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Low prevalence of amblyopia and strabismus in Hani school
children in rural southwest China
Journal: BMJ Open
Manuscript ID bmjopen-2018-025441
Article Type: Research
Date Submitted by the Author: 20-Jul-2018
Complete List of Authors: Zhu, Hui; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology Pan, Chenwei; School of Public Health, Medical College of Soochow University, Sun, Qigang; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology Huang, Dan; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology
Fu, ZhuJun; Nanjing Children’s Hospital, Nanjing, Ophthalmology Wang, Jing; Jinling vision care center for children and adolescents Chen, XueJuan; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology Wang, Zijing; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology Liu, Hu; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology
Keywords: Epidemiology < TROPICAL MEDICINE, Public health < INFECTIOUS DISEASES, Strabismus < OPHTHALMOLOGY, Paediatric ophthalmology < OPHTHALMOLOGY
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Title page
Low prevalence of amblyopia and strabismus in Hani school children in rural
southwest China
Hui Zhu,1 Chenwei Pan,
2 Qigang Sun,
1 Dan Huang,
1 Zhujun Fu,
3 Jing Wang,
4
Xuejuan Chen,1 Zijing Wang,
1 Hu Liu
1*
1The First Affiliated Hospital with Nanjing Medical University, Nanjing, China
2School of Public Health, Medical College of Soochow University, Suzhou, China
3Nanjing Children’s Hospital, Nanjing, China
4Jinling vision care center for children and adolescents, Nanjing, China
*Correspondence to: Hu Liu, 300 Guangzhou Road, Department of Ophthalmology,
The First Affiliated Hospital with Nanjing Medical University, Nanjing 210029,
China. Email: [email protected], Phone: +86 (25) 68136470, Fax: +86 (25)
83275171.
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ABSTRACT
Purpose: To determine the prevalence of amblyopia and strabismus in Chinese Hani
ethnic school-aged children.
Methods: All grade 1 and grade 7 students in Mojiang Hani Autonomous County,
located in southwest China, were invited for comprehensive eye examinations,
including visual acuity, ocular alignment and movements, cycloplegic refraction,
anterior segment and fundus examinations. Participants with amblyopia or strabismus
were identified.
Results: A total of 2432 (90.2% response rate) grade 1 students and 2346 (93.5%
response rate) grade 7 students participated in the study. Among them, 1656 grade 1
Hani students and 1394 grade 7 Hani students were analyzed. Amblyopia was present
in 25 Hani students (0.82%, 95% CI 0.50%-1.14%), with no significant differences in
grade (p=0.328) and gender (p=0.602). Among these, 17 had unilateral amblyopia and
8 had bilateral amblyopia, including 16 anisometropic, 8 binocular refractive, and 1
strabismic. Strabismus was found in 59 Hani students (1.93%, 95% CI 1.44%-2.42%),
including 47 with intermittent exotropia, 6 with constant exotropia, 5 with constant
esotropia, and 1 with unilateral superior oblique palsy. Grade 7 students had a
significantly higher strabismus prevalence than grade 1 (p=0.063), while no
significant difference in gender was observed (p=0.340).
Conclusion: The prevalence of amblyopia and strabismus in Chinese Hani school
children are both lower than that previously reported for Chinese Han children in
China and for many other racial/ethnic populations from non-China studies.
Refractive error is the main cause for amblyopia and intermittent exotropia is the
main strabismus type.
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Strengths and limitations of this study
� This is a school-based cohort study conducted in Mojiang Hani Autonomous
County, rural southwest China.
� Mojiang has 13.5% of the total Chinese Hani population, and an enrollment rate
of 99% for elementary and middle schools.
� A total of 1656 grade 1 Hani students and 1394 grade 7 Hani students were
analyzed.
� Standard definitions of amblyopia and strabismus were applied.
� The prevalence estimates might be distorted as children who dropped out of
schools or were incapable of studying in regular schools were not included.
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INTRODUCTION
Amblyopia and strabismus are primarily pediatric eye diseases and can lead to vision
loss, impaired binocular function and cosmetic consequences, which might persist
through adulthood if left untreated. To form a rational policy for early detection and
management of amblyopia and strabismus, it is necessary to do epidemiologic studies
to estimate the prevalence of both diseases in children. With standard study design
and diagnostic criteria, the Multi-ethnic Pediatric Eye Disease Study (MEPEDS)1,2
,
the Baltimore Pediatric Eye Disease Study (BPEDS)3, the Strabismus, Amblyopia,
and Refractive Error in Singaporean children Study (STARS)4, the Sydney Paediatric
Eye Disease Study (SPEDS)5, the Nanjing Pediatric Vision Project (NPVP)
6, and the
Anyang childhood eye study (ACES)7 reported rates ranging from 0.8% to 2.6% for
amblyopia and 0.8% to 5.7% for strabismus. This variation of reported prevalence
mostly comes from various characteristics of study populations, especially with
respect to ethnic origin of participants.
The Hani people, an ethnic minority group, form one of the 56 officially recognized
nationalities of China. Over 90% of Hani peoples live in Yunnan Province, rural
southwest China, which is located across mountains and less prosperous than the
eastern and southern regions in China. Previous Chinese amblyopia or strabismus
prevalence studies mainly focused on the Han nationality, which accounts for 91.5%
of the Chinese population, and none on the Hani nationality. However, data from Han
populations should not be extrapolated to Hani children because of potential ethnic
variations and health care disparities. Our study was designed to assess the prevalence
of amblyopia and strabismus among Chinese Hani school children based on standard
methodology and definitions. This analysis is part of the Mojiang Myopia Progression
Study (MMPS).
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METHODS
Survey design and population
MMPS is a school-based cohort study aiming to longitudinally observe the onset and
progression of myopia, amblyopia, strabismus and other childhood ocular diseases in
grade1 and grade 7 students in Mojiang Hani Autonomous County, Yunnan Province,
rural southwest China8–11
. The baseline survey was conducted in 2016 and all the
grade 1 students from elementary schools and grade 7 students from middle schools in
Mojiang were invited to participate in this study.
Mojiang Hani Autonomous County, an area of 5,312 km2, is one of the 6 main
residences of the Hani people in Yunnan Province, China. There were 222,174 Hani
people in Mojiang as of 2010, accounting for 61.7% of the total population in
Mojiang and 13.5% of the total Chinese Hani population. The compulsory schooling
system is well executed in Mojiang with an enrollment rate of 99% for elementary
and middle schools in 2014. Thus, school-based samples in Mojiang are highly
representative of the local population.
Ethics committee approval was obtained from the Institutional Review Board of
Kunming Medical University. We carried out the study according to the tenets of the
Declaration of Helsinki involving human participants and the approved guidelines.
Additionally, we obtained written informed consents from at least one parent or legal
guardian of each participant.
Questionnaire and eye examinations
A questionnaire was filled up by the parents or legal guardians of the children to
collect detailed information regarding ethnicity and medical history. Uncorrected
visual acuity (UCVA) was measured using the Early Treatment Diabetic Retinopathy
Study visual acuity (VA) chart at a distance of 4 m. For children with UCVA ≤20/40
or two-line interocular difference, subjective optometry was performed to obtain best
corrected VA (BCVA). Ocular alignment was assessed by using the Hirschberg light
reflex test, the cover-uncover test and the alternate cover test. Cover test was
performed by using fixation targets at both distance (6 m) and near (33 cm). Binocular
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and monocular ocular movements were examined at nine diagnostic positions of gaze
with the head in a stationary position. Strabismus magnitude was measured in prism
diopters (PD) using the simultaneous prism and cover test. Each participant's
refractive status was measured after cycloplegia using an autorefractor (RM-8000;
Topcon Corp., Tokyo, Japan) by optometrists. For cycloplegia, each participant was
first administered two drops of 1% cyclopentolate (Alcon) after a 5-minute interval.
Thirty minutes later, a third drop was administered if pupillary light reflex was still
present or the pupil size was less than 6.0 mm. Other ocular examinations including
slit lamp examination, digital retinal photographs, ocular biometry, and optical
coherence tomography, were conducted to exclude any abnormalities precluding
normal vision.
Definitions
Unilateral amblyopia was defined as a 2-line inter-ocular difference between eyes
with BCVA ≤20/32 (≥ logMAR 0.2) in the worse eye and at least one of the
following unilateral amblyopia risk of factors: (1) strabismus on examination; (2)
previous strabismus surgery; (3) anisometropia consistent with the worse eye (≥
1.00D spherical equivalent (SE) anisohyperopia, ≥3.00D SE anisomyopia, or ≥
1.50D anisoastigmatism); (4) past or present obstruction of visual axis2,12
. Bilateral
amblyopia was defined as BCVA in both eyes <20/40 (>logMAR 0.3) with bilateral
ametropia (≥4.00D SE hyperopia, ≥6.00D SE myopia, or ≥2.50D astigmatism) or
with past or present bilateral obstruction of visual axis2,12
.
Strabismus was defined if any tropia was present at distance or near, with or without
spectacles and then classified according to the primary direction (esotropia, exotropia,
and vertical) of the tropia. Strabismus is considered as constant tropia if constant at
both near and distance fixation, otherwise it is considered as intermittent tropia.
Statistical analysis
All data were analyzed using SPSS 13.0 (IBM, China) at the 0.05 significance level.
Prevalence was calculated as the ratio of the number of individuals with any type of
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amblyopia or strabismus to the total number of individuals evaluated. Age- and sex-
specific prevalence for amblyopia and strabismus was calculated; chi-square tests
were used to evaluate statistically significant differences in prevalence between
subgroups. 95% confidence intervals (CIs) of prevalence were also provided.
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RESULTS
Study population
A total of 2432 (90.2% response rate) grade 1 students aged 7-8 years and 2346 (93.5%
response rate) grade 7 students aged 13-14 years participated in the study, including
3050 Hani (63.8%), 774 Han (16.2%), 954 other ethnic minorities (20.0%). The 3050
Hani ethnic students were included in the analysis, including 1656 grade 1 (mean age,
7.7 ± 0.6 years; 54.6% male) and 1394 grade 7 students (mean age, 13.8 ± 0.7 years;
51.5% male). There was no statistically significant age difference between boys and
girls in the 3050 students (p=0.274).
