Refractive Error, Visual Acuity and Causes of Vision Loss in Children in Shandong, China. The Shandong Children Eye Study
Refractive Error, Visual Acuity and Causes of Vision Loss in Children in Shandong, China. The Shandong Children Eye Study
     Abstract
     Purpose: To examine the prevalence of refractive errors and prevalence and causes of vision loss among preschool and
     school children in East China.
     Methods: Using a random cluster sampling in a cross-sectional school-based study design, children with an age of 4–
     18 years were selected from kindergartens, primary schools, and junior and senior high schools in the rural Guanxian
     County and the city of Weihai. All children underwent a complete ocular examination including measurement of
     uncorrected (UCVA) and best corrected visual acuity (BCVA) and auto-refractometry under cycloplegia. Myopia was defined
     as refractive error of #20.5 diopters (D), high myopia as #26.0D, and amblyopia as BCVA #20/32 without any obvious
     reason for vision reduction and with strabismus or refractive errors as potential reasons.
     Results: Out of 6364 eligible children, 6026 (94.7%) children participated. Prevalence of myopia (overall: 36.960.6%;95%
     confidence interval (CI):36.0,38.0) increased (P,0.001) from 1.761.2% (95%CI:0.0,4.0) in the 4-years olds to 84.663.2%
     (95%CI:78.0,91.0) in 17-years olds. Myopia was associated with older age (OR:1.56;95%CI:1.52,1.60;P,0.001), female gender
     (OR:1.22;95%CI:1.08,1.39;P = 0.002) and urban region (OR:2.88;95%CI:2.53,3.29;P,0.001). Prevalence of high myopia
     (2.060.2%) increased from 0.760.3% (95%CI:0.1,1.3) in 10-years olds to 13.963.0 (95%CI:7.8,19.9) in 17-years olds. It was
     associated with older age (OR:1.50;95%CI:1.41,1.60;P,0.001) and urban region (OR:3.11;95%CI:2.08,4.66);P,0.001).
     Astigmatism ($0.75D) (36.360.6%;95%CI:35.0,38.0) was associated with older age (P,0.001;OR:1.06;95%CI:1.04,1.09), more
     myopic refractive error (P,0.001;OR:0.94;95%CI:0.91,0.97) and urban region (P,0.001;OR:1.47;95%CI:1.31,1.64). BCVA was
     #20/40 in the better eye in 19 (0.32%) children. UCVA #20/40 in at least one eye was found in 2046 (34.05%) children, with
     undercorrected refractive error as cause in 1975 (32.9%) children. Amblyopia (BCVA #20/32) was detected in 44 (0.7%)
     children (11 children with bilateral amblyopia).
     Conclusions: In coastal East China, about 14% of the 17-years olds were highly myopic, and 80% were myopic. Prevalence of
     myopia increased with older age, female gender and urban region. About 0.7% of pre-school children and school children
     were amblyopic.
  Citation: Wu JF, Bi HS, Wang SM, Hu YY, Wu H, et al. (2013) Refractive Error, Visual Acuity and Causes of Vision Loss in Children in Shandong, China. The
  Shandong Children Eye Study. PLoS ONE 8(12): e82763. doi:10.1371/journal.pone.0082763
  Editor: Steven Barnes, Dalhousie University, Canada
  Received August 5, 2013; Accepted November 5, 2013; Published December 23, 2013
  Copyright: ß 2013 Wu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
  use, distribution, and reproduction in any medium, provided the original author and source are credited.
  Funding: This study was supported by Shandong Science & Technology Department (2011GGB14097, 2011GGH21835, 2012YD18081), Shandong Health
  Department (2011HD014), Jinan Science & Technology Bureau (201102061). The funders had no role in study design, data collection and analysis, decision to
  publish, or preparation of the manuscript.
  Competing Interests: The authors have declared that no competing interests exist.
