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Ophthalmic Epidemiology, 2014; 21(3): 197–203
!Informa Healthcare USA, Inc.
ISSN: 0928-6586 print / 1744-5086 online
DOI: 10.3109/09286586.2014.904371
ORIGINAL ARTICLE
Prevalence of Amblyopia and Strabismus in a
Population of 7th-Grade Junior High School Students
in Central China: The Anyang Childhood Eye Study
(ACES)
Jing Fu
1
, Shi Ming Li
1
, Luo Ru Liu
2
, Jin Ling Li
2
, Si Yuan Li
1
, Bi Dan Zhu
3
,HeLi
2
,
Zhou Yang
1
, Lei Li
1
, Ning Li Wang
1
and the Anyang Childhood Eye Study Group
1
Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University; Beijing Ophthalmology &
Visual Sciences Key Lab, Beijing, China,
2
Anyang Eye Hospital, Henan Province, China, and
3
Department of
Ophthalmology, the Second Hospital affiliated to Harbin Medical University, Heilongjiang Province, China
ABSTRACT
Purpose: To determine the prevalence of amblyopia and strabismus in 7th-grade junior high school students in
central China.
Methods: Using stratified cluster sampling, 2363 7th-grade students were recruited from four junior high schools
in Anyang city into the cross-sectional Anyang Childhood Eye Study (ACES). All students underwent visual
acuity (VA), cycloplegic autorefraction, cover test, and ocular movement examinations. Uncorrected VA and
best-corrected VA (BCVA) were measured with a logarithm of the minimum angle of resolution (logMAR)
chart. Cycloplegic autorefraction was performed after administration of 1.0% cyclopentolate and Mydrin-P.
Strabismus was defined as heterotropia at near or distance fixation. Amblyopia was defined as BCVA0.1
logMAR units in one or both eyes, without ocular pathology in either eye.
Results: Of the 2363 eligible students, 2260 (95.6%) completed all examinations. The mean age of the students
was 12.4 ± 0.6 years. Amblyopia was present in 52 students (2.5%), of whom 33 (63.5%) had unilateral and
19 (36.6%) had bilateral amblyopia. Of those with unilateral amblyopia, 18 (54.5 %) had anisometropia and
7 (21.2%) had strabismus. Of those with bilateral amblyopia, 6 (31.6%) had significant refractive error.
Strabismus was present in 108 students (5.0%), of whom 2 (1.9%) had esotropia, 102 (94.4%) had exotropia,
3 (2.8%) had vertical strabismus, and 1 (0.9%) had microstrabismus. Of the 108 students with strabismus,
9 (8.3%) had amblyopia.
Conclusion: The cross-sectional ACES which examined the prevalence of amblyopia and strabismus in 7th-grade
students in central China revealed the prevalence of strabismus, particularly the proportion of exotropia, to be
higher than previously reported.
Keywords: Amblyopia, children, epidemiology, prevalence, strabismus
INTRODUCTION
Amblyopia and strabismus are two of the most
common pediatric eye diseases, both of which can
lead not only to cosmetic impairment but also to grave
functional sequelae. The negative effects of both of
these childhood-onset visual developmental disorders
frequently persist into adulthood.
Amblyopia manifests as a unilateral or bilateral
reduction of best-corrected visual acuity (BCVA). It is
a condition in which no ocular pathologies are
detectable on physical ophthalmological examination
and, in appropriate cases, is reversible by therapeutic
measures.
1
Early detection and early initiation of
treatment is widely accepted as being necessary to
improve visual acuity (VA) outcomes for children
Correspondence: Ningli Wang, MD, PhD, No. 1 Dongjiao Min Xiang, Dongcheng District, Beijing, China, 100730. Tel: +86 10 58269919. Fax: +86
10 58269920. E-mail: wningli@vip.163.com
Received 13 April 2013; Revised 1 February 2014; Accepted 2 February 2014; Published online 16 April 2014
197
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with amblyopia. Moreover, younger age of the patient
at initial treatment has been proven to be associated
with better treatment outcomes.