Prevalence of amblyopia in Hani
According to the findings from comprehensive ocular examinations of the 3050 Hani
participants, amblyopia was present in 25 students (0.82%, 95% CI 0.50%-1.14%),
including 16 grade 1 students(0.97%, 95% CI 0.50%-1.44%) and 9 grade 7
students(0.65%, 95% CI 0.23%-1.07%). The prevalence of amblyopia did not differ
between grade 1 and grade 7 (p=0.328), or between boys and girls (p=0.602). Table 1
summarizes the prevalence of unilateral and bilateral amblyopia by different causes.
Unilateral amblyopia was diagnosed in 17 children (0.56%, 95% CI 0.30%-0.82%),
and bilateral amblyopia was diagnosed in 8 children (0.26%, 95% CI 0.07%-0.44%).
Anisometropia was the cause in 16 of the 17 children (94.1%) with unilateral
amblyopia and ametropic the cause in all bilateral amblyopia. Nearly half of the 33
amblyopic eyes (51%, 17/33) had severe amblyopia (BCVA ≤20/100) and one third
(27%, 9/33) had BCVA ≤20/160. According to the questionnaire information
reported by the parents or legal guardians, no children had been previously diagnosed
or treated as having amblyopia.
Table 1. Prevalence of unilateral and bilateral amblyopia by different causes in Hani
Amblyopia type With
amblyopia, n
Prevalence (95% CI)
(%)
Unilateral 17 0.6 (0.3-0.8)
Strabismic 1 0.0 (0.00-0.1)
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Anisometropic 16 0.5 (0.3-0.8)
≥1.00 D SE anisohyperopia 5 0.2 (0.0-0.3)
≥3.00 D SE anisomyopia 4 0.1 (0.0-0.3)
≥1.50 D anisoastigmatism 6 0.2 (0.0-0.4)
≥1.00 D SE anisohyperopia+≥1.50 D anisoastigmatism 1 0.0 (0.00-0.1)
Bilateral 8 0.3 (0.1-0.4)
Ametropic 8 0.3 (0.1-0.4)
≥4.00 D SE hyperopia 3 0.1 (0.0-0.2)
≥6.00 D SE myopia 1 0.0 (0.0-0.1)
≥2.50 D astigmatism 4 0.1 (0.0-0.3)
CI, confidence interval; SE, spherical equivalent.
Prevalence of strabismus in Hani
A total of 59 (1.93%, 95% CI 1.44%-2.42%) were found to have strabismus, including
25 grade 1 students (1.50%, 95% CI 0.91%-2.09%) and 34 grade 7 students (2.44%,
95% CI 1.63%-3.25%). Grade 7 students had a significantly higher strabismus
prevalence than grade 1 (p=0.063), while no significant difference between boys and
girls was observed (p=0.340). Of the 59 strabismic students, 47 (80%) had
intermittent exotropia, 6 (10%) had constant exotropia, 5 (8%) had constant esotropia,
1 (2%) had unilateral superior oblique palsy. 5 of the intermittent exotropia and 1 of
constant esotropia had bilateral inferior oblique muscle overaction. The distribution of
strabismus magnitude in 58 students with horizontal strabismus is shown in Table 2.
Nearly one third of the horizontal strabismic students had more than 30 PD strabismus
magnitude at near or at distance. Based on the questionnaire information reported by
the parents or legal guardians, no children had been previously diagnosed or treated as
having strabismus.
Table 2. Distribution of strabismus magnitude in 58 Hani
students with horizontal strabismus
Strabismus magnitude n (%)
At near
1-9 PD 5 (9%)
10-30 PD 31 (53%)
>30 PD 22 (38%)
At distance
1-9 PD 28 (48%)
10-30 PD 14 (24%)
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>30 PD 16 (28%)
PD, prism diopter.
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DISCUSSION
In this school-based sample of Hani school children in China, we reported a 0.82%
prevalence of amblyopia. Amblyopia definitions have significant influence on
amblyopia prevalence estimation. Compared with the MEPEDS, BPEDS, STARS,
SPEDS, NPVP, and ACES studies which applied the same definitions as our study, the
amblyopia prevalence in Hani children was at a low level (Table 3). The
multi-country Refractive Error Study in Children (RESC) study, although using
different definitions of amblyopia, found significant differences among ethnic groups,
with low prevalence rates reported for African and south Asian (Indian) ethnic groups,
and higher prevalence rates in Hispanic and east Asian (Chinese) ethnic groups13
. The
authors speculated that general loss of pigmentation in the European and east Asian
people might be associated with low amblyopia prevalence. Chinese Hani people live
near south Asia and have more pigmentation than Chinese Han and European, which
might be a possible reason for the low amblyopia prevalence in Hani group. In our
findings, amblyopia prevalence was not significantly related with age or gender, and
refractive error, especially anisometropia, was the main cause for amblyopia, which
were consistent with the results from MEPEDS, STARS, SPEDS, NPVP and ACES.
Globally, the prevalence of strabismus in the Hani sample was lower than rates in
school children from other countries, including England (2.3%)14
,
Australia
(2.7%-2.8%)15,16
, Mexico (2.3%)17
, and Sweden (2.7%)18
. In China, the strabismus
prevalence in our study was also lower than most Chinese school children, including
2.8% from Shunyi (representative of rural northern China)19
, 3.0% from Guangzhou
(representative of urban southern China)20
, 2.5% from Maqin (representative of rural
Tibetan area)21
, and 5.0% from Anyang (representative of rural central China)22
. In
addition, when compared with studies in preschool children, the strabismus
prevalence in our study was also at a low level (Table 3). Population differences in
genetic susceptibility, environment, and lifestyle factors may contribute to the low
strabismus prevalence in Chinese Hani students.
Table 3. Prevalence of amblyopia and strabismus in different studies
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Study Country Age, years (n) Ethnicity Prevalence of
amblyopia*
Prevalence of
strabismus
MEPEDS, 2008 United States 2.5-6 (3350) African American (1663)
Hispanic/Latino (1687)
1.5%
2.6%
2.5%
2.4%
MEPEDS, 2013 United States 2.5-6 (1883) Asian American (938)
Non-Hispanic White
(945)
1.8%
1.8%
3.6%
3.2%
BPEDS, 2009 United States 2.5-6 (1546) Non-Hispanic White
(673)
African American (873)
1.8%
0.8%
3.3%
2.1%
STARS, 2010 Singapore 2.5-6 (1682) Singaporean Chinese 1.2% 0.8%
SPEDS, 2012 Australia 2.5-6 (1422) predominantly white 1.9% N/A**
NPVP, 2015 China 3-6 (5667) Chinese Han 1.2% 5.7%
ACES, 2014 China 6-9 (2893) Chinese Han 1.0 % N/A**
MMPS, 2018 China 7-8 (2432),13-14
(2346)
Chinese Hani 0.8% 1.9%
*Same definitions of amblyopia were used.
** No strabismus data.
Regarding strabismus type, about 90% of the strabismus was exotropia in the present
study. Previous studies have found that east Asian populations had higher
exotropia:esotropia ratio than Caucasians, and presumed that less hyperopic in east
Asian populations and less myopic in Caucasians might be the cause of the
difference1–4,6,16,18,23,24
. Our previous research revealed that exotropia was associated
with astigmatism, myopia and low to moderate hyperopia, while esotropia had a
severity-dependent relationship with hyperopia25
. Thus, distribution characteristics of
refraction may be partly responsible for higher exotropia:esotropia ratio. The
MEPEDS and NPVP studies have found higher prevalence of strabismus in older
preschool children1,2,6
. In our study, grade 7 students did have higher strabismus
prevalence than grade 1. This finding suggests that strabismus might increase with
age. No significant statistical differences of strabismus were observed in gender from
our study, which was in line with previous studies2,5,6,14–16
.
Limitations of this study include the following. First, the study is a school-based study
rather than a population-based one. The prevalence estimates might be distorted as
children who dropped out of schools or were incapable of studying in regular schools
were not included. However, we expected that the non-responder bias is minimal
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because of the high school attendance rates of students in Mojiang. Second,
small-angle or intermittent strabismus may have been missed given the nature of both
conditions. Finally, information on the history of amblyopia or strabismus was
collected by questionnaires, which might be potentially inaccurate due to recall
biases.
CONCLUSIONS
Strabismus affects 1.93% of Chinese Hani school children and amblyopia affects
0.82%. The prevalence of amblyopia and strabismus in this population are both lower
than that previously reported for Chinese Han children and for many other
racial/ethnic populations from non-China studies. Further studies are needed to
explore why Chinese Hani children have low prevalence of amblyopia and
strabismus.
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Contributorship statement Conceived and designed the experiments: HL, HZ, and
CP. Performed the experiments: HZ, QS, DH, ZF, and JW. Analyzed the data: HL, HZ,
CP, XC, and ZW. Contributed reagents/materials/analysis tools: HL, HZ, CP, and DH.
Wrote the paper: HL and HZ.
Competing interests None declared.
Funding This study is supported by Natural Science Foundation of Jiangsu Province
(Grant No. BK20161595); National Natural Science Foundation of China (Grant No.
81773449, No. 81560169 and No. 81673198).
Data sharing statement No additional data are available.
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REFERENCES
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amblyopia or strabismus in asian and non-Hispanic white preschool children:
multi-ethnic pediatric eye disease study. Ophthalmology.
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3. Friedman DS, Repka MX, Katz J, et al. Prevalence of amblyopia and strabismus
in white and African American children aged 6 through 71 months the Baltimore
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China: results from screening of preschool children aged 36-72 months. Br J
Ophthalmol. 2016;100(4):515-519.
7. Fu J, Li SM, Li SY, et al. Prevalence, causes and associations of amblyopia in
year 1 students in Central China : The Anyang childhood eye study (ACES).
Graefes Arch Clin Exp Ophthalmol. 2014;252(1):137-143.
8. Pan CW, Wu RK, Li J, et al. Low prevalence of myopia among school children
in rural China. BMC Ophthalmol. 2018;18(1):140.