  * E-mail: hongshengbi@126.com (HSB); jost.jonas@medma.ma.uni-heidelberg.de (JBJ)
Western China or Northern China far from the industrialized              Shandong and the relatively highly developed city of Weihai in
coastal regions of China [29,30]. One of the characteristics of          Eastern Shandong as study sites, since both differed markedly in
myopia in China is that its prevalence still appears to be               their level of social and economic development.
increasing, and in particular, that the prevalence of high myopia           A stratified cluster sampling method was applied. The sampling
is increasing even more markedly. It shows the importance of             frame was based on the enumeration of grade-specific classes
having updated recent data on the actual prevalence of myopia in         within the schools and kindergardens. Stratification of clusters by
the country. A recent study on university students in Shanghai/          grade and age ensured that all ages from 4 years to 18 years were
China and recent investigations on military conscripts in urban          representatively included into the study samples. The sample size
Seoul/Korea as well as in rural Korean regions revealed that more        was calculated by estimating an age-specific prevalence of
than 95% of the study populations were myopic, and that about            refractive errors of 33.5% with a 20% error rate and a 95%
10–20% were highly myopic (myopia refractive error .26                   confidence interval. Assuming a non-response rate of 10%, the
diopters) [31–33]. Also, there has been little information about         cluster sample size was 210 for each age, so that 3150 children
regional differences in the prevalence of myopia in China. We            with an age from 4 years to 18 years old of the two regions should
therefore conducted this study to examine the prevalence of              be enrolled into the survey. Since there were about 50 students per
myopia in a school-based investigation in the East Chinese               class, 127 classes were included. For each grade, the classes were
province of Shandong in a rural region and an urban area. Since          drawn by a simple random sampling and all students in these
myopia is associated with visual impairment, we additionally             classes were asked to participate in the study.
measured visual acuity and assessed the causes for visual                   Before the examinations were carried out, an interview was
impairment. Methods.                                                     performed using a standardized questionnaire to obtain informa-
                                                                         tion of the children’s family history, time spent doing outdoor
Methods                                                                  activities and indoor activities, study intensity, history of previous
                                                                         eye examinations and treatments, lifestyle, etc. The questionnaire
Ethics Statement                                                         was similar to the questionnaire used previously in the RESC
  The Ethics Board of the Eye Institute of the Shandong                  (Refractive Error Study in Children) studies [35,36]. The first step
University of Traditional Chinese Medicine and the local                 of the series of examinations consisted of the assessment of
Administration of the Education and School Board approved                uncorrected visual acuity (UCVA), for which a tumbling ‘‘E’’ chart
the study and informed written consent was obtained from the             (#600722, Good-Lite Co., Elgin, IL, USA) was used at a distance
parents or guardians of all children.                                    of 3 m. The lowest line of the chart and the eyes of the tested
  The Shandong Children Eye Study was a cross-sectional,                 children were approximately at the same height. The children
school-based study which was performed in the city of Weihai in          were asked to start with the upper first line (visual acuity: 20/100)
the most Eastern part, and in the county of Guanxian in the most         of the chart, and to continue with the next lines, if at maximum
Western part of the coastal province of Shandong in East China.          one character of the line was incorrectly described. When the
According to the data from the census of 2010, the total                 children falsely described at least 2 characters in the line, visual
population of the city of Weihai was 2,804,800, and the total            acuity was recorded as the value of the previous line. If the
population of the rural region of Guanxian was 764,900 [34]. In          children could not read the 20/100 line at a distance of 3m, the
an attempt to cover the whole range of socioeconomic back-               test was repeated at a distance of 1m. If at that distance no line
ground, we chose the rural county of Guanxian in Western                 could be read, visual acuity was tested as counting fingers, hand
Table 1. Enumerated and Examined Population Stratified by Age in the Shandong Children Eye Study.
doi:10.1371/journal.pone.0082763.t001
Figure 1. Distribution of the refractive error (spherical equivalent) of right eyes, stratified by age and gender in the Shandong
Children Eye Study.
doi:10.1371/journal.pone.0082763.g001
movement, light perception or no light perception. In a second              ,20/20 underwent a repeated ophthalmoscopical examination in
step, auto-refractometry was performed (KR-8900, Topcon,                    medical mydriasis.
Itabashi, Tokyo, Japan). Each eye was measured at least 3 times.               Refractive errors were defined as suggested by the Refractive
The difference between the maximum and minimum value of the                 Error Study in Children (RESC) surveys [35–36]. Myopia and
measurements of spherical refractive error and cylindrical                  hyperopia were calculated as spherical equivalent of the refractive
refractive error had to be less than 0.5 D, otherwise the                   error, defined as the sum of the spherical refractive error plus half
measurements had to be repeated. If UCVA was less than 20/                  of the cylindrical refractive error (measured as minus values).