2,3
Patients with
amblyopia are at great risk of bilateral blindness, a
condition typically resulting from traumatic eye
injury in young people and age-related macular
degeneration in older persons.
4
Strabismus, a condition in which the eyes are
improperly aligned, can result in loss of binocularity
and depth perception if left untreated.
5
It is a
common cause of amblyopia
6
and has significant
psychosocial consequences.
7,8
The condition can be
treated successfully by surgery, thus averting ambly-
opia as well as improving psychosocial health,
especially if treated at an early age, e.g. the early
teenage years.
Estimates of the prevalence of amblyopia and
strabismus have been based largely on results of a
number of population- and school-based studies.
9–27
Global estimates of the prevalence of ambly-
opia
9–17,20–29
and strabismus
9–13,15–25
in pre-school/
school-age populations differ, ranging from 0.2–4.7%
for amblyopia and 0.4–3.3% for strabismus. Possible
reasons for such disparities include dissimilarities in
both study design and disease classification.
13–15,24,26
Although the importance of early detection and
treatment of various visual disorders in young
children is well-documented, there are relatively
few estimates of the prevalence of amblyopia and
strabismus in China, and none at all for central
China.
The purpose of this cross-sectional study was to
determine the prevalence of amblyopia and strabis-
mus in primary and junior high school students in
central China. This analysis is part of the Anyang
Childhood Eye Study (ACES).
MATERIALS AND METHODS
Patient Population
The ACES is a school-based survey of refractive error,
amblyopia, strabismus, and other abnormal ocular
conditions in a sample of 1st- and 7th-grade students
in Anyang, Henan province, central China. A detailed
description of the ACES protocol was recently pub-
lished.
28
The study adheres to the Declaration of
Helsinki and was approved by the Beijing Tongren
Hospital ethics committee. Written informed consent
was obtained from parents or legal representatives of
all participating students. Using a stratified cluster
sampling method, 2363 7th-grade students from four
secondary schools and 3112 1st-grade students from
11 primary schools in the city of Anyang were
recruited. Data presented here were collected from
7th-grade students examined between October 2011
and December 2011.
Procedures
Distance VA
All students had distance VA measured, with and
without spectacles, using a logarithm of the minimum
angle of resolution (LogMAR) visual acuity chart
(Precision Vision, La Salle, IL, USA) at a distance of
4 m. The chart was retro-illuminated and had 70
tumbling ‘‘E’’ optotypes, with five letters on each line.
Each eye was examined separately (the right eye
followed by the left eye), according to a detailed
procedure described elsewhere.
30
For students with
distance VA 50.0 logMAR units, subjective refraction
was performed to obtain BCVA.
Cycloplegic Autorefraction
The refractive status of all students was evaluated
before and after cycloplegia using an autorefractor
(HRK-7000A, Huvitz, Gunpo, South Korea). One drop
of the topical anesthetic Alcaine (Alcon
Pharmaceuticals, Puurs, Belgium) was first adminis-
tered to each eye to alleviate discomfort, followed by
two drops of 1.0% cyclopentolate (Cyclogyl, Alcon
Pharmaceuticals) and 1 drop of Mydrin-P (Santen
Pharmaceuticals, Osaka, Japan) at 5 minute intervals.
Thirty minutes after the drop of Mydrin-P, a third
drop of cyclopentolate was administered if the pupil-
lary light reflex was still present or if pupil size was
56.0 mm. Three consecutive readings of sphero-cylin-
drical autorefraction were averaged.
31
Spherical
equivalent (SEq) was calculated as the sum of the
spherical plus half of the cylindrical power. Myopia,
high myopia, and hyperopia were defined as
SEq0.5 diopters (D), 6.0 D, and +0.5 D,
respectively, in one or both eyes. Astigmatism was
defined as cylindrical error 1.0 D.
Ocular Motility
Ocular alignment was assessed using the Hirschberg
light reflex, cover, and prism cover-uncover tests.
Cover tests were performed with fixation targets at
both distance (6 m) and near (33 cm).