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9. Pan CW, Wu RK, Wang P, et al. Reduced vision, refractive errors and
health-related quality of life among adolescents in rural China. Clin Exp Optom.
March 2018.
10. Pan CW, Wu RK, Liu H, et al. Types of Lamp for Homework and Myopia
among Chinese School-Aged Children. Ophthalmic Epidemiol.
2018;25(3):250-256.
11. Pan CW, Qiu QX, Qian DJ, et al. Iris colour in relation to myopia among
Chinese school-aged children. Ophthalmic Physiol Opt. 2018;38(1):48-55.
12. American academy of Ophthalmology Pediatric Ophthalmology/ Strabismus
Panel (2012): Preferred practice pattern guidelines. Amblyopia. San Francisco,
CA: American Academy of Ophthalmology, www. aao. org/ppp.
13. Xiao O, Morgan IG, Ellwein LB, et al. Prevalence of Amblyopia in School-Aged
Children and Variations by Age, Gender, and Ethnicity in a Multi-Country
Refractive Error Study. Ophthalmology. 2015;122(9):1924-1931.
14. Williams C, Northstone K, Howard M, et al. Prevalence and risk factors for
common vision problems in children: data from the ALSPAC study. Br J
Ophthalmol. 2008;92(7):959-964.
15. Robaei D, Rose KA, Ojaimi E, et al. Causes and associations of amblyopia in a
population-based sample of 6-year-old Australian children. Arch Ophthalmol.
2006;124(6):878-884.
16. Robaei D, Kifley A, Rose KA, et al. Impact of amblyopia on vision at age 12
years: findings from a population-based study. Eye (Lond). 2008;22(4):496-502.
17. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, amblyopia, and ocular
pathology in 12- to 13-year-old children in Northern Mexico. J AAPOS.
2003;7(1):47-53.
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18. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, residual amblyopia and
ocular pathology in a screened population of 12-13-year-old children in Sweden.
Acta Ophthalmol Scand. 2001;79(6):589-595.
19. Zhao J, Pan X, Sui R, et al. Refractive Error Study in Children: results from
Shunyi District, China. Am J Ophthalmol. 2000;129(4):427-435.
20. He M, Zeng J, Liu Y, et al. Refractive error and visual impairment in urban
children in southern china. Invest Ophthalmol Vis Sci. 2004;45(3):793-799.
21. Lu P, Chen X, Zhang W, et al. Prevalence of ocular disease in Tibetan primary
school children. Can J Ophthalmol. 2008;43(1):95-99.
22. Fu J, Li SM, Liu LR, et al. Prevalence of amblyopia and strabismus in a
population of 7th-grade junior high school students in Central China: the Anyang
Childhood Eye Study (ACES). Ophthalmic Epidemiol. 2014;21(3):197-203.
23. Yu CB, Fan DS, Wong VW, et al. Changing patterns of strabismus: a decade of
experience in Hong Kong. Br J Ophthalmol. 2002;86(8):854-856.
24. Chia A, Roy L, Seenyen L. Comitant horizontal strabismus: an Asian perspective.
Br J Ophthalmol. 2007;91(10):1337-1340.
25. Zhu H, Yu JJ, Yu RB, et al. Association between childhood strabismus and
refractive error in Chinese preschool children. PloS One. 2015;10(3):e0120720.
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No Recommendation
Page
No
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
1-2
(b) Provide in the abstract an informative and balanced summary of what
was done and what was found
1-2
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
4
Objectives 3 State specific objectives, including any prespecified hypotheses 4
Methods
Study design 4 Present key elements of study design early in the paper 5
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
5-6
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods
of selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and
methods of case ascertainment and control selection. Give the rationale for
the choice of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
5
(b) Cohort study—For matched studies, give matching criteria and number
of exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders,
and effect modifiers. Give diagnostic criteria, if applicable
5-6
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods
if there is more than one group
5-6
Bias 9 Describe any efforts to address potential sources of bias 5-6
Study size 10 Explain how the study size was arrived at 5
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If
applicable, describe which groupings were chosen and why
6-7
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
6-7
(b) Describe any methods used to examine subgroups and interactions 6-7
(c) Explain how missing data were addressed 6-7
(d) Cohort study—If applicable, explain how loss to follow-up was
addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
6-7
(e) Describe any sensitivity analyses 6-7
Continued on next page
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Results
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
8
(b) Give reasons for non-participation at each stage 8
(c) Consider use of a flow diagram
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
8
(b) Indicate number of participants with missing data for each variable of interest 8
(c) Cohort study—Summarise follow-up time (eg, average and total amount)
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
Cross-sectional study—Report numbers of outcome events or summary measures 8-10
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
8-10
(b) Report category boundaries when continuous variables were categorized
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
8-10
Discussion
Key results 18 Summarise key results with reference to study objectives 11
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
12-
13
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
11-
13
Generalisability 21 Discuss the generalisability (external validity) of the study results 11-
23
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
14
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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For peer review onlyPrevalence of amblyopia and strabismus in Hani school
children in rural southwest China: a cross-sectional study
Journal: BMJ Open
Manuscript ID bmjopen-2018-025441.R1
Article Type: Research
Date Submitted by the Author: 17-Sep-2018
Complete List of Authors: Zhu, Hui; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyPan, Chenwei; School of Public Health, Medical College of Soochow University, Sun, Qigang; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyHuang, Dan; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyFu, ZhuJun; Nanjing Children’s Hospital, Nanjing, OphthalmologyWang, Jing; Jinling vision care center for children and adolescentsChen, XueJuan; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyWang, Zijing; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyLiu, Hu; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology
<b>Primary Subject Heading</b>: Ophthalmology
Secondary Subject Heading: Epidemiology, Paediatrics, Public health
Keywords: Strabismus < OPHTHALMOLOGY, Paediatric ophthalmology < OPHTHALMOLOGY, EPIDEMIOLOGY, PUBLIC HEALTH
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Title page
Prevalence of amblyopia and strabismus in Hani school children in rural
southwest China: a cross-sectional study
Hui Zhu,1 Chenwei Pan,
2 Qigang Sun,
1 Dan Huang,
1 Zhujun Fu,
3 Jing Wang,
4
Xuejuan Chen,1 Zijing Wang,
1 Hu Liu
1*
1The First Affiliated Hospital with Nanjing Medical University, Nanjing, China
2School of Public Health, Medical College of Soochow University, Suzhou, China
3Nanjing Children’s Hospital, Nanjing, China
4Jinling vision care center for children and adolescents, Nanjing, China
*Correspondence to: Hu Liu, 300 Guangzhou Road, Department of Ophthalmology,
The First Affiliated Hospital with Nanjing Medical University, Nanjing 210029,
China. Email: [email protected], Phone: +86 (25) 68136470, Fax: +86 (25)
83275171.
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ABSTRACT
Purpose: To determine the prevalence rate of amblyopia and strabismus in Chinese
Hani ethnic school-aged children.
Methods: All grade 1 and grade 7 students in Mojiang Hani Autonomous County,
located in southwest China, were invited for comprehensive eye examinations
performed by experienced ophthalmologists and optometrists, including visual acuity,
ocular alignment and movements, cycloplegic refraction, anterior segment, and
fundus examinations. Standard definitions of amblyopia and strabismus were applied
to calculate their prevalence rate.
Results: A total of 1656 (91.0% response rate) grade 1 Hani students and 1394 (92.8%
response rate) grade 7 Hani students participated in the study. Amblyopia was present
in 25 Hani students (0.82%, 95% CI 0.55%-1.20%), with no significant differences in
grade (p=0.42) and gender (p=0.69). Among these 25 amblyopic children, 17 had
unilateral amblyopia and 8 had bilateral amblyopia, including 16 anisometropic, 8
binocular refractive, and 1 strabismic. Strabismus was found in 59 Hani students
(1.93%, 95% CI 1.50%-2.48%), including 47 with intermittent exotropia, 6 with
constant exotropia, 5 with constant esotropia, and 1 with unilateral superior oblique
palsy. The prevalence rate of strabismus was higher in grade 7 students than grade 1
students with borderline significance (2.44% vs. 1.50%, p=0.07), but was similar by
gender (2.16% in boys vs. 1.68% in girls, p=0.36).
Conclusion: The prevalence of amblyopia and strabismus in Chinese Hani school
children are both lower than that previously reported for Chinese Han children in
China and for many other racial/ethnic populations from non-China studies.
Refractive error is the major cause for amblyopia and intermittent exotropia is the
primary strabismus type.
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Strengths and limitations of this study
� This is a large school-based cohort study conducted in Mojiang Hani
Autonomous County, rural southwest China.
� Mojiang has 13.5% of the total Chinese Hani population, and an enrollment rate
of 99% for elementary and middle schools.
� A total of 1656 grade 1 Hani students and 1394 grade 7 Hani students were
analyzed, with high study participation rate (>90%).
� Standard definitions of amblyopia and strabismus were applied.
� The prevalence estimates might be biased as small percent of students did not
participate, and children who dropped out of schools or were not enrolled into
regular schools were not included.
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INTRODUCTION
Amblyopia and strabismus are primarily pediatric eye diseases and can lead to vision
loss, impaired binocular function and cosmetic consequences, which might persist
through adulthood if left untreated. To develop a rational policy for early detection
and management of amblyopia and strabismus, it is necessary to conduct
population-based epidemiologic studies to estimate their prevalence in children. With
standard study design and diagnosis criteria, the Multi-ethnic Pediatric Eye Disease
Study (MEPEDS)1,2
, the Baltimore Pediatric Eye Disease Study (BPEDS)3, the
Strabismus, Amblyopia, and Refractive Error in Singaporean children Study
(STARS)4, the Sydney Paediatric Eye Disease Study (SPEDS)
5, the Nanjing Pediatric
Vision Project (NPVP)6, the Anyang childhood eye study (ACES)
7 and the Yuhuatai
Pediatric Eye Disease Study (YPEDS)8 reported prevalence rates ranging from 0.8%
to 2.6% for amblyopia and 0.8% to 5.7% for strabismus. This large variation in
reported prevalence rate most likely is due to differences in the characteristics of
study populations, particularly the ethnicity of participants.
