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Screening amblyopia for year 1 students with uncorrected
vision and stereopsis test in central China
FU Jing,1 Li Shi-ming,1 Li Jin-ling, 2 Li Si-yuan,1 Liu Luo-ru,2 Wang Yang,1
Li He,2 Zhu Bi-dan,3 Ji Ya-zhou, 2 Yang Zhou,1 Li Lei,1 Chen Wei2 and
Wang Ning-li,1 and the Anyang Childhood Eye Study Group
1
Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University;
Beijing Ophthalmology and Visual Science Key Lab, Beijing, China
2
Anyang Eye Hospital, Henan Province, China
3
Department of Ophthalmology, the Second Hospital affiliated to Harbin Medical
University
Correspondence: Ning-Li Wang, Beijing Tongren Eye Center, Beijing Tongren
Hospital,
Capital
Medical
University,
Beijing,
China,
100730;
Email:
[email protected], Fax: 010-58269920, Tel: 010-58269920
Conflicts of interest: none for all authors
Number of Figures: 1
Number of Tables: 6
Word counts: Abstract: 300, Text: 2727 (excluding abstract, references and tables)
Key Words: amblyopia; vision screening; visual acuity; steropsis test
Background: Screening for amblyopia at earliest is important for early treatment and
better prognosis. This study aimed at evaluating the validity of uncorrected distant
and near visual acuity and stereoacuity for screening amblyopia in year 1 students in
central China.
Methods: By stratified cluster sampling, 3112 year 1 students from 11 Anyang
primary schools were selected for the study. All the participants underwent
uncorrected distant and near visual acuity, stereopsis test, cycloplegic refraction, best
corrected visual acuity (BCVA), cover test and ocular movement examination. Visual
acuity (VA) was measured with a logarithm of the minimum angle of resolution
(logMAR) chart. Stereoacuity was measured with the Lang II stereo card and TNO
test. Amblyopia was defined as the BCVA less than or equal to 0.1 logMAR units of
any eye in the absence of significant pathological abnormalities. The sensitivity,
specificity, positive predictive value and negative predictive value of uncorrected
visual acuity and stereoacuity for amblyopia were analyzed.
Results: Out of the 3112 eligible students, 2893 (92.96%) students completed the
examinations. The average age of the students was 7.10±0.41 （mean ± standard
deviation, SD）years. Screened by distant visual acuity with low cutoff (logMAR0.1),
high cutoff (logMAR0.0) and near visual acuity (logMAR0.0), 31.64, 73.18 and
50.23% students were abnormal. Screened by stereopsis test, only 4.69% students
were abnormal. By a senior pediatric ophthalmologist, 61 students were diagnosed
amblyopia. The sensitivities of distant visual acuity with low/high cutoff and near
visual acuity were 92.31/100.00 and 80.77%, whereas that of stereoacuity by TNO
test was 15.38%. Simultaneous testing of either two of the three tests improved the
sensitivity.
Conclusions: Distant visual acuity test of high cutoff alone display a high sensitivity
but a low specificity. Simultaneous testing of distant visual acuity of low cutoff and
stereoacuity is a better choice to balance between sensitivity and specificity.
Optimising the probability of early detection of eye disorders in children is crucial for
successful clinical mamagement.1 Amblyopia is decrease of vision caused by
strabismus, anisometropia, media opacity, and significant refractive errors, such as
high hyperopia, astigmatism, myopia. Global estimates of the prevalence of
amblyopia2-18 in preschool and school populations are different, ranging from 0.18%
to 4.7%. Screening and treatment for amblyopia at an early age, when it is a sensitive
period of visual development, lead to a better visual outcome.19-21 However, screening
for amblyopia is sometimes unsatisfactory because of the lack of a reliable single test
for vision assessment,22 an adequate quality of screening,23 and standardized
conditions.24
Screening for amblyopia with standardized refractive methods is costly and
labour-intensive. Traditional vision test, such as visual acuity and stereoacuity, is a
direct and cheaper method than advanced diagnostic refractive methods. And
traditional vision test is easier to train general health worker and apply to children,
which might be conveniently used for amblyopia screening. However, it's specificity
and sensitivity, especially the specificity which is crucial for screening, is to be
determined.
