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CLINICAL SCIENCES
Development of Visual Acuity in Children
With Cerebral Visual Impairment
Mira Lim, MD; Janet S. Soul, MD; Ronald M. Hansen, PhD; D. Luisa Mayer, PhD;
Anne Moskowitz, OD, PhD; Anne B. Fulton, MD
Objective: To study the development of visual acuity in
Results: All children had measurable PL and VEP acu-
term-born children with cerebral visual impairment and
a history of neonatal hypoxic-ischemic encephalopathy.
ity, despite poor visual behavior. In nearly all, both PL and
VEP acuity were below normal for age. For both PL and
VEP measures, acuity at the last visit was, on average, 1
octave better than at the first visit, with a rate of improvement lower than normal. Although parallel courses of PL
and VEP development occurred in many, substantial disparities in PL and VEP acuity were observed in others.
Methods: We studied 19 term-born children, aged 6
months to 6 years, with moderate to severe neonatal hypoxic-ischemic encephalopathy and behaviors indicative
of cerebral visual impairment. Longitudinal measures of
grating acuity were obtained using preferential looking (PL)
and visual evoked potential (VEP) procedures. Visual acuities at first and last visits were compared. The courses of
acuity development in the 9 children who underwent both
VEP and PL acuity assessment at 4 or more ages were compared with normal development.
L
Author Affiliations:
Department of Ophthalmology,
Children’s Hospital and Harvard
Medical School, Boston, Mass.
Conclusions: Modest increases in PL and VEP grating
acuity occur during early childhood in many of these patients. The rate of increase is lower than normal.
Arch Ophthalmol. 2005;123:1215-1220
ITTLE IS KNOWN ABOUT THE
course of development of
acuity in cerebral visual impairment (CVI), the most
common cause of bilateral
visual impairment in infants and children.1 Typically, the ocular structures are
healthy and the pupillary responses are
brisk. In short, the ocular findings do not
explain the child’s visual impairment.
Anomalous behaviors in children with CVI
include avoidance of faces, light gazing,
and preference for moving rather than stationary objects and familiar rather than
novel objects. Visual response to complex visual displays is reduced, delayed,
or suppressed, especially in the presence
of competing auditory or tactile stimuli.1-6
Preferential looking (PL) and visual
evoked potential (VEP) measures of visual acuity are feasible and deemed reliable and valid in infants and children with
CVI.7-9 Both measures are used in clinical
practice. Visual evoked potential acuity depends on the integrity of the pathway from
the eye to the visual cortex. Preferential
looking acuity is also dependent on this
pathway, but additional factors such as attention and ocular motor abilities affect the
child’s response and thus the examiner’s
judgment of the child’s response. It is well
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1215
established that normal grating acuity,
whether measured by PL or VEP, increases during early childhood.10
Reports of young children with CVI often present the acuities as cross-sectional
data and include patients with diverse
causes of CVI.9,11-14 Serial measurements
of visual acuity in individual children, all
with the same cause of CVI, have seldom
been reported.9,11,13-15
The aim of this study is to determine
whether a developmental increment in visual acuity occurs in children with neonatal hypoxic-ischemic encephalopathy and
poor visual behavior consistent with CVI.
Herein we report longitudinal measures of
visual acuity in children with moderate to
severe neonatal hypoxic-ischemic encephalopathy who were born at term and were
referred because of CVI-like behaviors. Every patient underwent PL and VEP acuity
evaluations as a function of age.
METHODS
PATIENTS
All patients were referred because of parental
concern about visual impairment and behaviors consistent with CVI.2-5 All of the patients
had major disabilities in addition to the con-
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Table 1. Neurological Features
Patient No.