The Hani, an ethnic minority group, is one of the 56 officially recognized nationalities
in China. Over 90% of Hani people live in Yunnan Province, rural southwest China,
which is located across mountains and is less prosperous than the eastern and southern
regions in China. Previous Chinese amblyopia or strabismus prevalence studies
mainly focused on the Han nationality, which accounts for 91.5% of the Chinese
population, and these studies did not include the Hani nationality. However, data from
Han populations could not be extrapolated to Hani children because of potential
impact of ethnic variations and health care disparities on prevalences of eye diseases.
Our study was designed to assess the prevalence of amblyopia and strabismus among
Chinese Hani school children using standard methodology and definitions. This
analysis is part of the Mojiang Myopia Progression Study (MMPS).
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METHODS
Survey design and population
MMPS is a school-based cohort study designed to longitudinally assess the onset and
progression of myopia, amblyopia, strabismus and other childhood ocular diseases in
grade 1 and grade 7 students in Mojiang Hani Autonomous County, Yunnan Province,
rural southwest China9–12
. The baseline eye examination was conducted in 2016 and
all grade 1 students from elementary schools and grade 7 students from middle
schools in Mojiang were invited to participate in this study. This paper used data from
this baseline eye examination in grade 1 and grade 7 Hani students.
Mojiang Hani Autonomous County, an area of 5,312 km2, is one of the 6 main
residences of the Hani people in Yunnan Province, China. There were 222,174 Hani
people in Mojiang as of 2010, accounting for 61.7% of the total population in
Mojiang and 13.5% of the total Chinese Hani population. The compulsory 9-year
mandatory education system is well executed in Mojiang with an enrollment rate of
99% for elementary and middle schools in 2014. Thus, school-based samples in
Mojiang are highly representative of this school-aged population.
Ethics committee approval was obtained from the Institutional Review Board of
Kunming Medical University. We carried out the study according to the tenets of the
Declaration of Helsinki involving human participants and the approved guidelines.
Additionally, we obtained written informed consents from at least one parent or legal
guardian of each participant.
Questionnaire and eye examinations
A questionnaire was completed by the parents or legal guardians of the children to
collect detailed information regarding ethnicity and medical history. Comprehensive
eye examinations were performed by experienced ophthalmologists and optometrists.
Uncorrected visual acuity (UCVA) was measured using the Early Treatment Diabetic
Retinopathy Study visual acuity (VA) chart at a distance of 4 m. For children with
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UCVA ≤20/40 or at-least two-line interocular difference, subjective optometry was
performed to obtain best corrected VA (BCVA). Ocular alignment was assessed by
using the Hirschberg light reflex test, the cover-uncover test and the alternate cover
test. Cover test was performed by using fixation targets at both distance (6 m) and
near (33 cm). Binocular and monocular ocular movements were examined at nine
diagnostic positions of gaze with the head in a stationary position. Strabismus
magnitude was measured in prism diopters (PD) using the simultaneous prism and
cover test. Each participant's refractive status was measured after cycloplegia using an
autorefractor (RM-8000; Topcon Corp., Tokyo, Japan) by optometrists. For
cycloplegia, each participant was first administered two drops of 1% cyclopentolate
(Alcon) after a 5-minute interval. Thirty minutes later, a third drop was administered
if pupillary light reflex was still present or the pupil size was less than 6.0 mm. Other
ocular examinations including slit lamp examination, digital retinal photographs,
ocular biometry, and optical coherence tomography, were conducted to exclude any
abnormalities precluding normal vision.
Definitions
Unilateral amblyopia was defined as at least 2-line inter-ocular difference between
eyes with BCVA ≤20/32 (≥0.2 logMAR) in the worse eye and presence of at least
one of the following unilateral amblyopia risk of factors: (1) strabismus on
examination; (2) previous strabismus surgery; (3) anisometropia consistent with the
worse eye (≥ 1.00D spherical equivalent (SE) anisohyperopia, ≥ 3.00D SE
anisomyopia, or ≥1.50D anisoastigmatism); (4) past or present obstruction of visual
axis (e.g., cataract, corneal opacity, ptosis, eyelid hemangioma) which could not
explain the vision loss directly2,13
. Bilateral amblyopia was defined as BCVA in both
eyes <20/40 (>0.3 logMAR) with bilateral ametropia (≥4.00D SE hyperopia, or ≥
6.00D SE myopia, or ≥2.50D astigmatism) or with past or present bilateral
obstruction of visual axis (see above) which could not directly explain the vision
loss2,13
.
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Strabismus was defined present if any tropia was present at distance or near, with or
without spectacles and was classified according to the primary direction (esotropia,
exotropia, and vertical) of the tropia. Strabismus is considered as constant tropia if
constant at both near and distance fixation, otherwise it is considered as intermittent
tropia.
Statistical analysis
All data were analyzed using SPSS 13.0 (IBM, China) and 2-sided p<0.05 was
considered statistical significant. Prevalence rate for amblyopia and strabismus was
calculated as the percent of children with amblyopia or strabismus among all the Hani
children evaluated. Age- and sex- specific prevalence rate for amblyopia and
strabismus was calculated; Fisher exact test was used to compare the prevalence rate
between grade 1 and grade 7 and between boys and girls. 95% confidence intervals
(CIs) for prevalence rates were calculated using Wilson method.
Patient and Public Involvement
Patients and public were not involved in any aspects of the study including the
development of study question, study design, conduct of the study and dissemination
of results.
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RESULTS
Study population
A total of 1656 (91.0% response rate) grade 1 Hani students aged 7-8 years and 1394
(92.8% response rate) grade 7 Hani students aged 13-14 years participated in the study.
The mean age was 7.7 ± 0.6 and 13.8 ± 0.7 years for grade 1 and 7 students
respectively. There was similar percentage of boys among grade 1 students and grade
7 students (54.6% vs. 51.5%).
Prevalence of amblyopia in Hani
Based on the findings from comprehensive ocular examinations of the 3050 Hani
participants, amblyopia was present in 25 students (0.82%, 95% CI 0.55%-1.20%),
including 16 grade 1 students (0.97%, 95% CI 0.59%-1.56%) and 9 grade 7 students
(0.65%, 95% CI 0.34%-1.22%). The prevalence of amblyopia did not differ between
grade 1 and grade 7 (p=0.42), or between boys and girls (p=0.69). Unilateral
amblyopia was diagnosed in 17 children (0.56%, 95% CI 0.35%-0.89%), and bilateral
amblyopia was diagnosed in 8 children (0.26%, 95% CI 0.13%-0.51%). Table 1
summarizes the prevalence of unilateral and bilateral amblyopia by different causes.
Anisometropia was the cause in 16 of the 17 children (94.1%) with unilateral
amblyopia and ametropic was the cause in all bilateral amblyopia. Nearly half of the
33 amblyopic eyes (51%, 17/33) had severe amblyopia (BCVA ≤20/100) and one
third (27%, 9/33) had BCVA ≤20/160. Based on the questionnaire responses from
their parents or legal guardians, no children had been previously diagnosed with
amblyopia or treated for amblyopia.
Table 1. Prevalence of unilateral and bilateral amblyopia by different causes in Hani students
(N=3050)
Amblyopia type With amblyopia, n Prevalence (95% CI) (%)
Unilateral 17 0.56 (0.35-0.89)
Strabismic 1 0.03 (0.00-0.18)
Anisometropic 16 0.52 (0.32-0.84)
≥≥≥≥1.00 D SE anisohyperopia 5 0.16 (0.07-0.37)
≥≥≥≥3.00 D SE anisomyopia 4 0.13 (0.05-0.33)
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≥≥≥≥1.50 D anisoastigmatism 6 0.20 (0.09-0.43)
≥≥≥≥ 1.00 D SE anisohyperopia+ ≥≥≥≥ 1.50 D
anisoastigmatism
1 0.03 (0.00-0.18)
Bilateral 8 0.26 (0.13-0.51)
Ametropic 8 0.26 (0.13-0.51)
≥≥≥≥4.00 D SE hyperopia 3 0.10 (0.03-0.29)
≥≥≥≥6.00 D SE myopia 1 0.03 (0.00-0.18)
≥≥≥≥2.50 D astigmatism 4 0.13 (0.05-0.33)
CI, confidence interval; SE, spherical equivalent.
Prevalence of strabismus in Hani
A total of 59 (1.93%, 95% CI 1.50%-2.48%) children were found to have strabismus,
including 25 grade 1 students (1.50%, 95% CI 1.01%-2.20%) and 34 grade 7 students
(2.44%, 95% CI 1.75%-3.38%). The prevalence of strabismus was higher in grade 7
students than grade 1 students with borderline significance (2.44% vs. 1.50%, p=0.07),
but was similar in boys and girls (2.16% and 1.68% respectively, p=0.36). Of the 59
strabismic students, 47 (80%) had intermittent exotropia, 6 (10%) had constant
exotropia, 5 (8%) had constant esotropia, 1 (2%) had unilateral superior oblique palsy,
5 of the intermittent exotropia and 1 of constant esotropia had bilateral inferior
oblique muscle overaction. The distribution of strabismus magnitude in 58 students
with horizontal strabismus is shown in Table 2. Nearly one third of the horizontal
strabismic students had more than 30 PD strabismus magnitude at near or at distance.
Based on the questionnaire responses from the parents or legal guardians, no children
had been previously diagnosed with or treated for strabismus.
Table 2. Distribution of strabismus magnitude in 58 Hani
students with horizontal strabismus
Strabismus magnitude n (%)
At near
1-9 PD 5 (9%)
10-30 PD 31 (53%)
>30 PD 22 (38%)
At distance
1-9 PD 28 (48%)
10-30 PD 14 (24%)
>30 PD 16 (28%)
PD, prism diopter.