11,18,32
The pres-
ence of strabismus and its characteristics (constant or
intermittent), type (exotropia, esotropia, hyper/hypo-
tropia, or dissociated vertical deviation), and size
(prism diopters) were also recorded.
Ocular Examination
All students had a comprehensive eye examination,
including stereopsis screening, color vision assess-
ment, ocular biometry, slit lamp examination, and
optical coherence tomography. Retinal photographs
were taken and assessed to exclude retinal anomalies
or pathologies.
Questionnaire
Parents were asked to complete a comprehensive
111-item questionnaire, including sociodemographic
198 J. Fu et al.
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information, e.g. nationality, city of birth, education,
occupation, and parental age. Data regarding each
student’s birth, medical history, and maternal obstet-
ric history were also obtained. In addition, the
questionnaire sought information regarding periods
during which the students usually engaged in close-
up and distance activities.
Definition of Amblyopia and Strabismus
Strabismus was defined as a heterotropia at near
and/or distance fixation. Micro-strabismus was
defined as a deviation of 510 prism diopters in the
presence of demonstrable binocular vision on the
Lang II test. In the absence of demonstrable binocular
vision, a deviation of this magnitude was classified
simply as strabismus.
Amblyopia was defined as BCVA 0.1 logMAR
units, (50 letters, equivalent to Snellen VA 54/5)
in one or both eyes in otherwise normal eyes, or with
ocular pathology that involved the eye/visual path-
ways, with reduction in VA not attributable only to
the ocular pathology.
33,34
Statistical Analysis
Prevalence was calculated as the ratio of the number
of individuals with any type of amblyopia or strabis-
mus to the total number of individuals evaluated.
All data were analyzed using version 3.1 Epidata
software (The EpiData Association, Odense,
Denmark) by two individuals, independently. All
statistical analyses were performed using SAS statis-
tical software version 9.1.3 (SAS Institute Inc, Cary,
NC, USA). Sex-specific prevalence estimates of ambly-
opia and strabismus were calculated and analyzed;
95% confidence intervals (CIs) of prevalence are
provided. When cluster effects were not significant,
2
and ttests were used.
RESULTS
Subjects
Of the 2363 eligible 7th-grade students, 2356 (99.7%)
were given parental permission to participate, with
questionnaire data provided. Of these 2356 students,
2260 were examined (95.6% response rate; 96 students
were absent during the week of the survey).
Compared with participants, non-participants did
not differ significantly in age (p= 0.06) or sex
(p= 0.25). Distance VA measures were available for
2221 students (98.3%). Autorefraction examinations
without cycloplegia were available for 2125 students
(94.3%), and with cycloplegia for 2117 students
(90.2%). Ocular motility data were available for 2151
students (91.3%). The mean age of participants was
12.4 ± 0.6 years (range 10–16 years); 789 students
(34.9%) were 12 years old and 1310 (58.0%) were 13
years old. Of the recruited students, 49.6% were
female and 50.4% male. None had any refractive
medium opacities or pathological retinal
abnormalities.
Prevalence of Amblyopia
Amblyopia was diagnosed in 52 students (2.5%),
including 11 with a previous history of amblyopia
(reported by their parents) and 41 who were newly
diagnosed during the examination. Of the 11 students
with a previous history of amblyopia, spectacles had
been prescribed for six students and occlusion treat-
ment for seven. There was no significant difference
in the prevalence of amblyopia between boys and
girls (p= 1.0). Of the 52 students with amblyopia, 33
(63.5%) were unilateral and 19 (36.5%) bilateral. Of
the 33 with unilateral amblyopia, 18 (54.6%) had
anisometropia, 7 (21.2%) had strabismus (3 were
associated with anisometropia and 2 with nystagmus)
and 8 (24.2%) had no amblyopia-related risk factors.
Of the 19 students with bilateral amblyopia, 6 (31.6%)
had significant refractive errors, e.g. hyperopia (SEq
4.0 D), myopia (SEq 6.0 D), or astigmatism
(SEq 2.5 D); 1 (5.3%) had nystagmus; and 12
(63.2%) had no amblyopia-related risk factors.