20, best corrected visual acuity (BCVA) was measured in a third             Myopia was defined per subject as refractive error (spherical
step of the examination. For that purpose, the results of auto-             equivalent) of #20.50D in one or both eyes. High myopia was
refractometry were used as basis. To assure the quality for the             defined as refractive error #26.0D in one or both eyes. Mild
measurements of visual acuity and refractometry, the examiners              hyperopia was defined as a refractive error of .+0.50D to
were repeatedly checked for the accuracy of their results.                  #+2.0D, and medium to marked hyperopia was defined as a
Intraocular pressure was measured by a non-contact tonometer                refractive error of .+2.0 D, in one or both eyes if neither eye was
(CT-80A, Topcon, Co., Tokyo, Japan). An ophthalmologist                     myopic. Emmetropia was consequently considered to be a
examined the anterior and posterior ocular segments of all                  refractive error of .20.50D and #+0.50D in both eyes.
children. After ensuring that there was no risk for a medical               Astigmatism was a cylindrical refractive error $0.75D in either
mydriasis, cycloplegia was performed. Cycloplegia was achieved              eye. Anisometropia was defined as difference between right eye to
by using 1% cyclopentolate eye drops (Alcon, Ft. Worth, Texas,              left eye in refractive error (spherical error) of $1.0D. All refractive
USA). After an initial topical anesthesia with one drop of 0.4%             errors were measured under cycloplegia.
oxybuprocaine (Santen Co., Shiga, Japan) for each eye, three                   The reasons for a reduced UCVA were assessed by refractom-
drops of 1% cyclopentolate were instilled in intervals of 5 minutes.        etry and by the ophthalmological examination. Amblyopia was
About 30 minutes after the last drop instillation, a repeated               present if BCVA could not be improved to more than 20/32, if no
autorefractometry was performed. If a pupil diameter of at least            other reason such as cataract could be detected as cause for the
6 mm was not achieved, another drop of cyclopentolate was given             reduction in BCVA, and if factors such as strabismus, hyperopia,
and the examination was repeated 10 minutes later. Less than                myopia or anisometropia could explain amblyopia. If these
10% of the children needed an additional drop of cyclopentolate             conditions did not prevail, a reduced BCVA was considered to
due to an initially insufficient pupillary mydriasis and cycloplegia.       be unexplained. The same definition of amblyopia was applied by
To assess the causes for visual impairment, children with a BCVA            in the study by Negrel and colleagues [38].
Figure 2. Distribution of the refractive error (spherical equivalent) of right eyes, stratified by age and region of habitation, in the
Shandong Children Eye Study.
doi:10.1371/journal.pone.0082763.g002
   Statistical analysis was performed using a commercially                 (3186 (52.9%) boys) with a mean age of 9.763.3 years (range 4 to
available statistical software package (SPSS for Windows, version          18 years) (Table 1). Out of the 6026 children, 3112 children lived
21.0, IBM-SPSS, Chicago, IL). In a first step, we examined the             in the rural Guanxian County (51.6%) and 2914 children came
mean values (presented as mean 6 standard deviation). Frequen-             from the city of Weihai (48.4%). Except for a boy with phthisis
cies were presented as mean 6 standard error. In a second step,            bulbi in his left eye, all children underwent bilateral cycloplegic
we performed a univariate binary regression analysis with the              refractive error measurements.
presence of myopia (or of hyperopia) as dependent parameter and               The mean spherical equivalent of the right eyes was
one of the ocular parameters or one of the general parameters as           20.2262.06 D (median: 0.38 D; range: 211.75D to +10.5D)
independent parameter. In a third step, we carried out a                   and of the left eyes 20.1362.05 D (median: 0.50 D; range:
multivariate binary regression analysis, with the presence of              211.75D to +11.25D). The mean spherical equivalent of the
myopia (or of hyperopia) as the dependent variable and all those           worse eye was 20.1862.11 D (median: 0.50 D; range: 211.75D
parameters as independent parameters which were significantly              to +11.25D).