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DISCUSSION
In this school-based sample of Hani school children in China, we found a low (0.82%)
prevalence rate of amblyopia. Amblyopia definitions can have significant impact on
amblyopia prevalence estimate. Using the same standard amblyopia definition as
MEPEDS, BPEDS, STARS, SPEDS, NPVP, ACES and YPEDS studies, the
amblyopia prevalence in Hani children was lower than all these studies, including
these in Chinese Han children (Table 3). Compared with a study from Western China
in school children that used different amblyopia definition from this study14
, the
amblyopia prevalence rate in Hani school children was lower. The multi-country
Refractive Error Study in Children (RESC) study15
, also using different amblyopia
definition, reported higher amblyopia prevalence rates in Hispanic and Chinese
(predominantly Han) school children and lower amblyopia prevalence rates in African
and south Asian (Indian) school children than that in this study15
. General loss of
pigmentation in Hispanic and Chinese Han people might be associated with high
amblyopia prevalence. Chinese Hani people live near south Asia and have more
pigmentation than Chinese Han and Hispanic, which might be a possible reason for
the low amblyopia prevalence in Hani group. In a recent Israel study among young
adults, the prevalence of amblyopia was 0.8% in the population born between 1986
and 1994, which is similar to the rate in our study16
. Besides the difference in
amblyopia definition, the implementation of mandatory vision screening and the
universal healthcare provided to all Israel citizens by legislation might explain the low
prevalence rate of amblyopia in Israel. In this study, we found age and gender was not
significantly associated with amblyopia prevalence rate while refractive error,
particularly anisometropia, was the major cause for amblyopia. These findings are
consistent with the results from MEPEDS, STARS, SPEDS, NPVP, ACES and
YPEDS.
Globally, the prevalence rate of strabismus (1.90%) in the Hani sample was lower
than rates in school children from other countries, including England (2.3%)17
,
Australia (2.7%-2.8%)18,19
, Mexico (2.3%)20
, and Sweden (2.7%)21
. The strabismus
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prevalence rate in our study was also lower than most Chinese school children in
China, including 2.8% from Shunyi (representative of rural northern China)22
, 3.0%
from Guangzhou (representative of urban southern China)23
, 2.5% from Maqin
(representative of rural Tibetan area)24
, and 5.0% from Anyang (representative of rural
central China)25
. The strabismus prevalence rate in our study was also lower than
those from studies in preschool children (Table 3). Differences in genetic
susceptibility, environmental factors, and lifestyle may contribute to the lower rate of
strabismus in Chinese Hani students.
Table 3. Prevalence of amblyopia and strabismus in different studies
Study Country Age, years (n) Ethnicity Prevalence of
amblyopia*
Prevalence of
strabismus
MEPEDS, 2008 United States 2.5-6 (3350) African American (1663)
Hispanic/Latino (1687)
1.5%
2.6%
2.5%
2.4%
MEPEDS, 2013 United States 2.5-6 (1883) Asian American (938)
Non-Hispanic White
(945)
1.8%
1.8%
3.6%
3.2%
BPEDS, 2009 United States 2.5-6 (1546) Non-Hispanic White
(673)
African American (873)
1.8%
0.8%
3.3%
2.1%
STARS, 2010 Singapore 2.5-6 (1682) Singaporean Chinese 1.2% 0.8%
SPEDS, 2012 Australia 2.5-6 (1422) predominantly white 1.9% N/A**
NPVP, 2015 China 3-6 (5667) Chinese Han 1.2% 5.7%
ACES, 2014 China 6-9 (2893) Chinese Han 1.0 % N/A**
YPEDS, 2018 China 3-4 (1695) Chinese Han 1.47% N/A**
MMPS, 2018 China 7-8 (2432),13-14
(2346)
Chinese Hani 0.82% 1.93%
*Same definition of amblyopia was used.
** No strabismus data.
Our study found about 90% of the strabismus was exotropia. Previous studies have
found that east Asian populations had higher exotropia : esotropia ratio than
Caucasians, which might be due to less hyperopia in east Asian population than
Caucasians1–4,6,19,21,26,27
. Our previous research found that exotropia was associated
with astigmatism, myopia and low to moderate hyperopia, while esotropia was
associated with hyperopia in a dose-response manner28
. Thus, difference in refractive
error distribution may be responsible for higher exotropia : esotropia ratio in the study
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compared with other studies. Consistent with the MEPEDS and NPVP studies that
found higher prevalence of strabismus in older preschool children1,2,6
, our study found
that prevalence rate of strabismus was higher in grade 7 students than grade 1 students,
although the difference is only borderline significant (2.44% vs. 1.50%, p=0.07). This
finding suggests that strabismus might increase with age. Consistent with other
studies2,5,6,17–19
, our study did not find any significant difference in prevalence rate of
strabismus between boys and girls.
Our study has some limitations. First, the study is school-based rather than
population-based. The prevalence estimates might be biased as small percent of
school children did not participate in this study, and children who dropped out of
schools or did not attend regular schools were not included into the study. However,
we expect that this small percent of children not in our study will not substantially
bias our prevalence estimate. Second, small-angle or intermittent strabismus may have
been missed given the nature of both conditions. Third, the study used the cycloplegic
autorefraction instead of cycloplegic retinoscopy, and it could potentially bias the
refractive error measure. Finally, information on the history of amblyopia or
strabismus was collected by questionnaires, which might be potentially inaccurate due
to recall biases.
CONCLUSIONS
In this large school-based study of Chinese Hani school children, we found amblyopia
affects 0.82% children and strabismus affects 1.93% children. These prevalence rates
are both lower than those previously reported for Chinese Han children and for many
other racial/ethnic populations from non-China studies. Further studies are needed to
explore why Chinese Hani children have low prevalence of amblyopia and
strabismus.
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Contributorship statement Conceived and designed the experiments: HL, HZ, and
CP. Performed the experiments: HZ, QS, DH, ZF, and JW. Analyzed the data: HL, HZ,
CP, XC, and ZW. Contributed reagents/materials/analysis tools: HL, HZ, CP, and DH.
Wrote the paper: HL and HZ.
Competing interests None declared.
Funding This study is supported by Natural Science Foundation of Jiangsu Province
(Grant No. BK20161595); National Natural Science Foundation of China (Grant No.
81773449, No. 81560169 and No. 81673198).
Data sharing statement No additional data are available.
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REFERENCES
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2. McKean-Cowdin R, Cotter SA, Tarczy-Hornoch K, et al. Prevalence of amblyopia or
strabismus in asian and non-Hispanic white preschool children: multi-ethnic pediatric eye
disease study. Ophthalmology 2013;120:2117-24.
3. Friedman DS, Repka MX, Katz J, et al. Prevalence of amblyopia and strabismus in white
and African American children aged 6 through 71 months the Baltimore Pediatric Eye
Disease Study. Ophthalmology 2009;116:2128-34.e1-2.
4. Chia A, Dirani M, Chan YH, et al. Prevalence of amblyopia and strabismus in young
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5. Pai AS, Rose KA, Leone JF, et al. Amblyopia prevalence and risk factors in Australian
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6. Chen X, Fu Z, Yu J, et al. Prevalence of amblyopia and strabismus in Eastern China: results
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7. Fu J, Li SM, Li SY, et al. Prevalence, causes and associations of amblyopia in year 1
students in Central China : The Anyang childhood eye study (ACES). Graefes Arch Clin
Exp Ophthalmol 2014;252:137-43.
8. Huang D, Chen X, Zhu H, et al. Prevalence of amblyopia and its association with refraction
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9. Pan CW, Wu RK, Li J, et al. Low prevalence of myopia among school children in rural
China. BMC Ophthalmol 2018;18:140.
10. Pan CW, Wu RK, Wang P, et al. Reduced vision, refractive errors and health-related quality
of life among adolescents in rural China. Clin Exp Optom 2018.
11. Pan CW, Wu RK, Liu H, et al. Types of Lamp for Homework and Myopia among Chinese
School-Aged Children. Ophthalmic Epidemiol 2018;25:250-6.
12. Pan CW, Qiu QX, Qian DJ, et al. Iris colour in relation to myopia among Chinese
school-aged children. Ophthalmic Physiol Opt 2018;38:48-55.
13. American academy of Ophthalmology Pediatric Ophthalmology/ Strabismus Panel (2012):
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14. Pi LH, Chen L, Liu Q, et al. Prevalence of eye diseases and causes of visual impairment in
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15. Xiao O, Morgan IG, Ellwein LB, et al. Prevalence of Amblyopia in School-Aged Children
and Variations by Age, Gender, and Ethnicity in a Multi-Country Refractive Error Study.
Ophthalmology 2015;122:1924-31.
16. Shapira Y, Machluf Y, Mimouni M, et al. Amblyopia and strabismus: trends in prevalence
and risk factors among young adults in Israel. Br J Ophthalmol 2018;102:659-66.
17. Williams C, Northstone K, Howard M, et al. Prevalence and risk factors for common vision
problems in children: data from the ALSPAC study. Br J Ophthalmol 2008;92:959-64.
18. Robaei D, Rose KA, Ojaimi E, et al. Causes and associations of amblyopia in a
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2006;124:878-84.
19. Robaei D, Kifley A, Rose KA, et al. Impact of amblyopia on vision at age 12 years: findings
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20. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, amblyopia, and ocular pathology in
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21. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, residual amblyopia and ocular
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22. Zhao J, Pan X, Sui R, et al. Refractive Error Study in Children: results from Shunyi District,
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23. He M, Zeng J, Liu Y, et al. Refractive error and visual impairment in urban children in
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24. Lu P, Chen X, Zhang W, et al. Prevalence of ocular disease in Tibetan primary school
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25. Fu J, Li SM, Liu LR, et al. Prevalence of amblyopia and strabismus in a population of
7th-grade junior high school students in Central China: the Anyang Childhood Eye Study
(ACES). Ophthalmic Epidemiol 2014;21:197-203.
26. Yu CB, Fan DS, Wong VW, et al. Changing patterns of strabismus: a decade of experience
in Hong Kong. Br J Ophthalmol 2002;86:854-6.
27. Chia A, Roy L, Seenyen L. Comitant horizontal strabismus: an Asian perspective. Br J
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28. Zhu H, Yu JJ, Yu RB, et al. Association between childhood strabismus and refractive error
in Chinese preschool children. PloS One 2015;10:e0120720.
