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Prevalence of amblyopia and strabismus in Eastern China: results from screening of preschool children aged 36–72 months
  1. Xuejuan Chen1,
  2. Zhujun Fu1,
  3. Jiajia Yu2,
  4. Hui Ding3,
  5. Jing Bai3,
  6. Ji Chen3,
  7. Yu Gong4,
  8. Hui Zhu1,
  9. Rongbing Yu5,
  10. Hu Liu1
  1. 1Department of Ophthalmology, The First Affiliated Hospital with Nanjing Medical University, Nanjing, China
  2. 2Department of Ophthalmology, Wuxi No. 2 People's Hospital, Wuxi, China
  3. 3Maternal and Child Healthcare Hospital of Yuhua District, Nanjing, China
  4. 4Department of Ophthalmology, Soochow University Affiliated Children's Hospital, Suzhou, China
  5. 5School of Public Health, Nanjing Medical University, Nanjing, China
  1. Correspondence to Professor Hu Liu, Department of Ophthalmology, The First Affiliated Hospital with Nanjing Medical University, 300 Guangzhou Road, Nanjing 210029, China; liuhu66{at}163.com

Abstract

Purpose To determine the prevalence of amblyopia and strabismus in preschool children in Eastern China.

Methods The Nanjing Pediatric Vision Project was a cross-sectional, population-based cohort study conducted in preschool children aged 36–72 months from 2011 to 2012 in Yuhua District, Nanjing, China, using an age-stratified random sampling procedure. A questionnaire totalling 117 items was sent to be completed by the corresponding parents or legal guardians of each eligible child. Comprehensive eye examinations, including visual acuity, anterior segment examination, autorefraction, cover test and ocular motility, were conducted. Postcycloplegic refraction and fundus examinations were performed if necessary.

Results Amblyopia was present in 68 children (1.20%, 95% CI 0.92% to 1.48%), with no statistical differences in gender (p=0.903) and age (p=0.835). Among these, 27 had bilateral amblyopia and 41 had unilateral amblyopia, including 26 anisometropic without strabismus, 26 binocular refractive, 7 strabismic, 6 combined strabismic/anisometropic and 3 deprivation amblyopia. Strabismus was found in 320 children (5.65%, 95% CI 5.05% to 6.25%), including 43 with concomitant esotropia, 259 with concomitant exotropia (1 esotropia at near but exotropia at distance), 8 with microtropia (3 esotropia and 5 exotropia), 10 with pure vertical strabismus (3 dissociated vertical deviation and 7 oblique muscle dysfunction) and 1 with Type I Duane syndrome. The prevalence of strabismus had no statistical differences in gender (p=0.952), but had significant statistical differences between different age groups (p=0.021).

Conclusions The prevalence of amblyopia and strabismus in preschool children in Eastern China were 1.20% and 5.65%, respectively. The refractive and strabismus are the main factors associated with amblyopia.

  • Child health (paediatrics)
  • Epidemiology
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Introduction

Amblyopia and strabismus are two major visual development disorders in childhood, which could persist into adulthood unless successfully treated. Amblyopia, a leading cause of paediatric vision impairment,1–3 is believed to develop during critical maturation of the visual system following abnormal binocular interaction or visual deprivation. And individuals with unilateral amblyopia from childhood have greater lifetime risk of eventual bilateral visual impairment and age-related macular degeneration development.4 ,5 This visual deficit is potentially reversible; earlier detection and younger age of initial treatment can achieve better visual acuity (VA) outcomes.6 ,7 Strabismus is a condition in any misalignment of the eyes in coordination between the extraocular muscles, adversely affecting the binocularity, stereopsis and depth of perception. In children, strabismus is a common contributing factor to amblyopia. In addition, strabismus affects normal binocular vision function even in the absence of amblyopia,8 subsequently affecting daily physiological and psychosocial performance unless successfully treated.9 ,10

