits when reading nonlin-
guistic stimuli (DEM). They also showed elevated deficits in
rate, fixations, and regressions on the Visagraph, even when
reading text at their grade-equivalent level with adequate
Figure 3. Mean (SE) Visagraph EyeTracker Parameters in TypicallyDeveloping (TD) Readers and Individuals
With Developmental Dyslexia (DD)
250
200
150
100
50
0
Reading Rate, Words/min
TD Group DD Group
at Grade
Level
DD Group
Below Grade
Level
Visagraph reading rate
A
300
250
200
150
100
50
0
Fixations, per 100 Words
TD Group DD Group
at Grade
Level
DD Group
Below Grade
Level
Visagraph fixations
B
70
60
50
40
30
20
10
0
Regressions, per 100 Words
TD Group DD Group
at Grade
Level
DD Group
Below Grade
Level
Visagraph regressions
C
A, Reading rate, F
2,59
= 15.63;
P< .001. B, Fixations, F
2,59
= 16.12;
P< .001. C, Regressions,
F
2,59
= 14.64; P< .001. In the DD
group, 15 children had a reading
proficiency at grade level, and 11
children had a reading proficiency
below grade level. For all 3
parameters, both DD subgroups
performed more poorly than the TD
group (P< .001) but not different
from each other.
Figure 4. Distribution of Visual Function Deficits Between Individuals With DevelopmentalDyslexia (DD) and
Typically Developing(TD) Readers
3
22
11
24
2
3
5
6
5
26
Ocular motor tracking
A
ccommo
d
atio
n
Accommo
d
ation
Ocular motor tracking
V
ergence
V
ergenc
e
No deficits
No deficits
Individuals with developmental dyslexia (n
=
29) Typically developing readers (n
=
33)
The numerals in the circles indicate
number of patients. The DD group
had more deficits (79%) than the TD
control group, and the deficits (33%)
clustered in subgroups of individuals
with DD (χ
2
= 13.18; difference, 46%;
95% CI, 23%-69%; P< .001).
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comprehension. Some have questioned whether DEM is a valid
measure of saccadic eye movements.
25,26
In our study, DEM
horizontal gaze parameters had a moderate correlation with
Visagraph parameters, supporting its utility as a clinical
screener of ocular motor tracking in children.
Visual Function and Reading
Although this study documents a higher frequency of im-
paired visual function in children with DD, the association with
the reading process is uncertain. Clinically, patients with ac-
commodation deficits can report blurry vision at near, words
coming in and out of focus, difficulty maintaining clear vi-
sion while reading, and difficulty switching focus from dis-
tance to near.
27-29
Although the amplitude of accommoda-
tion of the DD group was not within a range expected to cause
near-vision work-related blur or asthenopic symptoms, the
push-up method we used overestimates amplitude of
accommodation.
30
Hence, the decrease in accommodation ob-
served in the DD group could have been greater had objective
measures been used, within a range that could cause diffi-
culty sustaining clear near vision.
30
Accommodative facility has been correlated with reading
prowess in children in the first grade,
31
and vergence facility
correlated significantly with the reading rate among children
with learning disabilities,
22
but, again, the direction of causa-
tion and functional significance is uncertain. The Conver-
gence Insufficiency Treatment Trials showed that eye exer-
cises improved near work-related symptoms in children with
reduced accommodation and convergence.
8,32
In children with
learning disabilities with nonstrabismic binocular vision
anomalies, eye exercises improved vergence, accommoda-
tion, and tracking, but their effect on reading was not studied.
33
Horizontal vergence training improved reading speed and
positive fusional vergence in an uncontrolled trial in children
with dyslexia and normal binocular vision.
24
More evidence
is needed to further establish the association between
vergence and accommodation deficits and reading metrics.
Tracking has also been associated with reading. Horizon-
tal DEM scores are correlated with the reading rate amongchil-
dren with dyslexia and poor readers.
34,35
In addition, beginning
readers exhibit more fixations, longerfixation duration, shorter
saccades, and more regressions than skilled readers, but these
deficits persist in children with dyslexia and are specific to
reading.
32-37
Because eye movements can be influenced by
higher-order cognitive and linguistic demands, such visual defi-
cits in children with dyslexia have been understood as effects
of the reading deficits rather than as a low-order pure ocular
motor deficit that might affect reading. Similarly, deficits in
ocular motor skills in children with DD are comparable to those
of reading age–matched controls (but inferior to those of
typically reading chronological age controls), suggesting an
immature ocular motor system in children with DD. Again,
whether this result is a cause or an effect of reading impair-
ment is uncertain.