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No Recommendation
Page
No
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
1-2
(b) Provide in the abstract an informative and balanced summary of what
was done and what was found
1-2
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
4
Objectives 3 State specific objectives, including any prespecified hypotheses 4
Methods
Study design 4 Present key elements of study design early in the paper 5
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
5-6
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods
of selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and
methods of case ascertainment and control selection. Give the rationale for
the choice of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
5
(b) Cohort study—For matched studies, give matching criteria and number
of exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders,
and effect modifiers. Give diagnostic criteria, if applicable
5-7
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods
if there is more than one group
5-6
Bias 9 Describe any efforts to address potential sources of bias 5-6
Study size 10 Explain how the study size was arrived at 5
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If
applicable, describe which groupings were chosen and why
6-7
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
7
(b) Describe any methods used to examine subgroups and interactions 7
(c) Explain how missing data were addressed 7
(d) Cohort study—If applicable, explain how loss to follow-up was
addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
5, 7
(e) Describe any sensitivity analyses 7
Continued on next page
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Results
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
8
(b) Give reasons for non-participation at each stage 8
(c) Consider use of a flow diagram
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
8
(b) Indicate number of participants with missing data for each variable of interest 8
(c) Cohort study—Summarise follow-up time (eg, average and total amount)
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
Cross-sectional study—Report numbers of outcome events or summary measures 8-9
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
8-9
(b) Report category boundaries when continuous variables were categorized
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
8-9
Discussion
Key results 18 Summarise key results with reference to study objectives 10
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
12
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
10-
12
Generalisability 21 Discuss the generalisability (external validity) of the study results 10-
12
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
13
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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For peer review onlyPrevalence of amblyopia and strabismus in Hani school
children in rural southwest China: a cross-sectional study
Journal: BMJ Open
Manuscript ID bmjopen-2018-025441.R2
Article Type: Research
Date Submitted by the Author: 10-Nov-2018
Complete List of Authors: Zhu, Hui; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyPan, Chenwei; School of Public Health, Medical College of Soochow University, Sun, Qigang; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyHuang, Dan; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyFu, ZhuJun; Nanjing Children’s Hospital, Nanjing, OphthalmologyWang, Jing; Jinling vision care center for children and adolescentsChen, XueJuan; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyWang, Zijing; The First Affiliated Hospital with Nanjing Medical University, OphthalmologyLiu, Hu; The First Affiliated Hospital with Nanjing Medical University, Ophthalmology
<b>Primary Subject Heading</b>: Ophthalmology
Secondary Subject Heading: Epidemiology, Paediatrics, Public health
Keywords: Strabismus < OPHTHALMOLOGY, Paediatric ophthalmology < OPHTHALMOLOGY, EPIDEMIOLOGY, PUBLIC HEALTH
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Title page
Prevalence of amblyopia and strabismus in Hani school children in rural
southwest China: a cross-sectional study
Hui Zhu,1 Chenwei Pan,2 Qigang Sun,1 Dan Huang,1 Zhujun Fu,3 Jing Wang,4
Xuejuan Chen,1 Zijing Wang,1 Hu Liu1*
1The First Affiliated Hospital with Nanjing Medical University, Nanjing, China
2School of Public Health, Medical College of Soochow University, Suzhou, China
3Nanjing Children’s Hospital, Nanjing, China
4Jinling vision care center for children and adolescents, Nanjing, China
*Correspondence to: Hu Liu, 300 Guangzhou Road, Department of Ophthalmology,
The First Affiliated Hospital with Nanjing Medical University, Nanjing 210029,
China. Email: [email protected], Phone: +86 (25) 68136470, Fax: +86 (25)
83275171.
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ABSTRACT
Purpose: To determine the prevalence rate of amblyopia and strabismus in Chinese
Hani ethnic school-aged children.
Methods: All grade 1 and grade 7 students in Mojiang Hani Autonomous County,
located in southwest China, were invited for comprehensive eye examinations
performed by experienced ophthalmologists and optometrists, including visual acuity,
ocular alignment and movements, cycloplegic autorefraction, anterior segment, and
fundus examinations. Standard definitions of amblyopia and strabismus were applied
to calculate their prevalence rate.
Results: A total of 1656 (91.0% response rate) grade 1 Hani students and 1394
(92.8% response rate) grade 7 Hani students participated in the study. Amblyopia was
present in 25 Hani students (0.82%, 95% CI 0.55%-1.20%), with no significant
differences in grade (p=0.42) and gender (p=0.69). Among these 25 amblyopic
children, 17 had unilateral amblyopia and 8 had bilateral amblyopia, including 16
anisometropic, 8 binocular refractive, and 1 strabismic. Strabismus was found in 59
Hani students (1.93%, 95% CI 1.50%-2.48%), including 47 with intermittent
exotropia, 6 with constant exotropia, 5 with constant esotropia, and 1 with unilateral
superior oblique palsy. The prevalence rate of strabismus was higher in grade 7
students than grade 1 students with borderline significance (2.44% vs. 1.50%,
p=0.07), but was similar by gender (2.16% in boys vs. 1.68% in girls, p=0.36).
Conclusion: The prevalence of amblyopia and strabismus in Chinese Hani school
children are both lower than that previously reported for Chinese Han children in
China and for many other racial/ethnic populations from non-China studies.
Refractive error is the major cause for amblyopia and intermittent exotropia is the
primary strabismus type.
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Strengths and limitations of this study
This is a large school-based cohort study conducted in Mojiang Hani
Autonomous County, rural southwest China.
Mojiang has 13.5% of the total Chinese Hani population, and an enrollment rate
of 99% for elementary and middle schools.
A total of 1656 grade 1 Hani students and 1394 grade 7 Hani students were
analyzed, with high study participation rate (>90%).
Standard definitions of amblyopia and strabismus were applied.
The prevalence estimates might be biased as small percent of students did not
participate, and children who dropped out of schools or were not enrolled into
regular schools were not included.
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INTRODUCTION
Amblyopia and strabismus are primarily pediatric eye diseases and can lead to vision
loss, impaired binocular function and cosmetic consequences, which might persist
through adulthood if left untreated. To develop a rational policy for early detection
and management of amblyopia and strabismus, it is necessary to conduct
population-based epidemiologic studies to estimate their prevalence in children. With
standard study design and diagnosis criteria, the Multi-ethnic Pediatric Eye Disease
Study (MEPEDS)1,2, the Baltimore Pediatric Eye Disease Study (BPEDS)3, the
Strabismus, Amblyopia, and Refractive Error in Singaporean children Study
(STARS)4, the Sydney Paediatric Eye Disease Study (SPEDS)5, the Nanjing Pediatric
Vision Project (NPVP)6, the Anyang childhood eye study (ACES)7 and the Yuhuatai
Pediatric Eye Disease Study (YPEDS)8 reported prevalence rates ranging from 0.8%
to 2.6% for amblyopia and 0.8% to 5.7% for strabismus. This large variation in
reported prevalence rate most likely is due to differences in the characteristics of
study populations, particularly the ethnicity of participants.
The Hani, an ethnic minority group, is one of the 56 officially recognized nationalities
in China. Over 90% of Hani people live in Yunnan Province, rural southwest China,
which is located across mountains and is less prosperous than the eastern and southern
regions in China. Previous Chinese amblyopia or strabismus prevalence studies
mainly focused on the Han nationality, which accounts for 91.5% of the Chinese
population, and these studies did not include the Hani nationality. However, data from
Han populations could not be extrapolated to Hani children because of potential
impact of ethnic variations and health care disparities on prevalences of eye diseases.
Our study was designed to assess the prevalence of amblyopia and strabismus among
Chinese Hani school children using standard methodology and definitions. This
analysis is part of the Mojiang Myopia Progression Study (MMPS).
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METHODS
Survey design and population
MMPS is a school-based cohort study designed to longitudinally assess the onset and
progression of myopia, amblyopia, strabismus and other childhood ocular diseases in
grade 1 and grade 7 students in Mojiang Hani Autonomous County, Yunnan Province,
rural southwest China9–12. The baseline eye examination was conducted in 2016 and
all grade 1 students from elementary schools and grade 7 students from middle
schools in Mojiang were invited to participate in this study. This paper used data from
this baseline eye examination in grade 1 and grade 7 Hani students.
Mojiang Hani Autonomous County, an area of 5,312 km2, is one of the 6 main
residences of the Hani people in Yunnan Province, China. There were 222,174 Hani
people in Mojiang as of 2010, accounting for 61.7% of the total population in
Mojiang and 13.5% of the total Chinese Hani population. The compulsory 9-year
mandatory education system is well executed in Mojiang with an enrollment rate of
99% for elementary and middle schools in 2014. Thus, school-based samples in
Mojiang are highly representative of this school-aged population.
Ethics committee approval was obtained from the Institutional Review Board of
Kunming Medical University. We carried out the study according to the tenets of the
Declaration of Helsinki involving human participants and the approved guidelines.
Additionally, we obtained written informed consents from at least one parent or legal
guardian of each participant.
Questionnaire and eye examinations
A questionnaire was completed by the parents or legal guardians of the children to
collect detailed information regarding ethnicity and medical history. Comprehensive
eye examinations were performed by experienced ophthalmologists and optometrists.
Uncorrected visual acuity (UCVA) was measured using the Early Treatment Diabetic
Retinopathy Study visual acuity (VA) chart at a distance of 4 m. For children with
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UCVA 20/40 or at-least two-line interocular difference, subjective optometry was ≤
performed to obtain best corrected VA (BCVA). Ocular alignment was assessed by
using the Hirschberg light reflex test, the cover-uncover test and the alternate cover
test. Cover test was performed by using fixation targets at both distance (6 m) and
near (33 cm). Binocular and monocular ocular movements were examined at nine
diagnostic positions of gaze with the head in a stationary position. Strabismus
magnitude was measured in prism diopters (PD) using the simultaneous prism and
cover test. Each participant's refractive status was measured after cycloplegia using an
autorefractor (RM-8000; Topcon Corp., Tokyo, Japan) by optometrists. For
cycloplegia, each participant was first administered two drops of 1% cyclopentolate
(Alcon) after a 5-minute interval. Thirty minutes later, a third drop was administered
if pupillary light reflex was still present or the pupil size was less than 6.0 mm. Other
ocular examinations including slit lamp examination, digital retinal photographs,
ocular biometry, and optical coherence tomography, were conducted to exclude any
abnormalities precluding normal vision.