The purpose of this study is to examine the validity of uncorrected distant and near
visual acuity and stereoacuity to screen amblyopia in year 1 students. The data of the
study came from year 1 students of Anyang Childhood Eye Study (ACES).
MATERIAL AND METHODS
Populations
The Anyang Childhood Eye Study is a school-based survey of refractive error,
amblyopia, strabismus and other eye conditions in a sample of year 1 and year 7
students in Anyang, Henan province, central China. A description in detail of Anyang
Childhood Eye Study Protocol was recently described in design and methodology
paper of our group (submitted to Ophthalmic Epidemiology, under review). The study
adhered to the Declaration of Helsinki, ethics approval was obtained from the Beijing
Tongren Hospital Ethical Committee and written informed consent was obtained from
all participants’ parents or legal guardians. Stratified cluster sampling was used in the
ACES. All primary and junior high schools in Anyang city were stratified into three
levels based on the quality evaluation of local government. Finally, 3112 Year
1students of 11 primary schools and 2363 Year 7students of 4 junior high schools
were randomly sampled, respectively. The following report is based on data from the
year 1 students examined from February to May 2011. The examination procedure for
current population is similar with Australia Pediatric Eye Study17, 18, described in
detail as following.
Procedures
Distant Visual Acuity: All students were measured for their distant visual acuity
without and with spectacles, if worn, using Logarithmic Visual Acuity Chart
(Precision Vision, La Salle, IL, USA) at a distance of 4 meters. The chart was
retroilluminated and has 70 tumbling “E” optotypes with 5 letters on each line. The
students were examined monocularly (right eye followed by the left eye) and the
procedure in detail has been described elsewhere.25 For the students with distant
visual acuity less than 1.0 (logMAR0), subjective refraction will be performed to
obtain their best corrected visual acuity.
Near visual acuity: A LogMAR HOTV chart was used to test the students’ near visual
acuity at 40 cm. For those children, for example, the Year 1 students who can’t
recognize the letters well, an ancillary chart with four large letters of HOTV was used
to point out the observation.
Stereopsis test: In the ACES, the Lang II stereo card (Lang-stereotest, Forch,
Switzerland) was used to qualitatively screen the students with binocular dysfunction
at 40 cm26. TNO test (Lam´eris Ootech BV Nieuwegian, The Netherlands) was used
to quantitatively measure the degree of stereoacuity (retinal disparities ranging from
15 to 480 seconds of arc) for students at a distance of 40 cm.
Ocular Examination: All the students also had a comprehensive eye examination,
which included Cycloplegic Autorefraction, Ocular Motility (including cover test,
cover-uncover test et al.), color vision assessment, ocular biometry, slitlamp
examination, and optical coherence tomography. Digital retinal photographs were
taken and assessed to exclude retinal pathological abnormalities.
Definitions
Two Cutoffs points of abnormal uncorrected distance visual acuity were defined. The
high and low cutoff of abnormal uncorrected distant visual acuity in one eye or both
were less than 1.0 (logMAR 0) and 0.8 (logMAR 0.1), respectively. Students with
uncorrected near visual acuity in one eye or both less than 1.0 (logMAR 0) were
considered abnormal.27
TNO test was used to quantitatively measure the degree of stereoacuity. Stereoacuity
worse than 60 sec-arc was abnormal.
The visual acuity and stereoacuity were performed by trained health workers. The
final examination was performed by ophthalmologists and optometrists. The final eye
examination included cover test, cover-uncover test, cycloplegic refractions, slitlamp
examination, retinal photographs, and corrected visual acuity.