Epidemiological data on the prevalence of amblyopia and strabismus, especially in population-based studies, will help in evaluating the screening results for ocular diseases, improving screening strategies and guiding rational allocation of medical resources. The prevalence of amblyopia and strabismus have been estimated in preschool and school-age populations globally, including the Multi-Ethnic Pediatric Eye Disease Study (MEPEDS);11 ,12 the Baltimore Pediatric Eye Disease Study (BPEDS);13 and the Strabismus, Amblyopia, and Refractive Error in Singaporean Children Study (STARS).14 With similar study design and diagnostic criteria, these studies reported rates ranging from 0.8% to 2.6% for amblyopia and 0.8% to 3.5% for strabismus in their different samples.11–14 Nevertheless, these studies are poor representation for the Chinese mainland population, especially in Eastern China. This cross-sectional and population-based study was carried out to assess the prevalence of amblyopia and strabismus in a representative sample of 36- to 72-month-olds in Eastern China. This analysis is part of the Nanjing Pediatric Vision Project (NPVP).

Methods

Study design and population

NPVP was a cross-sectional, population-based cohort study conducted from 2011 to 2012 in Yuhua District, Nanjing, China, using an age-stratified random sampling procedure. All procedures were reviewed and approved by the local institutional ethical review board in accordance with the Declaration of Helsinki principles. Written informed consent was obtained from all parents before the examinations. Selection of preschools in Yuhua District of Nanjing was based on the protocol of population-based survey: the Refractive Error Study in Children, which was developed for school-aged children and has been used in Nepal,15 China,16 ,17 Chile,18 India19 and South Africa.20 According to geographical characteristics, all 43 preschools in Yuhua District were designed as sampling clusters with the size of 150 through 250, which was similar to a typical preschool population size in this area. That resulted in 48 clusters with an average population of 200. All the clusters were numbered according to their locations and were randomly selected using a random numbers table. For details, please see online supplementary method.

Parental questionnaire and eye examination

A questionnaire totalling 117 items was completed by corresponding parents or legal guardians of each eligible child. The questionnaire contained information about the child's birth, feeding and medical history, maternal obstetric history, parental age, education, smoking history and family history.

The comprehensive eye examination was performed by a team of two optometrists and two ophthalmologists who were trained and certified using standardised study protocols as described in the MEPEDS previously.21 The examination included distance VA, anterior segment examination, autorefraction, cover test at distance and near fixation, and ocular motility, were conducted. Postcycloplegic refraction and fundus examination were performed if necessary.

Distance VA was measured using the Early Treatment Diabetic Retinopathy Study VA chart at a distance of 4 m, with or without spectacles. For children with initial VA worse than 20/40 or two-line interocular difference, cycloplegic refraction was performed to obtain best corrected VA (BCVA). If glasses were worn, testing was performed both with and without correction.

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 distances (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. If strabismus was suspected, a prism cover test was performed to detect the degree of eye misalignment.

All participants had the measurement of refractive error using an autorefractor under non-cycloplegic conditions. The refraction status of children who were found abnormal in the examinations of ocular alignment, ocular movement and distance VA, was further evaluated at least 30 min after cycloplegia with one drop of topical 1.0% cyclopentolate given twice 5 min apart.

Definition of amblyopia

As in the MEPEDS,11 ,12 ,21 unilateral amblyopia was defined as a two-line interocular difference in BCVA, with ≤20/32 in the worse eye and at least one of the following risk factors: past or present strabismus, previous strabismus surgery, anisometropia consistent with the worse eye such as spherical equivalent (SE) difference ≥3.00 dioptres (D) in myopia, ≥1.00 D in hyperopia or ≥1.50 D in astigmatism, and evidence of past or present visual axis obstruction (eg, congenital cataract, intraocular lens, aphakia, corneal opacity, ptosis or eyelid haemangioma).