The distribution of BCVA in all amblyopic eyes is
shown in Figure 1. Mean-corrected VA was 0.2
logMAR, and the range was 1.0–0.1 logMAR. There
was no significant difference in mean-corrected VA
related to sex (p= 0.25).
Figure 2 illustrates the SEqs of refractive error for
all amblyopic eyes compared with non-amblyopic
eyes. The mean SEq refraction of amblyopic eyes was
0.4 D compared with a mean SEq of 1.5 D in non-
amblyopic eyes. Significant hyperopia (SEq +3.0 D)
was found in 21.2% of amblyopic eyes compared to
FIGURE 1. Distribution of best-corrected visual acuity (VA) in
71 amblyopic eyes and 4135 non-amblyopic eyes of students in
the Anyang Childhood Eye Study.
Prevalence of Amblyopia and Strabismus in China 199
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0.3% of non-amblyopic eyes; the difference was
statistically significant (p50.001).
The mean cylindrical refractive error was signifi-
cantly greater (p50.001) in amblyopic eyes (1.3 D)
than in non-amblyopic eyes (0.6 D; Figure 3).
The prevalence of anisometropia (SEq 1.5 D or
astigmatism 1.0 D) and astigmatism (2.5 D) in
students with amblyopia was 42.3% and 22.5%,
respectively, significantly higher than in subjects
without amblyopia; 10.4% (p50.001) and 1.2%
(p50.0001), respectively.
Prevalence of Strabismus
The overall prevalence of strabismus in 7th-grade
students was 5.0% (108 students), with an exotro-
pia:esotropia ratio of 51:1. There was no significant
difference in the prevalence of strabismus with regard
to sex (p = 0.66). Of the 108 students with strabismus,
37 (34.3%) had a previous history of strabismus,
whereas 71 (65.7%) were newly diagnosed.
The most frequent form of strabismus was inter-
mittent exotropia (77.8%), followed by constant
exotropia (16.7%), vertical deviation (2.8%), constant
esotropia (1.9%), and micro-strabismus (0.9%). Ten
cases (9.3%) of exotropia were noted in combination
with vertical deviation, and two of these had
dissociated vertical deviation. Six of the 18 (33.3%)
with constant exotropia had undergone previous
surgical correction (Table 1). Nine students (8.3%)
with strabismus also had amblyopia.
Students with strabismus were significantly more
myopic than those without strabismus (p50.0001),
with a mean SEq refraction of 2.4 D (95% CI 2.8 to
2.0 D) versus 1.5 D (95% CI 1.6 to 1.4 D). The
mean cyclindrical refraction of students with strabis-
mus (0.7 D) was significantly higher than for those
without strabismus (0.5 D; p= 0.002). The prevalence
of refractive errors, except hyperopia, in the right eye
was greater in students with strabismus than without
strabismus. A total of 90 students (83.3%) with
strabismus had myopia, 30 (27.8%) had astigmatism,
and 21 (19.4%) had anisometropia. Corresponding
rates in students without strabismus were 1480
(68.8%, p= 0.001), 440 (20.5%, p= 0.07), and 359
(16.7%, p= 0.45), respectively. The prevalence of
hyperopia (in right eyes) was lower in students with
strabismus (n= 9, 8.3%) than in those without (n= 334,
25.6%; p= 0.04). The prevalence of amblyopia was
predictably higher in students with strabismus, and
was present in 9 strabismic (8.3%) and 43 non-
strabismic students (2.0%; p50.0001; Table 2).