In this study, amblyopia was defined as best corrected visual acuity (BCVA) less than
1.0(logMAR0) in one or both eyes in absence of significant pathological
abnormalities.27, 28 All the students were examined by a pediatric ophthalmologist (FJ)
to evaluate risk factors of amblyopia, such as high refractive errors, anisometropia,
strabismus, and other ocular abnormalities.
For each criterion, we determined sensitivity, specificity, positive predictive value
(PPV), and negative predictive value (NPV) using standard analytical methods (Table
1).27 Sensitivity is the probability that the screening test will be positive when an
abnormality is present. Specificity indicated the probability that the screening test will
be negative when an abnormality is not present. The PPV indicates the probability of
an abnormality being present if the screening test is positive. The NPV indicates the
probability of normality if the screening test provides a normal result.
Statistical Analysis
All the data were independently input into a database using Epidata software 3.1 by
two individuals. All of Statistical analyses were performed using Statistical Analysis
System Software [SAS version 9.1.3 software (SAS Institute, Inc, Cary, NC)]. Where
cluster effects were not significant, X2 tests and t tests were used.
RESULTS
Subject
Of 3112 eligible year 1 students, 2893 (response rate 92.96%, 2893/3112) students
were given parental permission to participate and questionnaire data were provided by
parents. All the participants were examined and completed at least one test at the
health examination station. Uncorrected distant visual acuity measurements were
available for 2886 (92.74%, 2886/3112) students. Uncorrected near visual acuity were
available for 2859 (91.87%, 2859/3112) students. Stereoacuity (TNO test) were
available for 2860 (91.90%, 2860/3112) students. Close to 91.77% (2856/3112) of the
students took all the three screening tests. The mean age of participants was 7.10±0.41
years (range, 5.67-9.27 years); 42.18% of the students were girls and 57.82% were
boys. In this sample, 120 students (4.15%, 120/2893) were 6 years old, and 2383
students (82.37%, 2383/2893) were 7 years old.
Rates of Failing Screen Test
Screened by uncorrected distance visual acuity with a low cutoff, 913 (31.64%,
913/2886) students failed to pass the test, whereas screened by uncorrected distance
visual acuity with a high cutoff, 2212 (73.18%, 2212/2886) students failed. Screened
by near visual acuity, 1436 (50.23%, 1436/2859) students failed (Figure 1). Screened
by TNO stereoacuity test, 134 (4.69%, 134/2860) students
failed. The
above-mentioned proportion of students did not include those who did not perform the
test.
Prevalence and Causes of Amblyopia
Amblyopia was diagnosed in 61 students (2.16%, 61/2819, 95% confidence interval
[CI], 1.63-2.70) by a pediatric ophthalmologist (FJ) (Table 2). There was no
significant difference in amblyopia prevalence between the boys and the girls
(P=0.7820). Of the 61 students with amblyopia, 30 students (49.18%) had unilateral
amblyopia and 31 students (50.82%) had bilateral amblyopia. Of the 30 patients with
unilateral amblyopia, 17 students had anisometropia (anisometropic hyperopia ≧1.0D,
anisometropic myopia ≧3D , anisometropic astigmatism ≧1.5D; for 1 students
associated with stimulus deprivation, 1 with nystagmus, and 2 with strabismus), 5
strabismus (2 students associated with anisometropia), and 10 students had no
amblyopia related risk factors. Of the 31 patients with bilateral amblyopia, 11 had
significant refractive error such as hyperopia (SE)≧4.0D, myopia (SE)≦-6.0D or
astigmatism≧2.5D, 1 stimulus deprivation, 2 nystagmus and 17 students had no
amblyopia related risk factors. In total, twenty-seven students (44.26%, 27/61) who
met the visual acuity criteria (either unilateral or bilateral) didn’t have amblyogenic
risk factors.