Bilateral amblyopia was defined as bilateral subnormal BCVA <20/40 both in children aged 36–48 months and in those 48 months and older. This condition could be attributed to amblyopia factors, such as bilateral high ametropia (myopia ≥6.00 D, hyperopia ≥4.00 D or astigmatism ≥2.50 D) and evidence of past or present visual axis obstruction (see above). Children who meet the unilateral and bilateral amblyopia criteria were classified as unilateral amblyopia, similar to that used in the MEPEDS.11 ,12 ,21

Definition of strabismus

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, 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. Microstrabimus is defined as a deviation of less than 10 prism dioptres, in addition to binocular vision.

Data management and analysis

Statistical analyses were performed using the Statistic Product for Service Solution (SPSS) for Windows V.7.0 software (V.17.0, IBM, China). Age-specific and sex-specific prevalence rates for amblyopia and strabismus were calculated. Mixed models and generalised estimating equations were used to adjust for clustering within schools. χ2 tests and t tests with a 0.05 significance level were used when cluster effects were not significant. ORs and 95% CIs were also presented.

Results

Study population

Of the 5980 eligible preschool children, 5884 (98.39%) corresponding parents or legal guardians completed the questionnaire. Among them, 5862 (98.03%) preschool children participated in ocular examinations. After checking the data, 195 children (113 were males) were excluded as 15 with incomplete information and 180 beyond the age range of 36–72 months at the time of ocular examinations including 15 aged 32–35 months, 136 aged 73–75 months and 29 aged 76–80 months. The remaining 5667 subjects, with similar male and female were analysed for amblyopia and strabismus. The subjects aged from 36 to 72 months, with a mean age of 57.89±8.573 months. No statistical differences were observed between the males and females in each age group (p=0.971; see in table 1).

Table 1

Age and gender frequency distributions of the preschool children in the study

Prevalence of amblyopia

Based on the findings from the comprehensive eye examinations of the 5667 preschoolers, 68 children (1.20%, 95% CI 0.92% to 1.48%) were found with amblyopia, with 37 boys (1.23%, 95% CI 0.83% to 1.62%) versus 31 girls (1.17%, 95% CI 0.76% to 1.58%), no differences were observed in the prevalence of amblyopia in gender, with p=0.903. These 5667 preschoolers were divided into three groups by age, the prevalence of amblyopia in different age groups had no statistical difference, p=0.835 (see in table 2). Of the 68 amblyopia, 27 children (0.48%) had bilateral amblyopia and 41 (0.72%) had unilateral amblyopia, with 24 left eyes versus 17 right eyes in the latter. Of the 68 amblyopia, three children conformed to both unilateral and bilateral amblyopia diagnostic criteria, which were included in the unilateral amblyopia classification in this study, including two left eyes and one right eye.

Table 2

Prevalence of amblyopia in gender and different age groups

The results of the amblyopia analysis are shown according to pathogenic factors in table 3. Of the 41 unilateral amblyopia, 7 children were classified with strabismic amblyopia including 6 esotropia and 1 exotropia, 26 were anisometropic amblyopia including 16 SE anisohyperopia and 10 anisoastigmatism, 6 were combined strabismic/anisometropic amblyopia including 3 esotropia and 3 exotropia and 2 were deprivation amblyopia for unilateral congenital cataract. Of the 27 bilateral amblyopia, 26 children were refractive amblyopia and 1 was deprivation amblyopia with bilateral congenital cataract. The most two common types of amblyopia among all children were anisometropic without strabismus (38.24%; 26/68) and binocular refractive amblyopia (38.24%; 26/68), followed by strabismic (10.29%; 7/68) and combined strabismic/anisometropic amblyopia (8.82%, 6/68). In other words, the prevalence of amblyopia caused by the refractive factor was 85.29% (58/68), whereas 19.12% (13/68) was attributed to the strabismic factor in whole or in part; the former significantly leads to amblyopia more than the latter.