DISCUSSION
Interestingly, the prevalence of amblyopia (2.5%)
in this population sample was similar to that of
6–72-month-old Hispanic/Latino children (2.6%)
11
,
12–13-year-old children (2.5%) in Northern Mexico,
20
TABLE 1. Prevalence of strabismus and subtypes in the
Anyang Childhood Eye Study.
n(%)
Esotropia 2 (1.85)
Constant esotropia 2 (1.85)
Exotropia
a
102 (94.44)
Intermittent exotropia 84 (77.78)
Constant exotropia 18 (16.67)
Vertical deviation 3 (2.78)
Microstrabismus 1 (0.93)
Strabismus magnitude at distance (horizontal SPCT)
1–9 prism diopters 1 (0.93)
10–30 prism diopters 91 (84.26)
430 prism diopters 13 (12.04)
Strabismus magnitude at near (horizontal SPCT)
1–9 prism diopters 1 (0.93)
10–30 prism diopters 91 (84.26)
430 prism diopters 13 (12.04)
a
Ten students were noted in combination with vertical devi-
ation (2 with disassociated vertical deviation).
SPCT, simultaneous prism cover test
FIGURE 2. Distribution of spherical equivalent refraction (SER)
in 71 amblyopic eyes, 4135 non-amblyopic eyes and in total eyes
of students in the Anyang Childhood Eye Study.
FIGURE 3. Distribution of cylinder in 71 amblyopic eyes, 4135
non-amblyopic eyes and in total eyes of students in the Anyang
Childhood Eye Study.
200 J. Fu et al.
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and 3–6-year-old Taiwanese children (2.2%).
11,20,34
It
was, however, higher than that of previous reports of
Chinese adolescent populations, e.g. 5–15-year-old
urban children (0.8%) in southern China, 5–15-year-
old children (0.9%) in the Shunyi District of Beijing,
6–14-year-old children (1.0%) in Tibet, and 6–72-
month-old Chinese children (1.2%) in
Singapore.
13,15,16,24
Such differences in the prevalence
of amblyopia in Chinese students may be partly due
to differences in study design and definition of
amblyopia, and/or to availability of vision screening
programs early in life. Age of a population sample is
also a factor that may lead to variations in prevalence
data. In previous studies of Chinese adolescents,
individuals were, on average, younger than those
in the present study. In our study sample, 490% of
the children were 12–13 years old. At this age, visual
and ocular development is generally complete.
Amblyopia-related risk factors, if present, would
more likely have serious consequences in teenagers
than in younger children due to the fact that the
exposure time to risk factors has been shorter in
younger children. Last, but not least, 7th-grade
students comply well with doctors’ instructions, and
are able to complete more complicated examinations,
e.g. BCVA assessment and refraction, which are
indispensable for detecting mild cases of amblyopia.
Among the 52 students with amblyopia, only 11
(21.2%) had previously been diagnosed. The majority
(n= 41, 78.9%) had not been diagnosed prior to the
ACES. Questionnaire responses revealed that the
parents of these children were not aware of their
child’s vision problems. Treatment for these students
would be unlikely to be beneficial because of the long
delay in diagnosing the condition.
One striking finding of this study is that the
prevalence of strabismus in 7th-grade students in
central China was 5.0%, higher than in Chinese
children (0.8%) in the Strabismus, Amblyopia and
Refractive Error in Singaporean Children (STARS)
study, Hispanic/Latino (2.4%) and African-American
(2.5%) children in the Multi-Ethnic Pediatric Eye
Disease Study, Caucasian (3.3%) and African-
American (2.1%) children in the Baltimore Pediatric
Eye Disease Study, and Australian 6th- (2.8%)
and 12th-grade school children (2.7%) in the
Sydney Myopia Study.
10,11,13,15,16,18,19,24
It was also
1.9% higher than in 5–15-year-old children in a
metropolitan area of southern China, 2.8% higher
than in 5–15-year-old children in the Shunyi District
northeast of Beijing, China, and 2.5% higher than in
6–14-year-old primary school children in the rural
Tibetan area of China. The reason for such a high
prevalence of strabismus in 7th-grade students in
central China is not known. With regard to strabismus
type, the prevalence of esotropia in 7th-grade students
was much lower (n= 2, 2%). Most of the strabismus
was exotropia (n= 102, 94.4%). The reason for this
difference is uncertain. Although lower hyperopia
rates in East Asian populations may be partly
responsible, genetic and ethnic differences may also
play a role. Detection sensitivity of strabismus is also a
factor that could affect the outcome of a survey. The
collaboration of a pediatric ophthalmologist (JF), who
was responsible for all strabismus examinations
(Hirschberg light reflex, cover, and prism cover-
uncover tests) made detection of mild cases of
strabismus, e.g. microstrabismus, heterotropia, and
heterophoria more effectual.