Validity of Screen Test for Amblyopia
In order to evaluate validity of each test or simultaneous testing, the sensitivities,
specificities, PPV, and NPV were calculated and listed in Table 3. The sensitivity of
TNO test was low at 15.38%, whereas that of the near visual acuity was 80.77%. The
best one was the distance visual acuity with high cutoff, 100%; however, its
specificity was low at 22.74%. If the low cutoff of the distance visual acuity was
adopted, the sensitivity drop to 92.31%, but the specificity improved to 68.70%. The
PPV also improved from 2.42 to 5.36%.
Furthermore, the sensitivity, specificity, PPV, and NPV of the simultaneous testing of
distance visual acuity, near visual acuity, and stereoacuity (TNO) were calculated. The
result of simultaneously performing two tests was considered positive if either of the
two tests was positive. Simultaneous testing with stereoauity (TNO) and near visual
acuity only improved the sensitivity to 82.69% with a specificity of 47.91% and a
PPV of 2.96%. The simultaneous testing of stereoacuity (TNO) and distance visual
acuity with a low cutoff increased the sensitivity to 94.23%. The specificity and PPV
were 66.04 and 5.06%. In the simultaneous testing of stereoacuity (TNO) and distance
visual acuity with a high cutoff, the sensitivity improved to 100% and the specificity
was 21.82%, whereas PPV was 2.40%.
The highest sensitivity was achieved by simultaneous testing of distance visual acuity
(high cutoff) and near visual acuity test, or simultaneous testing of distance visual
acuity (high cutoff) and stereoacuity, both 100%; however, its specificity and PPV
were as low as 15.47% and 2.22%, 21.82% and 2.40%, respectively. Whereas, the
simultaneous testing of distance visual acuity (low cutoff) and near visual acuity
showed a sensitivity of 96.15%, specificity of 39.28%, and PPV of 2.95%.
Stereoacuity (TNO) and Uncorrected Near Visual Acuity, Strabismus
and Anisometropia in Amblyopia Students
The relationship between stereoacuity (TNO) and near visual acuity was examined
(Table 4). 61 amblyopic students had both tests of near visual acuity and stereoacuity
(TNO) successfully performed. Of those students whose near visual acuity were
below 0.3, 80.95% passed stereoacuity (TNO). With a near vision between 0.4 and 0.6,
50% students passed stereoacuity (TNO). With a near vision more than 0.7, 83.33%
students passed stereoacuity (TNO).
The relationship between stereoacuity (TNO) and strabismus was examined (Table 5).
61 amblyopic students had both tests of cover test, ocular motility and stereoacuity
(TNO) successfully performed. Of these students with strabismus, 75.00% passed
stereoacuity (TNO). Without strabismus, 83.33% students passed stereoacuity (TNO).
The relationship between stereoacuity (TNO) and anisometropia was examined
(Table 6). 61 amblyopic students had both tests of cycloplegic refraction and
stereoacuity (TNO) successfully performed. Of these students with anisometropia,
75.00% passed stereoacuity (TNO). Without anisometropia, 82.00% students passed
stereoacuity (TNO).
DISCUSSION
The data of the study came from year 1 students of Anyang Childhood Eye Study
(ACES). All the participants underwent comprehensive eye examinations. The main
purpose of ACES was not to screen out amblyopia, but rather to find a easy way for
amblyopia screening via data analysis. This study analyses the effectiveness of
uncorrected distant visual acuity, near visual acuity and stereopsis for screening
amblyopia. The result could be used as a reference for screening amblyopia in
preschool children.
The ideal screening test has high sensitivity and high specificity. But it is not always
feasible. In screening for amblyopia, a high sensitivity is required, because any
children should not be missed and delayed for treatment. Of the three tests in this
study, sensitivity of detecting amblyopia varies widely, from around 15.38% of
stereoacuity by TNO test to 100% of distant visual acuity test with high cutoff.
However, the limitation of the latter is its specificity is lower than 25% and PPV
around 2.5%. With such a low specificity and PPV, many children screened out would
require further evaluation by ophthalmologists. Additional time and cost will be
needed for a final diagnosis.