Table 3

Type of amblyopia

History and treatment of amblyopia

Based on the questionnaire information reported by the corresponding parents or legal guardians, 30 children had been previously diagnosed or treated as having amblyopia. Among which, 21 had been in prescription for spectacles and 9 had interrupted or terminated treatment before the examination (including 3 children who had a history of cataract extraction and intraocular lens implantation operation). Of the 30 children, 15 amblyopic children had been successfully treated according to the diagnostic criteria, with BCVA ≥20/40 and binocular vision difference of less than two lines.

Prevalence of strabismus

Based on the findings from the comprehensive eye examinations of the 5667 preschoolers, 320 children (5.65%, 95% CI 5.05% to 6.25%) found with strabismus, including 6 presenting normal position of the eyes but with exact histories of strabismus surgery (1 esotropia and 5 exotropia preoperative). Among the 320 strabismic children, 43 had concomitant esotropia, 259 had concomitant exotropia (1 esotropia at near but exotropia at distance), 8 had microtropia (3 esotropia and 5 exotropia), 10 had pure vertical strabismus (3 dissociated vertical deviation and 7 oblique muscle dysfunction) and 1 had Type I Duane syndrome. The most common type of strabismus among all children was intermittent exotropia (57.81%, 95% CI 49.48% to 66.14%; 185/320), followed by constant exotropia (23.13%, 95% CI 17.86% to 28.39%; 74/320) and constant esotropia (10.63%, 95% CI 7.05% to 14.20%; 34/320; see in figure 1).

Figure 1

Proportion of subtypes of strabismus.

The prevalence of strabismus in boys and girls were 5.66% (95% CI 4.84% to 6.49%) and 5.63% (95% CI 4.75% to 6.50%), concomitant esotropia were 0.83% (95% CI 0.50% to 1.15%) and 0.68% (95% CI 0.37% to 0.99%), concomitant exotropia were 4.57% (95% CI 3.83% to 5.32%) and 4.61% (95% CI 3.81% to 5.41%), respectively. No statistical differences in gender were observed, with p values of 0.952, 0.521 and 0.948, respectively. The children were divided into three groups by age; the prevalence of strabismus had significant statistical differences between different age groups (p=0.021). Further analysis showed no statistical difference in the prevalence of concomitant esotropia (p=0.408), but statistically significant in concomitant exotropia (p=0.027). These results from the strabismus analysis are shown in table 4.

Table 4

Prevalence of strabismus

Discussions

The prevalence of amblyopia in our population-based sample of 36- to 72-month-old preschool children from Yuhua District of Nanjing was 1.20%. Compared with 30- to 71/72-month-old children in the MEPEDS and BPEDS, some differences were observed in our study. First, bilateral amblyopia was defined as bilateral subnormal BCVA worse than 20/40 in children younger than 48 months in our study, but as BCVA worse than 20/50 in the MEPEDS and BPEDS.11–13 Second, children with a previous history of treatment for amblyopia were also included in the current study, even when they were normal by the time of examination. This demographic data for amblyopia was lower compared with those of the children aged 36 to 71/72 months old in the MEPEDS (1.63% in African–American, 2.79% in Hispanic/Latino, 1.76% in Asian and 2.00% in non-Hispanic white),11 ,12 the Australian children in the Sydney Paediatric Eye Disease Study ( 2.07%),22 and in the BPEDS (1.89% in white).13 However, our data were comparable with other Asian studies, such as the Singaporean Chinese children (1.19%).14 In addition, our rate is also similar to other studies in China, with 0.92% and 0.87% in Shunyi and Guangzhou,15 ,16 respectively. Unfortunately, both studies did not include deprivational amblyopia and used different criteria, so it is difficult to compare current study to them directly. Vision screening in preschooler children from the Yuhua district had been conducted earlier than other communities in China, early detection and intervention had achieved good outcomes, which would be a likely explanation for the relative lower prevalence of amblyopia. Parallel to our findings, no significant statistical difference of amblyopia in age or gender has been reported previously.10–14 ,22