36
In our study, children in the DD group read texts corre-
sponding to their single-word reading grade-equivalent
level. Although their comprehension was adequate, they still
made more fixations and regressions than children in the TD
group. These results do not necessarily support a causal role
for ocular motor deficits in children with dyslexia; instead, they
document the presence of ocular motor deficits even when the
children with dyslexia read passages at their readinglevel. Chil-
dren with dyslexia with short visual spans had more right-
ward fixations in reading text but performed similarly to con-
trols on a visual search task; these short visual spans influence
ocular motor tracking in dyslexia.
37
Such a mechanism could
also account for the ocular motor deficits in our DD group, even
when reading at their proficiency level.
Strengths and Limitations
The strengths of the study include the prospective, group
comparison design and the well-defined group with dyslexia
to ensure objective comparisons. The limitations are the
relatively small sample size and unmasked examiners. The
latter could be mitigated, in part, by the fact that most of the
data were collected electronically and not amenable to
examiner bias or influence.
Conclusions
This study demonstrates deficits in the visual functioning of
children with dyslexia. Although this comparative study does
not address any causal association of these deficits with read-
ing performance, the findings support further investigation of
visual function in dyslexia. We propose that assessmentof ver-
gence, accommodation, and eye movements may be helpful
in the initial evaluation of children with dyslexia and will
supplement the findings of a comprehensive ophthalmologic
examination and a detailed literacy evaluation. The study fur-
ther provides evidence that supports the design of controlled
cohort studies to determine whether treatment of these defi-
cits can bring about changes in visual symptoms and/or read-
ing parameters.
ARTICLE INFORMATION
Accepted for Publication: May 25, 2018.
Published Online: July 19, 2018.
doi:10.1001/jamaophthalmol.2018.2797
Author Affiliations: Department of
Ophthalmology, Boston Children’s Hospital, Boston,
Massachusetts (Raghuram, Gowrisankaran,
Swanson, Hunter); Department of Ophthalmology,
Harvard Medical School, Boston, Massachusetts
(Raghuram, Hunter); Department of
Anesthesiology, Boston Children’s Hospital, Boston,
Massachusetts (Zurakowski); Department of
Surgery, Boston Children’s Hospital, Boston,
Massachusetts (Zurakowski); Department of
Anesthesia, Harvard Medical School, Boston,
Massachusetts (Zurakowski); Division of
Psychology,Depar tment of Psychiatry, Boston
Children’s Hospital, Boston, Massachusetts
(Waber); Department of Psychiatry,Harvard
Medical School, Boston, Massachusetts (Waber).
Author Contributions: Drs Raghuram and Waber
had full access to all the data in the study and take
responsibility for the integrity of the data and the
accuracy of the data analysis.
Concept and design: Raghuram, Zurakowski,
Hunter, Waber.
Acquisition, analysis, or interpretation of data: All
authors.
Drafting of the manuscript: Raghuram, Zurakowski,
Waber.
Critical revision of the manuscript for important
intellectual content: All authors.
Statistical analysis: Raghuram, Zurakowski.
Obtained funding: Raghuram, Hunter.
Research Original Investigation Frequency of Visual Deficits in Children With Developmental Dyslexia
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Administrative, technical, or material support:
Raghuram, Swanson.
Supervision: Raghuram, Hunter, Waber.
Conflict of Interest Disclosures: All authors have
completed and submitted the ICMJE Form for
Disclosure of Potential Conflicts of Interest and
none were reported.
Funding/Support: This study was supported by a
Knights TemplarCareer Development Grant and a
Discovery Award from the Children’sHospital
Ophthalmology Foundation (Dr Raghuram).
Role of the Funder/Sponsor:The funding sources
had no role in the design and conduct of the study;
collection, management, analysis, and
interpretation of the data; preparation, review, or
approval of the manuscript; and decision to submit
the manuscript for publication.
REFERENCES
1. Eunice Kennedy Shriver National Institute of
Child Health and Human Development. Report of
the National Reading Panel: TeachingChildren to
Read (00-4769). Washington,DC: US Government
Printing Office; 2000.