The low PPV of screening for amblyopia was not caused by high number of false
positive, as the specificities of most screening methods in this study were around
50-80%. Instead, low prevalence of amblyopia2-18 in the general population, from
0.18% to 4.7%, is the main cause of low PPV. Specificity can be influenced by
prevalence. When a diagnosis method with a high specificity is used to screen for a
disease in a very low prevalence population, the positive results will contain relatively
a large number of false positive patients, which reduces the positive predictive value
(PPV). Since the prevalence of amblyopia is low, unless both sensitivity and
specificity are close to 100%, PPV is not easy to be high in such a low prevalence
disease.
Simultaneous performing two tests will increase the sensitivity if either of them
showing positive is considered positive. Simultaneous testing of distant visual acuity
of high cutoff and other tests increases sensitivity to 100%, but its limitation is
specificity less than 25%. Simultaneous testing of distant visual acuity of low cutoff
and other tests increases sensitivity to around 95%, and it reserves a specificity of
40% for combining distant VA of low cutoff and near VA, 65% for combining distant
VA of low cutoff and stereoacuity by TNO. Simultaneous testing of near visual acuity
and stereoacuity (TNO), sensitivity and specificity are similar to near visual acuity
test alone. So simultaneous testing of distant VA of low cutoff and stereoacuity is a
better choice to balance between sensitivity and specificity.
In this study, screening amblyopia by stereopsis test, its sensitivity was low, around
15%. Around 80% amblyopia students with near visual acuity equal to or lower than
0.3 pass the TNO test. Around 75.00% amblyopia students with strabismus pass the
TNO test, and 82.00% amblyopia students without strabismus pass the TNO test .
Around 69.57% amblyopia students with anisometropia pass the TNO test, 86.84%
amblyopia students without anisometropia pass the TNO test. Of 61 amblyopia
students, 12 (19.67%) had strabismus, 23 (37.70%) had anisometropia. Schmidt et al.
reported that the sensitivity of Random Dot E stereoacuity and Stereo Smile II
stereoacuity was 28 and 61% in detecting amblyopia.29 Thus, stereopsis test alone is
not sensitive enough for amblyopia. However, Visual screening for children is not
only to detect amblyopia but also to find strabismus, which is most effectively
detected by stereopsis test and cover test. A combination of visual acuity test and
stereopsis test is cost-effective to increase the sensitivity to detect amblyopia and
strabismus simultaneously.
The sensitivity of distant visual acuity of high/low cutoff was 100/92.31%. The
distant visual acuity test has a high sensitivity for amblyopia patients because these
amblyopic eyes always have an abnormal uncorrected distant visual acuity. However,
the specificity of distant visual acuity is low, so the rate of misdiagnosis will high
when it is used to screen amblyopia. This will bring subsequently consumption of
additional time and money to confirm amblyopia diagnosis. Near visual acuity is a
screening test easy to perform, however, its sensitivity was 80.77% in this study,
lower than distant visual acuity.
The ideal screening tests should be inexpensive, easy, and time saving to perform both
for the examiner and the children. The distant/near visual acuity test and stereopsis
test are much cheaper and easier to do than photoscreening methods. It is also more
cost-effective to be performed by the community health workers. In Chang et al study,
around 20-30% of 3-year-old children was not able to perform visual acuity and
stereopsis test, but the number decreased after age 3 years.27 Treatment of amblyopia
should be started as early as possible, because younger age of initial treatment has
been proved to be associated with better treatment outcomes.20, 30 If 70% of 3-year-old
children knows how to do the test, it is worthwhile to screen these children.27 Since
visual acuity of children is still under development naturally, different visual acuity
cutoff should be adopted for different age groups.
The earlier detection and treatment of amblyopia leads to a better vision prognosis, so
it becomes particularly important for amblyopia screening. As screening is mainly
carried out in community health service centers, training of community health
workers is very important. Community health workers play a very important role in
screening work for amblyopia and the traditional vision screen method is more
appropriate for them. The quality of the screening on one hand depends on the
socio-economic situation, but even more on training and devotion of the screening
performers on the other hand. So community health workers need more training in
order to increase the validity of the screening test.