In this study, the amblyopia caused by the refractive factor was 85.29%, whereas 19.12% was attributed to the strabismic factor in whole or in part; the former leads to amblyopia more than the latter. The result was consistent with the STARS and the MEPEDS in Hispanic/Latino children.10 ,14 By contrast, other studies in Britain23 and Australia24 reported that amblyopia in Caucasian population is attributed to strabismus more than refractive error. These differences may be due to the racial/ethnic effect, or to the lower prevalence of esotropia among Asian compared with Caucasian children; hence, further research is necessary. Strabismus was detected in 5.65% of our subjects, which was higher in comparison with the 36- to 71/72-month-old children in the MEPEDS (3.32% in African–American, 3.11% in Hispanic/Latino, 4.23% in non-Hispanic white and 4.64% in Asian),11 ,12 in the BPEDS (3.61% in white and 2.68% in African–American) and 0.97% in the Singaporean Chinese children.13 ,14 The MEPEDS reported 6.25% in 48 through 59 months and 5.30% in 60 through 72 months for Asian,12 compared with 5.9% in 60 through 71 months for whites in the BPEDS;13 hence, higher rates of strabismus in older population would be a reason for our rate higher than the other studies. Parallel to our findings, no significant statistical difference of strabismus was observed in gender from other studies.11–14 ,25 The prevalence of strabismus had significant statistical differences between three age groups (p=0.021), with more strabismus in old than in younger children, which was comparable with the MEPEDS.11 ,12 In regard to strabismus subtype, concomitant exotropia was almost six times as frequent as concomitant esotropia in 36- to 72-month-olds children in our study, which was consistent with findings from the STARS study of East Asian children,14 whereas the resultant in the MEPEDS and BPEDS was reversed.11–13 The cause of this difference is uncertain, and lower hyperopia rates in East Asian populations may be a possible explanation.26–28 As accommodative esotropia might be related to moderate or high hyperopia, decreasing incidence of hyperopic would result in less accommodative esotropia, thereby increasing the exotropia and esotropia ratio. Genetic and ethnic differences may be also partly responsible for this difference.12 ,29

Our study has several limitations. Small-angle strabismus and intermittent strabismus may have been missed given the nature of both conditions, especially in the setting of the study. This could have underestimated the prevalence of strabismus. Children undergoing ophthalmic care or with completely treated amblyopia were possibly absent in the current examination, which may also have led to the lower prevalence of amblyopia in our study. Inherent selection bias is the limitation of the study, which could potentially increase or decrease the incidence of amblyopia.

In conclusion, the prevalence of amblyopia and strabismus in preschool children in Eastern China were 1.20% (95% CI 0.92% to 1.48%) and 5.65% (95% CI 5.05% to 6.25%), respectively, with refractive and strabismus as the factors associated with amblyopia.

Acknowledgments

We thank the children, the corresponding parents or legal guardians and all the members of the Maternal and Child Healthcare Hospital of Yuhua District, Nanjing, China, for helpful advice and support.

References

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Supplementary materials

  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

Footnotes

  • XC, ZF and JY contributed equally.

  • Contributors Conceived and designed the experiments: HL, XC, JY and RY. Performed the experiments: HL, XC, HD, JB, JC, YG and HZ. Analysed the data: XC, ZF and JY. Contributed reagents/materials/analysis tools: HL and RY. Wrote the paper: XC and HL.

  • Funding This work was supported by the Science and Technology Projects in Nanjing (Grant No. 201001110); National Natural Science Foundation of China (Grant No. 81400435); Natural Science Foundation of Jiangsu Province (Grant No. BK20141027).

  • Competing interests None declared.

  • Patient consent Obtained.

  • Ethics approval the Institutional Review Board of Jiangsu Province Hospital.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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