Postneonatal
Seizures
Motor Findings
Developmental
Quotient
Head Circumference,
Percentile
Score*
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
No
Yes
No
No
No
Yes
No
Yes
Yes
No
No
No
Yes
No
Yes
No
No
No
No
Quadriparesis
Quadriparesis
Quadriparesis
Quadriparesis
Ambulatory hemiparesis
Quadriparesis
Quadriparesis
Quadriparesis
Spastic quadriparesis
Quadriparesis
Dyskinetic spastic quadriparesis
Quadriparesis
Quadriparesis
Spastic quadriparesis
Quadriparesis
Ambulatory proximal weakness
Ambulatory spastic quadriparesis
Dyskinetic quadriparesis
Quadriparesis
⬍50
⬍50
⬍50
⬍50
68
⬍50
⬍50
⬍50
⬍50
⬍50
⬍50
⬍50
⬍50
⬍50
⬍50
50
⬍50
⬍50
⬍50
⬍2
⬍2
⬍2
⬍2
⬍2
⬍2
5
5
⬍2
⬍2
45
⬍2
⬍2
⬍2
⬍2
2
10
10
⬍2
2
3
2
2
1
3
1
2
3
2
1
2
3
2
3
0
1
1
3
*Described in the “Patients” subsection of the “Methods” section.
cerns about vision (Table 1). Clinical inclusion criteria for
this report were a history of birth at term, antenatal or perinatal distress or both, moderate to severe neonatal encephalopathy with seizures, and magnetic resonance imaging evidence
of brain injury in a pattern typical of hypoxic-ischemic encephalopathy. Each had assessment of his or her developmental quotient using the Bayley Scales of Infant Development.16
We excluded patients with metabolic disorders, hypoglycemia, trauma, abnormal ocular structures (except mild optic atrophy), or malformations of the brain.
The magnetic resonance imaging findings showed diffuse
signal abnormality in the subcortical gray matter, including
the thalamus and basal ganglia, and in the cerebral gray and
white matter, including portions of the optic radiations and
visual areas of the occipital cortex. Neurological features are
listed in Table 1. Every patient had some persistent motor abnormality; only 3 became ambulatory during the period of observation. Six patients had seizures after the neonatal period.
All but 2 patients had a developmental quotient below 50. A
normal developmental quotient16 is 100 (SD, 15). Head circumference was below the second percentile in most of the
patients. We considered unfavorable neurological features to
be seizures after the neonatal period, a developmental quotient less than 50, and acquired microcephaly with head circumference below the second percentile. Each of these features was scored, with 1 indicating unfavorable and 0,
favorable. The severity of neurological outcome was taken as
the sum of these scores (Table 1). Thus, those with the most
severe overall neurological outcome had a score of 3, and
those with less severe disease had a lower score.
Ophthalmic features (Table 2) included mild disc pallor
in 7 patients. All but 2 patients had strabismus. Most patients
were exotropic, typically with variable angle. All strabismus was
alternating. Four patients had nystagmus. The median spherical equivalent at the time of the first visual acuity test was ⫹1.50
diopters (D) (range, –1.63 to ⫹4.63 D). None had anisometropia greater than 1 D. Throughout their course, all except patient 19 had spherical equivalents within the 95% prediction
interval of normal for age.17 At 36 months of age, the spherical
equivalents for patient 19 were ⫹4.38 D OD and ⫹4.63 D OS.
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1216
Visual acuity testing in patient 19 was performed with correction in place.
VISUAL ACUITY TESTS
We included only patients who met the inclusion criteria described in the previous section, had both PL and VEP measurements of acuity at the same session on at least 1 date, and had
visual acuity (PL or VEP or both) measured at more than 1 session. Visits occurred during an 8-year period from March 1996
through February 2004. The median age at the first acuity test
was 15 months (range, 6-36 months). For the 9 patients who
had both PL and VEP acuity tests in the same session at 4 or
more ages, the median duration of follow-up was 29 months
(range, 24-76 months), during which time as many as 16 PL
and 6 VEP acuities were measured. Grating acuities were obtained with binocular viewing.
PL Procedure
A clinical variant of the Teller Acuity Card procedure was used
to measure PL acuity.18 The acuity cards were presented horizontally or vertically, lateral to, or central to the gaze direction
to ensure the child could view each grating position and the
observer could judge the child’s detection of the grating. Such
modifications minimize the effects of visual field defects and
eye movement abnormalities. The stimuli were 12.5-cm squares
of high-contrast (83%), black-and-white square-wave gratings (range, 0.23-26.0 cycles/cm, in approximately 0.5-octave
steps) on rectangular cards. The gratings had the same spaceaveraged luminance as the background of the gray cards. The
luminance of the cards was at least 10 candela (cd)/m2. The tester,
unaware of the right-left position of the stripes, presented the
cards at a distance of 38 to 55 cm from the patient. Based on
the patient’s looking behavior, the tester judged the finest grating that the child detected. This was taken as the acuity, expressed in cycles per degree (cpd). The patient’s acuities were
compared with normal binocular PL acuity for age.19 Although test-retest reliability is poorer in infants with an abnor-
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Table 2. Ophthalmic Features
Patient No.