Definitions
Unilateral amblyopia was defined as at least 2-line inter-ocular difference between
eyes with BCVA ≤20/32 (≥0.2 logMAR) in the worse eye and presence of at least
one of the following unilateral amblyopia risk of factors: (1) strabismus on
examination; (2) previous strabismus surgery; (3) anisometropia consistent with the
worse eye ( ≥ 1.00D spherical equivalent (SE) anisohyperopia, ≥ 3.00D SE
anisomyopia, or ≥1.50D anisoastigmatism); (4) past or present obstruction of visual
axis (e.g., cataract, corneal opacity, ptosis, eyelid hemangioma) which could not
explain the vision loss directly2,13. Bilateral amblyopia was defined as BCVA in both
eyes <20/40 (>0.3 logMAR) with bilateral ametropia (≥4.00D SE hyperopia, or ≥
6.00D SE myopia, or ≥ 2.50D astigmatism) or with past or present bilateral
obstruction of visual axis (see above) which could not directly explain the vision
loss2,13.
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Strabismus was defined present if any tropia was present at distance or near, with or
without spectacles and was classified according to the primary direction (esotropia,
exotropia, and vertical) of the tropia. Strabismus is considered as constant tropia if
constant at both near and distance fixation, otherwise it is considered as intermittent
tropia.
Statistical analysis
All data were analyzed using SPSS 13.0 (IBM, China) and 2-sided p<0.05 was
considered statistical significant. Prevalence rate for amblyopia and strabismus was
calculated as the percent of children with amblyopia or strabismus among all the Hani
children evaluated. Age- and sex- specific prevalence rate for amblyopia and
strabismus was calculated; Fisher exact test was used to compare the prevalence rate
between grade 1 and grade 7 and between boys and girls. 95% confidence intervals
(CIs) for prevalence rates were calculated using Wilson method.
Patient and Public Involvement
Patients and public were not involved in any aspects of the study including the
development of study question, study design, conduct of the study and dissemination
of results.
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RESULTS
Study population
A total of 1656 (91.0% response rate) grade 1 Hani students aged 7-8 years and 1394
(92.8% response rate) grade 7 Hani students aged 13-14 years participated in the
study. The mean age was 7.7 ± 0.6 and 13.8 ± 0.7 years for grade 1 and 7 students
respectively. There was similar percentage of boys among grade 1 students and grade
7 students (54.6% vs. 51.5%).
Prevalence of amblyopia in Hani
Based on the findings from comprehensive ocular examinations of the 3050 Hani
participants, amblyopia was present in 25 students (0.82%, 95% CI 0.55%-1.20%),
including 16 grade 1 students (0.97%, 95% CI 0.59%-1.56%) and 9 grade 7 students
(0.65%, 95% CI 0.34%-1.22%). The prevalence of amblyopia did not differ between
grade 1 and grade 7 (p=0.42), or between boys (0.74%, 95% CI 0.42%-1.28%) and
girls (0.91%, 95% CI 0.53%-1.54%; p=0.69). Unilateral amblyopia was diagnosed in
17 children (0.56%, 95% CI 0.35%-0.89%), and bilateral amblyopia was diagnosed in
8 children (0.26%, 95% CI 0.13%-0.51%). Table 1 summarizes the prevalence of
unilateral and bilateral amblyopia by different causes. Anisometropia was the cause in
16 of the 17 children (94.1%) with unilateral amblyopia and ametropia was the cause
in all bilateral amblyopia. Nearly half of the 33 amblyopic eyes (51%, 17/33) had
severe amblyopia (BCVA ≤20/100) and one third (27%, 9/33) had BCVA ≤20/160.
Based on the questionnaire responses from their parents or legal guardians, no
children had been previously diagnosed with amblyopia or treated for amblyopia.
Table 1. Prevalence of unilateral and bilateral amblyopia by different causes in Hani students (N=3050)Amblyopia type With amblyopia, n Prevalence (95% CI) (%)Unilateral 17 0.56 (0.35-0.89)Strabismic 1 0.03 (0.00-0.18)Anisometropic 16 0.52 (0.32-0.84)≥1.00 D SE anisohyperopia 5 0.16 (0.07-0.37)≥3.00 D SE anisomyopia 4 0.13 (0.05-0.33)
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≥1.50 D anisoastigmatism 6 0.20 (0.09-0.43)≥ 1.00 D SE anisohyperopia+ ≥ 1.50 D
anisoastigmatism1 0.03 (0.00-0.18)
Bilateral 8 0.26 (0.13-0.51)Ametropic 8 0.26 (0.13-0.51)≥4.00 D SE hyperopia 3 0.10 (0.03-0.29)≥6.00 D SE myopia 1 0.03 (0.00-0.18)≥2.50 D astigmatism 4 0.13 (0.05-0.33)
CI, confidence interval; SE, spherical equivalent.
Prevalence of strabismus in Hani
A total of 59 (1.93%, 95% CI 1.50%-2.48%) children were found to have strabismus,
including 25 grade 1 students (1.50%, 95% CI 1.01%-2.20%) and 34 grade 7 students
(2.44%, 95% CI 1.75%-3.38%). The prevalence of strabismus was higher in grade 7
students than grade 1 students with borderline significance (2.44% vs. 1.50%,
p=0.07), but was similar in boys and girls (2.16% and 1.68% respectively, p=0.36).
Of the 59 strabismic students, 47 (80%) had intermittent exotropia, 6 (10%) had
constant exotropia, 5 (8%) had constant esotropia, 1 (2%) had unilateral superior
oblique palsy, 5 of the intermittent exotropia and 1 of constant esotropia had bilateral
inferior oblique muscle overaction. The distribution of strabismus magnitude in 58
students with horizontal strabismus is shown in Table 2. Nearly one third of the
horizontal strabismic students had more than 30 PD strabismus magnitude at near or
at distance. Based on the questionnaire responses from the parents or legal guardians,
no children had been previously diagnosed with or treated for strabismus.
Table 2. Distribution of strabismus magnitude in 58 Hani students with horizontal strabismusStrabismus magnitude n (%)At near
1-9 PD 5 (9%)10-30 PD 31 (53%)>30 PD 22 (38%)
At distance1-9 PD 28 (48%)10-30 PD 14 (24%)>30 PD 16 (28%)
PD, prism diopter.
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DISCUSSION
In this school-based sample of Hani school children in China, we found a low (0.82%)
prevalence rate of amblyopia. Amblyopia definitions can have significant impact on
amblyopia prevalence estimate. Using the same standard amblyopia definition as
MEPEDS, BPEDS, STARS, SPEDS, NPVP, ACES and YPEDS studies, the
amblyopia prevalence in Hani children was lower than all these studies, including
these in Chinese Han children (Table 3). Compared with a study from Western China
in school children that used different amblyopia definition from this study14, the
amblyopia prevalence rate in Hani school children was lower.
The multi-country Refractive Error Study in Children (RESC) study15, also using
different amblyopia definition, reported higher amblyopia prevalence rates in
Hispanic and Chinese (predominantly Han) school children and lower amblyopia
prevalence rates in African and south Asian (Indian) school children than that in this
study15. General loss of pigmentation in Hispanic and Chinese Han people might be
associated with high amblyopia prevalence, because that many studies have reported
the associations between low pigmentation and refractive errors, especially
astigmatism16–18. Chinese Hani people live near south Asia and have more
pigmentation than Chinese Han and Hispanic, which might be a possible reason for
the low amblyopia prevalence in Hani group. In a recent Israel study among young
adults, the prevalence of amblyopia was 0.8% in the population born between 1986
and 1994, which is similar to the rate in our study19. Besides the difference in
amblyopia definition, the implementation of mandatory vision screening and the
universal healthcare provided to all Israel citizens by legislation might explain the low
prevalence rate of amblyopia in Israel.
In this study, we found that age and gender was not significantly associated with
amblyopia prevalence rate while refractive error, particularly anisometropia, was the
major cause for amblyopia. These findings are consistent with the results from
MEPEDS, STARS, SPEDS, NPVP, ACES and YPEDS.
Globally, the prevalence rate of strabismus (1.90%) in the Hani sample was lower
than rates in school children from other countries, including England (2.3%)20,
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Australia (2.7%-2.8%)21,22, Mexico (2.3%)23, and Sweden (2.7%)24. The strabismus
prevalence rate in our study was also lower than most Chinese school children in
China, including 2.8% from Shunyi (representative of rural northern China)25, 3.0%
from Guangzhou (representative of urban southern China)26, 2.5% from Maqin
(representative of rural Tibetan area)27, and 5.0% from Anyang (representative of
rural central China)28. The strabismus prevalence rate in our study was also lower than
those from studies in preschool children (Table 3). Differences in genetic
susceptibility, environmental factors, and lifestyle may contribute to the lower rate of
strabismus in Chinese Hani students.
Table 3. Prevalence of amblyopia and strabismus in different studiesStudy Country Age, years (n) Ethnicity Prevalence of
amblyopia*Prevalence of strabismus
MEPEDS, 2008 United States 2.5-6 (3350) African American (1663)Hispanic/Latino (1687)
1.5%2.6%
2.5%2.4%
MEPEDS, 2013 United States 2.5-6 (1883) Asian American (938)Non-Hispanic White (945)
1.8%1.8%
3.6%3.2%
BPEDS, 2009 United States 2.5-6 (1546) Non-Hispanic White (673)African American (873)
1.8%0.8%
3.3%2.1%
STARS, 2010 Singapore 2.5-6 (1682) Singaporean Chinese 1.2% 0.8%SPEDS, 2012 Australia 2.5-6 (1422) predominantly white 1.9% N/A**
NPVP, 2015 China 3-6 (5667) Chinese Han 1.2% 5.7%ACES, 2014 China 6-9 (2893) Chinese Han 1.0 % N/A**
YPEDS, 2018 China 3-4 (1695) Chinese Han 1.47% N/A**
MMPS, 2018 China 7-8 (2432),13-14 (2346)
Chinese Hani 0.82% 1.93%
*Same definition of amblyopia was used. ** No strabismus data.