2. Creavin AL, Lingam R, Steer C, Williams C.
Ophthalmic abnormalities and reading impairment.
Pediatrics. 2015;135(6):1057-1065.doi:10.1542/peds
.2014-3622
3. Handler SM, Fierson WM. Reading difficulties
and the pediatric ophthalmologist. J AAPOS.2017;
21(6):436-442. doi:10.1016/j.jaapos.2017.09.001
4. Garzia RP, Nicholson SB. Visual function and
reading disability: an optometric viewpoint. JAm
Optom Assoc. 1990;61(2):88-97.
5. Hoffman LG. Incidence of vision difficulties in
children with learning disabilities. JAmOptomAssoc.
1980;51(5):447-451.
6. Rosner J, Rosner J. Comparison of visual
characteristics in children with and without learning
difficulties. Am J Optom Physiol Opt. 1987;64(7):
531-533. doi:10.1097/00006324-198707000
-00008
7. World Medical Association. World Medical
Association Declaration of Helsinki: ethical
principles for medical research involving human
subjects. JAMA. 2013;310(20):2191-2194. doi:10
.1001/jama.2013.281053
8. Convergence Insufficiency Treatment Trial
(CITT) Study Group. The Convergence Insufficiency
Treatment Trial: design, methods, and baseline
data. Ophthalmic Epidemiol. 2008;15(1):24-36.
doi:10.1080/09286580701772037
9. Pediatric Eye Disease Investigator Group.
Home-based therapy for symptomatic convergence
insufficiency in children: a randomized clinical trial.
Optom Vis Sci. 2016;93(12):1457-1465. doi:10.1097
/OPX.0000000000000975
10. Scheiman M, Mitchell GL, Cotter S, et al;
Convergence Insufficiency Treatment Trial Study
Group. A randomized clinical trial of treatments for
convergence insufficiency in children. Arch
Ophthalmol. 2005;123(1):14-24.doi:10.1001/archopht
.12 3.1 .14
11. Scheiman M, Wick B. Clinical Management of
Binocular Vision: Heterophoric, Accommodative,
and Eye Movement Disorders.3rd ed. Philadelphia,
PA: Wolters Kluwer Health/Lippincott Williams &
Wilkins; 2008.
12. Brown LD, Cai TT, DasguptaA . Interval
estimation for a binomial proportion. Stat Sci. 2001;
16(2):101-117. doi:10.1214/ss/1009213286
13. Benjamini Y, Hochberg Y. Controlling the false
discovery rate: a practical and powerful approach to
multiple testing. J R Stat Soc B. 1995;57(1):289-300.
14. Hulsen T, de Vlieg J, AlkemaW. BioVenn—a web
application for the comparison and visualization of
biological lists using area-proportional Venn
diagrams. BMC Genomics. 2008;9:488. doi:10.1186
/1471-2164-9-488
15. American Academy of Pediatrics, Section on
Ophthalmology, Council on Children with
Disabilities; American Academy of Ophthalmology;
American Association for Pediatric Ophthalmology
and Strabismus; American Association of Certified
Orthoptists. Joint statement—learning disabilities,
dyslexia, and vision. Pediatrics. 2009;124(2):837-844.
doi:10.1542/peds.2009-1445
16. Borsting E, Mitchell GL, Kulp MT, et al; CITT
Study Group. Improvement in academic behaviors
after successful treatment of convergence
insufficiency. Optom Vis Sci. 2012;89(1):12-18. doi:
10.1097/OPX.0b013e318238ffc3
17. Scheiman M, Mitchell GL, Cotter SA, et al;
CITT-ART Investigator Group. Convergence
Insufficiency Treatment Trial–Attention and
Reading Trial(CIT T-ART):design and methods. Vis
Dev Rehabil. 2015;1(3):214-228.