Age at First Visual Acuity, mo
Nystagmus
Strabismus
Mild Optic Atrophy
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
6
7
8
8
9
10
11
12
14
15
16
21
24
24
26
28
29
30
36
No
Yes
Yes
Yes
No
Yes
No
No
No
No
No
No
No
No
No
No
No
No
No
XT
XT
XT
XT, hypertropia
E(T), X(T)
ET
ET, hypertropia
XT
XT
XT
E(T)
None
XT
X(T)
XT
E(T)
None
E(T)
XT
No
No
Yes
No
No
Yes
No
No
No
Yes
No
No
Yes
Yes
No
No
Yes
Yes
No
Abbreviations: ET, esotropia; E(T), intermittent esotropia; XT, exotropia; X(T), intermittent exotropia.
Sweep VEPs were recorded using the NUDiva system (SmithKettlewell, San Francisco, Calif ).7,23,24 The spatial frequency of
a high-contrast (80%) vertical square-wave grating (average luminance, 76 cd/m2) alternating at 5.5 Hz (11 reversals per second) was swept from low to high spatial frequency during a
10-second trial. To accommodate the large range of acuities,
the test distances were 50 to 150 cm. This provides nominal
test fields of approximately 42°⫻32° to 14°⫻11°. Thus, because the VEP represents the function of the central 5° to 8°
of the field,10 all subjects received adequate macular stimulation. Electrodes were placed 3 cm above the inion (Oz) and 3
cm to the left (O1) and right (O2), with a reference electrode at
the vertex and a ground electrode on the forehead. The electroencephalogram was amplified (Grass P10 preamplifier
[Astro-Med, Inc, West Warwick, RI]; gain, 20 000; bandpass,
1-100 Hz) and monitored continuously during the session.
The average of 5 or more sweeps was used. Acuity was estimated by linear extrapolation to estimate the spatial frequency
that produced a zero microvolt VEP. For VEP acuity, testretest agreement is somewhat lower in children with CVI than
in healthy children.7,25 For the present sample, VEP thresholds
were within 0.5 octave in 8 of 10 patients who had repeated
measures within 6 months.
64
16
Visual Acuity, cpd
VEP Procedure
A
4
1
0.25
0.0625
B
64
16
Visual Acuity, cpd
mal perinatal history20 or developmental delay,21,22 reliability
was clinically acceptable for the present sample. For the sample
reported herein, between- and within-tester variations were no
greater than 1 card interval (0.5 octave) in most of the patients.
4
1
0.25
0.0625
0
1
2
ANALYSIS OF LONGITUDINAL DATA
Visual acuity (log2 cpd, ie, an octave scale) was plotted as a function of age and compared with the normal course of development. An octave indicates a doubling of spatial frequency; in
Snellen nomenclature, an improvement from 20/80 to 20/40,
for example, is an improvement of an octave.
Normal PL and VEP acuity increases rapidly from birth to
6 months of age (Figure 1) and then more gradually there-
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1217
3
4
5
6
Age, y
Figure 1. All visual acuity measurements in our patients. A, Preferential looking
(PL) values; B, Visual evoked potential (VEP) values. Serial measurements in an
individual are connected by lines. The 95% prediction intervals for normal PL
and VEP acuities are indicated by the dotted and dashed lines, respectively. The
ordinates are a log base 2 scale; cpd indicates cycles per degree.
after.10 Courage and Adams19 reported that during normal development from 6 months to 3 years of age, average binocular
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32 Patient 1
Patient 3
Patient 4
Patient 8
Patient 9
Patient 14
Patient 15
Visual Acuity, cpd
16
8
4
2
1
0.5
0.25
0.125
32 Patient 5
Visual Acuity, cpd
16
8
4
2
1
0.5
0.25
0.125
32 Patient 12
Visual Acuity, cpd
16
8
4
2
1
0.5
0.25
0.125
0
1
2
3
4
5
6
0
1
Age, y
2
3
4
5
6
0
1
Age, y
2
3
4
5
6
Age, y
Figure 2. The courses of the patients who had 4 or more measurements of both preferential looking (PL) and visual evoked potential (VEP) acuities. The lower
limits of the normal interval for PL and VEP acuities are indicated by the dotted and dashed lines, respectively. The patients are described in Table 1. The ordinates
are a log base 2 scale; cpd indicates cycles per degree.