associated with the dependent variable in the univariate analysis.            Prevalence of myopia was overall 36.960.6% (95%CI: 36.0,
For continuous variables such as refractive error, we first                38.0). The prevalence of myopia increased from 1.761.2%
performed a univariate analysis to search for associations. We             (95%CI: 0.0, 4.0) in the 4 years old children to 84.663.2%
then carried out a multivariate linear regression analysis including       (95%CI: 78.0, 91.0) in 17-year olds (Fig. 1, 2, 3). In univariate
those variables which were significantly associated with the               analysis, prevalence of myopia was significantly associated with
continuous variable in the univariate analysis. Odds ratios (OR)           female gender (P,0.001) and urban region of habitation
and 95% confidence intervals (95%CI) were calculated. All P-               (P,0.001) (Fig. 1, 2). We then performed a multivariate analysis
values were 2-sided and were considered statistically significant          (binary regression analysis) with presence of myopia as dependent
when the values were less than 0.05.                                       variable and age, gender and region of habitation as independent
                                                                           parameters. It revealed that the presence of myopia was
Results                                                                    significantly associated with older age (OR: 1.56 (95%CI: 1.52,
                                                                           1.60); P,0.001), female gender (OR: 1.22 (95%CI: 1.08, 1.39);
   Out of the 6364 children who were primarily eligible for the            P = 0.002) and region of habitation OR: 2.88 (95%CI: 2.53,
study, 328 refused the examination and 10 children who had an              3.29); P,0.001).
intraocular pressure of more than 25 mmHg in one or both eyes                 The prevalence of high myopia was 2.060.2%. It increased
were excluded from the survey to avoid any risk associated with            significantly from 0% in the 4-years old, to 0.760.3% (95%CI:
cycloplegia. The study eventually included 6026 (94.7%) children           0.1, 1.3) in the 10-years olds, to 5.961.3% (95%CI: 3.4, 8.4) in the
Figure 3. Prevalence of Medium to Marked Hyperopia (.+2.0 Diopter (D)), Mild Hyperopia (.+0.50D to #+2.0D), Emmetropia, Mild
Myopia (#20.50D) and High Myopia (#26.0D) Stratified by Age in the Shandong Children Eye Study.
doi:10.1371/journal.pone.0082763.g003
14-years olds, and to 13.963.0 (95%CI: 7.8, 19.9) in the 17-years       lence of high myopia remained significantly associated with older
olds (Tables 2, 3, 4) (Fig. 4). Prevalence of high myopia was           age (OR: 1.50 (95%CI: 1.41, 1.60); P,0.001) and region of
additionally associated with female gender (P,0.001) and urban          habitation (OR: 3.11 (95%CI: 2.08, 4.66); P,0.001), while gender
region of habitation (P,0.001). In multivariate analysis, preva-        was no longer significantly (P = 0.25) associated.
Figure 4. Prevalence of High Myopia (Defined as Refractive Error #26.0 Diopters) Stratified by Age and Region of Habitation in the
Shandong Children Eye Study.
doi:10.1371/journal.pone.0082763.g004
6
                                               16           136       18       13.2            114      83.8 (77.0–89.4)   9     6.6(3.2–11.6)     2    1.5(0.2–4.5)      73      53.7 (45.3–61.9)   21    15.4 (10.0–22.1)
                                                                               (8.2–19.6)
                                               17           130       18       13.8            110      84.6 (77.8–90.1)   9     6.9(3.4–12.1)     0    2                 64      49.2 (40.7–57.8)   24     18.5 (12.4–25.7)
                                                                               (8.6–20.5)
                                               18           107       3        2.8 (0.7–7.1)   86       80.4 (72.2–87.1)   8     7.5(3.5–13.5)     3    2.8(0.7–7.1)      60      56.1(46.6–65.3)    18    16.8 (10.6–24.7)
                                               doi:10.1371/journal.pone.0082763.t002
                                                                                                                                                                                                                               Refractive Error in Shandong
        Table 3. Prevalence (95% confidence intervals) of high myopia, myopia, hyperopia, astigmatism, and anisometropia as measured under cycloplegia among children with an age
                                                                                                                                                                                                                                                                                                                                                                                              The prevalence of mild hyperopia was 42.8% (95%CI: 41.5,
                                                                                                                                                                                                                                                                                                                                                                                           44.0). In univariate analysis, it decreased significantly with older
Prevalence
                                                                                                                                                                                                                                       6.5 (5.6–7.4)
                                                                                                                                                                                                                                                          7.5 (6.6–8.5)
                                                                                                                                                                                                                                                                                      6.1 (5.3–7.0)
                                                                                                                                                                                                                                                                                                         7.9 (7.0–8.9)
                                                                                                                                                                                                                                                                                                                            7.0 (6.4–7.7)
                                                                                                                                                                                                                                                                                                                                                                                           age (P,0.001), urban region of habitation (P,0.001) and female
                                                                                                                                                                                                                                                                                                                                                                                           gender (P,0.001). In binary regression analysis, prevalence of
                                                                                                                                                                                                 Anisometropia
                                                                                                                                                                                                                                                                                                                                                                                           mild hyperopia remained significantly associated with younger age
                                                                                                                                                                                                                 (%)
                                                                                                                                                                                                                                                                                                                                                                                           (OR: 0.72 (95%CI: 0.70, 0.73); P,0.001), rural region of
                                                                                                                                                                                                                                                                                                                                                                                           habitation (OR: 0.58 (95%CI: 0.52, 0.64); P,0.001) and male
                                                                                                                                                                                                                                       206
                                                                                                                                                                                                                                                          214
                                                                                                                                                                                                                                                                                      189
                                                                                                                                                                                                                                                                                                         231
                                                                                                                                                                                                                                                                                                                            420
                                                                                                                                                                                                                                                                                                                                                                                           gender (OR: 0.83 (95%CI: 0.75, 0.92); P,0.001).