Our study found that about 90% of the strabismus was exotropia. Previous studies
have found that east Asian populations had higher exotropia : esotropia ratio than
Caucasians, which might be due to less hyperopia in east Asian population than
Caucasians1–4,6,22,24,29,30. Our previous research found that exotropia was associated
with astigmatism, myopia and low to moderate hyperopia, while esotropia was
associated with hyperopia in a dose-response manner31. Thus, difference in refractive
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error distribution may be responsible for higher exotropia : esotropia ratio in the study
compared with other studies. Consistent with the MEPEDS and NPVP studies that
found higher prevalence of strabismus in older preschool children1,2,6, our study found
that prevalence rate of strabismus was higher in grade 7 students than grade 1
students, although the difference is only borderline significant (2.44% vs. 1.50%,
p=0.07). This finding suggests that strabismus might increase with age. Consistent
with other studies2,5,6,20–22, our study did not find any significant difference in
prevalence rate of strabismus between boys and girls.
Our study has some limitations. First, the study is school-based rather than
population-based. The prevalence estimates might be biased as small percent of
school children did not participate in this study, and children who dropped out of
schools or did not attend regular schools were not included into the study. However,
we expect that this small percent of children not in our study will not substantially
bias our prevalence estimate. Second, small-angle or intermittent strabismus may have
been missed given the nature of both conditions. Third, the study used the cycloplegic
autorefraction instead of cycloplegic retinoscopy, and it could potentially bias the
refractive error measure. However, a recent study among school children found that
the two methods had a strong correlation and agreement, and the differences between
their measures were clinically insignificant32. Finally, information on the history of
amblyopia or strabismus was collected by questionnaires, which might be potentially
inaccurate due to recall biases.
CONCLUSIONS
In this large school-based study of Chinese Hani school children, we found that
amblyopia affects 0.82% children and strabismus affects 1.93% children. These
prevalence rates are both lower than those previously reported for Chinese Han
children and for many other racial/ethnic populations from non-China studies. Further
studies are needed to explore why Chinese Hani children have low prevalence of
amblyopia and strabismus.
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Contributorship statement Conceived and designed the experiments: HL, HZ, and
CP. Performed the experiments: HZ, QS, DH, ZF, and JW. Analyzed the data: HL,
HZ, CP, XC, and ZW. Contributed reagents/materials/analysis tools: HL, HZ, CP, and
DH. Wrote the paper: HL and HZ.
Competing interests None declared.
Funding This study is supported by Natural Science Foundation of Jiangsu Province
(Grant No. BK20161595); National Natural Science Foundation of China (Grant No.
81773449, No. 81560169, No. 81673198 and No. 81803258).
Data sharing statement No additional data are available.
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2. McKean-Cowdin R, Cotter SA, Tarczy-Hornoch K, et al. Prevalence of amblyopia or strabismus in asian and non-Hispanic white preschool children: multi-ethnic pediatric eye disease study. Ophthalmology 2013;120:2117-24.
3. Friedman DS, Repka MX, Katz J, et al. Prevalence of amblyopia and strabismus in white and African American children aged 6 through 71 months the Baltimore Pediatric Eye Disease Study. Ophthalmology 2009;116:2128-34.e1-2.
4. Chia A, Dirani M, Chan YH, et al. Prevalence of amblyopia and strabismus in young singaporean chinese children. Invest Ophthalmol Vis Sci 2010;51:3411-7.
5. Pai AS, Rose KA, Leone JF, et al. Amblyopia prevalence and risk factors in Australian preschool children. Ophthalmology 2012;119:138-44.
6. Chen X, Fu Z, Yu J, et al. Prevalence of amblyopia and strabismus in Eastern China: results from screening of preschool children aged 36-72 months. Br J Ophthalmol 2016;100:515-9.
7. Fu J, Li SM, Li SY, et al. Prevalence, causes and associations of amblyopia in year 1 students in Central China : The Anyang childhood eye study (ACES). Graefes Arch Clin Exp Ophthalmol 2014;252:137-43.
8. Huang D, Chen X, Zhu H, et al. Prevalence of amblyopia and its association with refraction in Chinese preschool children aged 36-48 months. Br J Ophthalmol 2018;102:767-71.
9. Pan CW, Wu RK, Li J, et al. Low prevalence of myopia among school children in rural China. BMC Ophthalmol 2018;18:140.
10. Pan CW, Wu RK, Wang P, et al. Reduced vision, refractive errors and health-related quality of life among adolescents in rural China. Clin Exp Optom 2018;101:758-63.
11. Pan CW, Wu RK, Liu H, et al. Types of Lamp for Homework and Myopia among Chinese School-Aged Children. Ophthalmic Epidemiol 2018;25:250-6.
12. Pan CW, Qiu QX, Qian DJ, et al. Iris colour in relation to myopia among Chinese school-aged children. Ophthalmic Physiol Opt 2018;38:48-55.
13. American academy of Ophthalmology Pediatric Ophthalmology/ Strabismus Panel (2012): Preferred practice pattern guidelines. Amblyopia. San Francisco, CA: American Academy of Ophthalmology, www. aao. org/ppp.
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14. Pi LH, Chen L, Liu Q, et al. Prevalence of eye diseases and causes of visual impairment in school-aged children in Western China. J Epidemiol 2012;22:37-44.
15. Xiao O, Morgan IG, Ellwein LB, et al. Prevalence of Amblyopia in School-Aged Children and Variations by Age, Gender, and Ethnicity in a Multi-Country Refractive Error Study. Ophthalmology 2015;122:1924-31.
16. Schweigert A, Lunos S, Connett J, et al. Changes in refractive errors in albinism: a longitudinal study over the first decade of life. J AAPOS 2018.
17. Yahalom C, Tzur V, Blumenfeld A, et al. Refractive profile in oculocutaneous albinism and its correlation with final visual outcome. Br J Ophthalmol 2012;96:537-9.
18. Wildsoet CF, Oswald PJ, Clark S. Albinism: its implications for refractive development. Invest Ophthalmol Vis Sci 2000;41:1-7.
19. Shapira Y, Machluf Y, Mimouni M, et al. Amblyopia and strabismus: trends in prevalence and risk factors among young adults in Israel. Br J Ophthalmol 2018;102:659-66.
20. Williams C, Northstone K, Howard M, et al. Prevalence and risk factors for common vision problems in children: data from the ALSPAC study. Br J Ophthalmol 2008;92:959-64.
21. Robaei D, Rose KA, Ojaimi E, et al. Causes and associations of amblyopia in a population-based sample of 6-year-old Australian children. Arch Ophthalmol 2006;124:878-84.
22. Robaei D, Kifley A, Rose KA, et al. Impact of amblyopia on vision at age 12 years: findings from a population-based study. Eye (Lond) 2008;22:496-502.
23. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, amblyopia, and ocular pathology in 12- to 13-year-old children in Northern Mexico. J AAPOS 2003;7:47-53.
24. Ohlsson J, Villarreal G, Sjöström A, et al. Visual acuity, residual amblyopia and ocular pathology in a screened population of 12-13-year-old children in Sweden. Acta Ophthalmol Scand. 2001;79:589-95.
25. Zhao J, Pan X, Sui R, et al. Refractive Error Study in Children: results from Shunyi District, China. Am J Ophthalmol 2000;129:427-35.
26. He M, Zeng J, Liu Y, et al. Refractive error and visual impairment in urban children in southern china. Invest Ophthalmol Vis Sci 2004;45:793-9.
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27. Lu P, Chen X, Zhang W, et al. Prevalence of ocular disease in Tibetan primary school children. Can J Ophthalmol 2008;43:95-9.
28. Fu J, Li SM, Liu LR, et al. Prevalence of amblyopia and strabismus in a population of 7th-grade junior high school students in Central China: the Anyang Childhood Eye Study (ACES). Ophthalmic Epidemiol 2014;21:197-203.
29. Yu CBO, Fan DSP, Wong VWY, et al. Changing patterns of strabismus: a decade of experience in Hong Kong. Br J Ophthalmol 2002;86:854-6.
30. Chia A, Roy L, Seenyen L. Comitant horizontal strabismus: an Asian perspective. Br J Ophthalmol 2007;91:1337-40.
31. Zhu H, Yu JJ, Yu RB, et al. Association between childhood strabismus and refractive error in Chinese preschool children. PloS One 2015;10:e0120720.
32. Hashemi H, Khabazkhoob M, Asharlous A, et al. Overestimation of hyperopia with autorefraction compared with retinoscopy under cycloplegia in school-age children. Br J Ophthalmol 2018.
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No Recommendation
Page
No
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
1-2
(b) Provide in the abstract an informative and balanced summary of what
was done and what was found
1-2
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
4
Objectives 3 State specific objectives, including any prespecified hypotheses 4
Methods
Study design 4 Present key elements of study design early in the paper 5
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
5-6
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods
of selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and
methods of case ascertainment and control selection. Give the rationale for
the choice of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
5
(b) Cohort study—For matched studies, give matching criteria and number
of exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders,
and effect modifiers. Give diagnostic criteria, if applicable
5-7
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods
if there is more than one group
5-6
Bias 9 Describe any efforts to address potential sources of bias 5-6
Study size 10 Explain how the study size was arrived at 5
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If
applicable, describe which groupings were chosen and why
6-7
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
7
(b) Describe any methods used to examine subgroups and interactions 7
(c) Explain how missing data were addressed 7
(d) Cohort study—If applicable, explain how loss to follow-up was
addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
5, 7
(e) Describe any sensitivity analyses 7
Continued on next page
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Results
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
8
(b) Give reasons for non-participation at each stage 8
(c) Consider use of a flow diagram
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
8
(b) Indicate number of participants with missing data for each variable of interest 8
(c) Cohort study—Summarise follow-up time (eg, average and total amount)
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
Cross-sectional study—Report numbers of outcome events or summary measures 8-9
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
8-9
(b) Report category boundaries when continuous variables were categorized
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
8-9
Discussion
Key results 18 Summarise key results with reference to study objectives 10
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
12
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
10-
12
Generalisability 21 Discuss the generalisability (external validity) of the study results 10-
12
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
13
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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