PL acuity increased 1.66 octaves from 5.9 to 18.6 cpd, or, on
average, 0.66 octave/y. Mayer and colleagues26 reported that in
healthy children aged 6 through 48 months, monocular PL acuity increased 2.12 octaves from 5.7 to 24.8 cpd, or 0.61 octave/y. Birch27 found that from 6 to 18 months of age, average
normal binocular VEP acuity increased from 12.82 to 18.27 cpd,
or 0.51 octave/y. An acuity of 18.27 cpd is only 0.19 octave less
than the mean normal VEP acuity in adults tested in our laboratory (20.91 cpd; n=11).
For all 19 patients, the first and last acuities were compared and expressed as octave change per year. For those 9 patients who had 4 or more sessions at which both PL and VEP
acuities were measured, the rate of change in acuity per year
was determined by linear regression.
RESULTS
All PL and VEP acuities of the 19 patients are plotted as
a function of age in Figure 1. Nearly all visual acuities
were below normal for age. Individual children underwent 2 to 16 measurements (median, 8 measurements)
of PL acuity and 1 to 7 measurements (median, 4 measurements) of VEP acuity.
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1218
Inspection of the course of PL acuity development in
each child (n=19) shows that between the first and last
measurement, acuity improved 1 octave on average (range,
−2.1 to 5.0 octaves). One octave is often considered a clinically significant change. Three patients had a decrease
in PL acuity. Two of the 3 (patients 2 and 13) had decreases of more than 1 octave in PL acuity; both had intractable seizures. In the third patient (patient 1), the
decrease was only 0.5 octave. The median period of observation was 2.7 years (range, 6 months to 6 years), and
for individuals the average rate of change in PL acuity
per year was ⫹0.18 octave/y (range, −0.90 to ⫹1.80 octaves/y). The final PL acuity was related to the neurological score (Spearman ␳=−0.70; P⬍.001); the more favorable the score, the better the acuity. The rate of change
in PL acuity was independent of the neurological score.
Improvement in VEP acuity (Figure 1) was also on average 1 octave (range, −0.22 to 3.09 octaves). During the
period of observation (median, 2 years; range, 6 months
to 6 years), the average rate of change in VEP acuity was
⫹0.41 octave/y (range, −0.34 to ⫹1.30 octaves/y). For individuals, the rate of change in VEP acuity did not differ
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COMMENT
All of these children with persistent CVI-like behaviors
had measurable visual acuity, although most remained
below normal. Furthermore, the typical developmental
course indicated a modest improvement in visual acuity, but at a slower rate than normal. Very few of the patients had a rate of improvement that was as fast as normal. On the other hand, only 2 with a seizure disorder
had substantial declines in acuity, and that was in their
PL but not their VEP acuity. Thus, the seizure disorder
may have interfered with the child’s looking behavior on
which the PL response depends.
In these young children with CVI, the overall improvement in PL and VEP acuities was about the same,
ie, 1 octave. Typically, in individuals, the rates of PL and
VEP improvement were similar, and in some of the patients with longitudinal data (Figure 2), the courses of
PL and VEP acuity were approximately parallel. In a few
patients (Figure 2), the course was suggestive of a delay
in development of visual responses. Visual acuity tests
at earlier ages would be informative about this matter.
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1219
32.0
16.0
8.0
4.0
VEP, cpd
significantly from that for PL acuity (paired t test, t13 =0.49;
P=.63). The rate of VEP acuity change and the final VEP
acuity were not related to the neurological score. Of note,
fewer VEP than PL test results were obtained, and the median period of observation for VEP tests was shorter than
that for the PL tests.
The courses of visual acuity in the 9 children with measures of both PL and VEP acuity at 4 or more ages are
plotted in Figure 2. As in normal development, VEP acuity was always better than PL acuity. For this subset of 9
children, as in the whole sample, most acuities were below normal, but some were not far below (patients 3, 5,
and 9). Only patient 14 had normal PL and VEP acuity.