                                                                                                                                                                                                                      n
                                                                                                                                                                                                                                                                                                                                                                                              The prevalence of medium to marked hyperopia was 5.8%
                                                                                                                                                                                                                                                                                                                                                                                           (95%CI: 5.2, 6.4). In univariate analysis, it decreased significantly
                                                                                                                                                                                                                      Prevalence (%)
                                                                                                                                                                                                                                       35.4 (33.8–37.1)
                                                                                                                                                                                                                                                          37.3 (35.5–39.1)
                                                                                                                                                                                                                                                                                      32.1 (30.5–33.8)
                                                                                                                                                                                                                                                                                                         40.7 (39.0–42.5)
                                                                                                                                                                                                                                                                                                                            36.3 (35.1–37.5)
                                                                                                                                                                                                                                                                                                                                                                                           with older age (P,0.001) and urban region of habitation
                                                                                                                                                                                                                                                                                                                                                                                           (P = 0.04). It did not differ significantly (P = 0.91) between boys
                                                                                                                                                                                                                                                                                                                                                                                           and girls. In binary regression analysis, prevalence of medium to
                                                                                                                                                                                                 Astigmatism
                                                                                                                                                                                                                                                                                      1000
                                                                                                                                                                                                                                                                                                         1187
                                                                                                                                                                                                                                                                                                                            2187
                                                                                                                                                                                                                                                                                                                                                                                              Astigmatism was found in 36.360.6% (95%CI: 35.0, 38.0). Its
                                                                                                                                                                                                                      n
                                                                                                                                                                                                                                                                                      199
                                                                                                                                                                                                                                                                                                         151
                                                                                                                                                                                                                                                                                                                            350
                                                                                                                                                                                                                                       44.9(43.2–46.7)
                                                                                                                                                                                                                                                          40.3(38.5–42.1)
                                                                                                                                                                                                                                                                                      49.2(47.5–51.0)
                                                                                                                                                                                                                                                                                                         35.9(34.2–37.6)
                                                                                                                                                                                                                                                                                                                            42.8(41.5–44.0)
                                                                                                                                                                                                                                                                                      1531
                                                                                                                                                                                                                                                                                                         1046
                                                                                                                                                                                                                                                                                                                            2577
                                                                                                                                                                                                                                                                                                                                                                                           older age (OR: 1.22 (95%CI: 1.19, 1.26); P,0.001) and urban
                                                                                                                                                                                                                                                                                                                                                                                           region (OR: 1.55 (95%CI: 1.26, 1.90); P,0.001), while it was no
                                                                                                                                                                                                                      Prevalence (%)
                                                                                                                                                                                                                                                                                      30.7 (29.1–32.3)
                                                                                                                                                                                                                                                                                                         43.5 (41.7–45.3)
                                                                                                                                                                                                                                                                                                                            36.9(35.6–38.1)
                                                                                                                                                                                                                                                                                                                                                                                           (Table 5). Out of these 6008 children, 1628 (27.1%) children had
                                                                                                                                                                                                                                       1079
                                                                                                                                                                                                                                                          1142
                                                                                                                                                                                                                                                                                                         1267
                                                                                                                                                                                                                                                                                                                            2221
                                                                                                                                                                                                                                                                                      954
                                                                                                                                                                                                                                       1.6 (1.2–2.0)
                                                                                                                                                                                                                                                          2.4 (1.8–3.0)
                                                                                                                                                                                                                                                                                      1.3 (0.9–1.7)
                                                                                                                                                                                                                                                                                                         2.7 (2.1–3.3)
                                                                                                                                                                                                                                                                                                                            2.0 (1.6–2.3)
(%)
                                                                                                                                                                                                                                                                                      40
                                                                                                                                                                                                                                                                                                         78
                                                                                                                                                                                                                      n
                                                                                                                                                                                                                                                                                      3111
                                                                                                                                                                                                                                                                                                         2914
                                                                                                                                                                                                                                                                                                                            6025
                                                                                                                                                                                                                                                                             Region
                                                                                                                                                                                                                                                          Female
                                                                                                                                                                                                                                                                                                                                                                                           had a BCVA of #20/40 in the better eye, and there was no child
                                                                                                                                                                                                                                                                                                                                                                                           with a BCVA #20/200 in the better eye. BCVA was significantly
 Table 4. Mean refractive error (mean 6 standard deviation) in the Shandong Children Eye Study stratified by age, gender and
 region of habitation (n: Number of children).