Esotropia was not common in this population
sample (0.1%), in accordance with the lower preva-
lence of hyperopia (8.3%). The exotropia:esotropia
ratio was 51:1 in this study, a ratio similar to that
previously reported in Asian populations. Yu and
co-authors and Matsuo and Matsuo reported that the
exotropia:esotropia ratio was increasing in Hong
Kong and Japan, presumably because these popula-
tions have become less hyperopic.
35,36
The resultant
high exotropia:esotropia ratio is typical of East Asian
populations.
15,16,22–24
In contrast, this ratio is fre-
quently reversed in many studies of Caucasians,
because Caucasians are less myopic.
18,19,21
Continued epidemiological research into the preva-
lence and risk factors of strabismus, as well as the
impact of strabismus on visual function of young
children, is of major public health importance.
Although there was a sizeable response rate
(95.6%), this survey had several limitations. First,
since some students with amblyopia and strabismus
may have been treated before participating in the
study, the prevalence may have been underestimated.
TABLE 2. Comparison of selected ocular characteristics in
students with and without strabismus in the Anyang
Childhood Eye Study.
Characteristic
With
strabismus
(N= 108)
Without
strabismus
(N= 2043) pValue
Mean uncorrected visual acuity (logMAR letters)
Worse eye 0.2383 (43.1) 0.1979 (45.1) 0.0860
Better eye 0.1321 (48.4) 0.1053 (49.7) 0.1647
Mean corrected visual acuity (logMAR letters)
Worse eye 0.005 (55.3) 0.005 (55.3) 0.9869
Better eye 0.071 (58.5) 0.024 (56.2) 50.0010
Mean spherical
equivalent, D
2.43 1.50 50.0001
With esotropia 1.94 –
With exotropia 2.43 –
Mean cylinder, D 0.73 0.49 0.0020
Myopia, n(%) 90 (83.33) 1480 (68.77) 0.0013
Hyperopia, n(%) 9 (8.33) 334 (25.58) 0.0422
Astigmatism, n(%) 30 (27.78) 440 (20.45) 0.0670
Anisometropia, n(%) 21 (19.44) 359 (16.68) 0.4539
Amblyopia, n(%) 9 (8.33) 43 (2.00) 50.0001
D, diopters; logMAR, logarithm of the minimum angle of
resolution.
Prevalence of Amblyopia and Strabismus in China 201
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The questionnaire revealed that several students,
7 with amblyopia and 37 with strabismus, were
never treated. Second, past histories of ocular treat-
ments were parent-reported and subject to recall bias
and measurement errors. Third, since we did not have
any specific data on VA, refraction, and ocular
motility of non-participants, it is uncertain as to how
many students with amblyopia or strabismus may
have been omitted. However, the response rate of
95.64% is relatively high, so that selection bias
introduced by non-participants is rather low. Major
strengths of the study are its large cross-sectional
population and thorough research methods.
In conclusion, the prevalences of strabismus and
amblyopia in 7th-grade students in Central China
were 5.0% and 2.5%, respectively. The prevalence of
strabismus was higher in this population than in other
populations, particularly the proportion of exotropia,
while the prevalence of amblyopia is comparable to
those reported in other studies. Amblyopia and
strabismus were found to affect boys and girls equally.
Our data suggest that the prevalence of strabismus
and amblyopia in Central China is high. Vision
screening is of the utmost importance and should be
strengthened in the future.
DECLARATION OF INTEREST
The authors report no conflicts of interest. The authors
alone are responsible for the content and writing of
the paper.
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 (81120108007) of the National
Natural Science Foundation of China.
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