ACKNOWLEDGMENTS
The ACES was supported by the Major State Basic Research Development Program
of China (‘‘973’’ Program, 2011CB504601) of the Ministry of Science and
Technology, the Major International (Regional) Joint Research Project (81120108807)
of the National Natural Science Foundation of China, partially from China
Postdoctoral Science Foundation (20110490247) and Research Foundation of Beijing
Tongren Hospital Affiliated to Capital Medical University (2012-YJJ-019). The
authors thank the supports from the Anyang city government for helping organize the
survey.
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Table 1 Definition of analytical measures
Screening result
Final ophthalmologists examination results (amblyopia)
Abnormal
Normal
Abnormal
A
B
Normal
C
D
Sensitivity=A/(A+C); specificity=D/(B+D); positive predictive value=A/(A+B); negative predictive
value=D/(C+D); n number of eyes examined=(A+B+C+D).
Table 2 Causes of amblyopia
Causes
N
Anisometropia*
17
Strabismus†
5
Significant refractive errors
11
Stimulus deprivation
2
Nystagmus
3
Unclear
27
Total
61
* 1 students associated with stimulus deprivation, 1 with nystagmus, 2 with strabismus
† 2 students associated with anisometropia,
Table 3 Validity of different methods of screening
Sensitivity(%)
Specificity(%)
Distance visual acuity (low cutoff)
92.31
68.70
5.36
99.79
Distance visual acuity (high cutoff)
100.00
22.74
2.42
100.00
Near visual acuity
80.77
49.61
2.99
99.26
Stereoacuity (TNO)
15.38
95.72
6.45
98.33
Distance visual acuity (low cutoff) and near visual acuity
96.15
39.28
2.95
99.81
Distance visual acuity (high cutoff) and near visual acuity
100.00
15.47
2.22
100.00
Distance visual acuity (low cutoff) and stereoacuity (TNO)
94.23
66.04
5.06
99.83
Distance visual acuity (high cutoff) and stereoacuity (TNO)
100.00
21.82
2.40
100.00
2.96
99.31
Near visual acuity and stereoacuity (TNO)
82.69
NPV=negative predictive value; PPV=positive predictive value
47.91
PPV (%)
NPV (%)
Table 4 Relationship of stereoacuity (TNO) and uncorrected near visual acuity in amblyopia students
Stereoacuity
Near visual acuity, N (%)
≤0.3
0.4-0.6
logMAR≥0.52
logMAR0.15-0.52 logMAR≤0.15
Normal
17 (80.95%)
2 (50.00%)
30 (83.33%)
49
Abnormal
4 (19.05%)
2 (50.00%)
6 (16.67%)
11
Total
21
4
36
61
(TNO)
≥0.7
Total
Table 5 Relationship of stereoacuity (TNO) and with/without strabismus in amblyopia students
Stereoacuity
(TNO)
Strabismus, N (%)
With
Without
Total
Normal
9 (75.00%)
41 (82.00%)
50
Abnormal
3 (25.00%)
9 (18.00%)
11
Total
12
49
61
Table 6 Relationship of stereoacuity (TNO) and with/without anisometropia in amblyopia students
Stereoacuity
(TNO)
Anisometropia, N (%)
With
Without
Total
Normal
16 (69.57%)
33 (86.84%)
49
Abnormal
7 (30.43%)
5 (13.36%)
12
Total
17
44
61
100.00
90.00
80.00
70.00
60.00
50.00
40.00
30.00
20.00
10.00
0.00
Abnormal
Normal
Distant vision Distant vision
(low cut-off) (high cut-off)
Near vision
stereoacuity
Figure 1 Performance of distant vision (low cut-off), distant vision (high cut-off), near vision,
stereoacuity in year 1 students.