18. Evans BJ, Drasdo N, Richards IL. Investigation
of accommodative and binocular function in
dyslexia. Ophthalmic Physiol Opt. 1994;14(1):5-19.
doi:10.1111/j.1475-1313.1994.tb00550.x
19. Latvala ML, Korhonen TT, PenttinenM, Laippala
P. Ophthalmic findings in dyslexic schoolchildren. Br
J Ophthalmol. 1994;78(5):339-343.doi:10.1136/bjo
.78.5.339
20. Ygge J, Lennerstrand G, RydbergA , Wijecoon S,
Pettersson BM. Oculomotor functions in a Swedish
population of dyslexic and normally reading
children. Acta Ophthalmol (Copenh). 1993;71(1):
10-21. doi:10.1111/j.1755-3768.1993.tb04953.x
21. Kapoula Z, Bucci MP. Posturalcontrol in dyslexic
and non-dyslexic children. J Neurol. 2007;254(9):
1174-1183. doi:10.1007/s00415-006-0460-0
22. Quaid P, Simpson T. Association between
reading speed, cycloplegic refractive error, and
oculomotor function in reading disabled children
versus controls. Graefes Arch Clin Exp Ophthalmol.
2013;251(1):169-187. doi:10.1007/s00417-012
-2135-0
23. Dusek W, Pierscionek BK, McClelland JF.
A survey of visual function in an Austrian
population of school-age children with reading and
writing difficulties. BMC Ophthalmol. 2010;10:16.
doi:10.1186/1471-2415-10-16
24. Wahlberg-Ramsay M, Nordström M, Salkic J,
Brautaset R. Evaluation of aspects of binocular
vision in children with dyslexia. Strabismus. 2012;
20(4):139-144. doi:10.3109/09273972.2012.735335
25. Ayton LN, Abel LA, Fricke TR, McBrien NA.
Developmental eye movement test: what is it really
measuring? Optom Vis Sci. 2009;86(6):722-730.
doi:10.1097/OPX.0b013e3181a6a4b3
26. Webber A, Wood J, Gole G, Brown B. DEM test,
Visagraph eye movement recordings, and reading
ability in children. Optom Vis Sci. 2011;88(2):295-302.
doi:10.1097/OPX.0b013e31820846c0
27. Daum KM. Accommodative dysfunction. Doc
Ophthalmol. 1983;55(3):177-198. doi:10.1007
/BF00140808
28. Hennessey D, Iosue RA, Rouse MW. Relation of
symptoms to accommodative infacility of
school-aged children. Am J Optom Physiol Opt.
1984;61(3):177-183. doi:10.1097/00006324
-198403000-00005
29. Levine S, Ciuffreda KJ, Selenow A, Flax N.
Clinical assessment of accommodative facility in
symptomatic and asymptomatic individuals. JAm
Optom Assoc. 1985;56(4):286-290.
30. Anderson HA, Stuebing KK. Subjective versus
objective accommodative amplitude: preschool to
presbyopia. Optom Vis Sci. 2014;91(11):1290-1301.
doi:10.1097/OPX.0000000000000402
31. Kulp MT, Schmidt PP. Visual predictors of
reading performance in kindergarten and first grade
children. Optom Vis Sci. 1996;73(4):255-262.doi:10
.1097/00006324-199604000-00007
32. Convergence Insufficiency Treatment Trial
Study Group. Randomized clinical trial of
treatments for symptomatic convergence
insufficiency in children. Arch Ophthalmol. 2008;
126(10):1336-1349.doi:10.1001/archopht.126.10.1336
33. Hussaindeen JR, Shah P, Ramani KK,
Ramanujan L. Efficacy of vision therapy in children
with learning disability and associated binocular
vision anomalies. J Optom. 2018;11(1):40-48. doi:10
.1016/j.optom.2017.02.002
34. Palomo-Alvarez C, Puell MC. Relationship
between oculomotor scanning determined by the
DEM test and a contextual reading test in
schoolchildren with reading difficulties. Graefes
Arch Clin Exp Ophthalmol. 2009;247(9):1243-1249.
doi:10.1007/s00417-009-1076-8
35. Northway N. Predicting the continued use of
overlays in school children—a comparison of the
Developmental Eye Movement testand the Rate of
Reading test. Ophthalmic Physiol Opt. 2003;23(5):
457-464. doi:10.1046/j.1475-1313.2003.00144.x
36. Bucci MP, Nassibi N, Gerard CL, Bui-Quoc E,
Seassau M. Immaturity of the oculomotor saccade
and vergence interaction in dyslexic children:
evidence from a reading and visual search study.
PLoS One. 2012;7(3):e33458. doi:10.1371/journal
.pone.0033458
37. Prado C, Dubois M, Valdois S. The eye
movements of dyslexic children during reading and
visual search: impact of the visual attention span.
Vision Res. 2007;47(19):2521-2530. doi:10.1016/j
.visres.2007.06.001
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