Linear regression analysis indicates an average improvement in PL acuity of ⫹0.26 octave/y. The individual slopes
determined by linear regression (range, −0.05 to ⫹0.55
octave/y) were within the range of estimated rate of change
for the whole sample. The rate of increase in normal PL
acuity is more than ⫹0.60 octave/y.19,26 For VEP acuity,
linear regression indicated an improvement of ⫹0.25 octave/y (range, −0.10 to ⫹1.52 octave/y). Although 2 patients had substantial declines in PL acuity, none of the
VEP courses showed substantial decline.
All pairs of PL and VEP data obtained at the same session are shown in Figure 3. The range of PL acuity (6.0
octaves) was greater than that for VEP acuity (4.5 octaves). In almost every case, VEP acuity was better than
PL acuity. The magnitude of the disparity was not related to the neurological score. For more than half of the
points, the disparity between VEP and PL acuity exceeded an octave, with better VEP acuity. The discrepancy between PL and VEP acuity was greatest at lower
acuity levels, as previously reported by Orel-Bixler and
coworkers28 in patients with developmental disabilities
and by Good7 in children with CVI due to several different causes. Also, as found in the study by Orel-Bixler et
al,28 the age of our patients did not account for the larger
discrepancy at lower acuities.
2.0
1.0
0.50
0.25
0.25
0.50
1.0
2.0
4.0
8.0
16.0
32.0
PL, cpd
Figure 3. The relationship of preferential looking (PL) and visual evoked
potential (VEP) acuities. Every patient is represented, and individual patients
contribute 1 to 5 points. The diagonal lines have a slope of 1.0. Data would
lie on the solid line if PL and VEP acuity values were in perfect agreement.
The dashed lines are 1 octave above and below the solid line. The ordinate
and the abscissa are a log base 2 scale; cpd indicates cycles per degree.
In many of these children, the PL and VEP results
yielded a similar picture of visual development, with VEP
acuity better than PL acuity by approximately 1 octave,
as is the case in normal development (Figure 1 and
Figure 2). However, large discrepancies between PL and
VEP acuity occurred in more than half of the test sessions (Figure 3). The reasons for these discrepancies must
lie in differences between PL and VEP procedures and
in abnormal processes in the brain with a history of diffuse injury. Unlike the VEP response, the PL response
requires other systems, such as the ocular motor system, and attention.
The luminous stimulus field and the apparent motion of the swept gratings distinguish the VEP from the
static black-and-white stripes on the PL cards and could
conceivably be more salient to the child with CVI. Differences in PL and VEP acuity are incompletely explained by differences in stimulus variables.29 Imprecise
retinotopic mapping might be postulated as the basis for
the larger VEP stimulus field producing much better VEP
than PL acuity in some of our patients (Figure 3). Other
potential explanations for substantially better VEP than
PL acuity in some patients are the larger number of trials
inherent in the sweep VEP than in the PL procedure and
different scoring of PL and VEP responses.28,29
In instances where PL and VEP measures give parallel information about visual development, both tests are
not needed. Our experience suggests that the VEP acuity test gives little additional information in children who
have PL acuities within 1 octave of normal for age, who
have a PL acuity of 4 cpd or better, or who during the
PL test have consistent, repeatable responses. For such
children, we find ourselves comfortably relying on the
fast and relatively inexpensive PL test alone. Children who
are difficult to engage, make only fleeting eye contact, if
that, and have a PL acuity of 4 cpd or less are likely to
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have much better VEP acuity. For such visually inattentive children, we find that the VEP provides a reliable measure of acuity, but acuity may be astonishingly good for
the child’s level of visual behavior. Thus, although clinicians find acuity a familiar measure, more specific tests
of visual cortical function and attention13,14 warrant consideration for valid assessment of vision in children such
as those included in this study.
11.
12.
13.
14.
Submitted for Publication: March 30, 2004; final revision received December 15, 2004; accepted January 13,
2005.
Correspondence: Anne B. Fulton, MD, Department of
Ophthalmology, Children’s Hospital and Harvard Medical School, 300 Longwood Ave, Boston, MA 02115 (Anne
[email protected]).
Financial Disclosure: None.
Funding/Support: This study was supported in part by
grants from the Blind Children Center, Los Angeles, Calif,
and United Cerebral Palsy Foundation, Washington, DC.
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