Table 4. Cont.
doi:10.1371/journal.pone.0082763.t004
higher in the urban region of habitation (P,0.001) and did not             Greater Beijing giving another example for the increased
differ significantly (P = 0.49) between boys and girls. Amblyopia          prevalence of myopia across the generations [42]. Correspond-
(defined as BCVA #20/32, explained by factors such as                      ingly, a recent study from Beijing showed that the refractive error
strabismus or refractive errors, and no morphological reason for           of children at the age of 11 years was similar to that of their
BCVA reduction) was the reason for reduced visual acuity in 44             parents, while children at the age of 18 years were up to 2.0 D
children (2.15% of the 2046 or 0.73% of the total study                    more myopic than their parents [43].
population), with 11 children having bilateral amblyopia. Nine                The prevalence of high myopia of 13.9% in the 17-year-old
of these children had bilateral hyperopia and two children were            children of our study was higher than in most previous children
highly myopic in both eyes with a myopic refractive error of               studies, and it was markedly higher than in the Beijing Eye Study
#27.38 D and #211.00 D in both eyes, respectively. In 33                   on adults (2.6%; 95%CI: 2.2, 3.1). Interestingly, the prevalence of
children, amblyopia was unilateral with hyperopia being the cause          high myopia showed a particular pattern, with the prevalence of
in 10 children and anisometropia in 23 children. Other causes of           high myopia starting to increase around the age of 10–12 years
reduced vision were congenital cataract, corneal opacity due to            (Fig. 3). This pattern has also been previously reported from
keratitis, lens injury, bilateral optic nerve atrophy and unilateral       Taiwan and from Guangzhou, and Xiang and colleagues have
phthisis bulbi. Visual impairment in 28 eyes of 22 children                suggested that it should be called ‘‘acquired high myopia’’, because
remained unexplained.                                                      the age of onset roughly corresponded to the time it would take for
                                                                           early onset myopia to progress to high myopia [23,44,45].
Discussion                                                                    Since the prevalence of high myopia increased with older age,
                                                                           one can assume that that the prevalence of high myopia in the
   Our school-based study was performed in a rural region and in
                                                                           school children of our study will further increase when the children
a city in the East Chinese province of Shandong. The overall
prevalence of myopia was 36.960.6% and increased from                      get older. It agrees with the high prevalence of high myopia of
1.761.2% in the 4 years olds to 84.663.2% in 17-year olds.                 20% found in recent studies on university students in Shanghai
Prevalence of myopia was associated with female gender, urban              and on military conscripts in urban and rural Korea [31–33].
region of habitation and increasing age. The prevalence of high            Since high myopia can lead to vision threatening ocular disorders,
myopia was 2.060.2% and increased from 0.760.3% in 10-years                the impact of myopia on Public Health in China will therefore
olds to 13.963.0 in the 17-years olds. As myopia in general, high          markedly increase. In the adult population in China, degenerative
myopia was associated with urban region but not with gender.               myopia is responsible for one third of the causes of visual
Astigmatism was found in 36.360.6% of the children, and it was             impairment and is second only to cataract [1].
associated with older age, urban region and more myopic                       Out of 6008 children, 2046 (34.05%) children had an UCVA of
refractive error. Anisometropia was detected in 7.060.3% of the            #20/40 in at least one eye, with refractive error being the cause in
study population in association with older age and urban region.           1975 (32.9%) children. This prevalence of 32.9% of refractive
   These results agree with previous population-based and school-          error as cause for UCVA was comparable to the figures found in
based investigations in China documenting a marked increased               the recent Global Burden of Disease Study, in which refractive
prevalence of myopia in the younger generation [22–27]. It is in           error was the most common cause for UCVA [46]. Among the
contrast to other countries such as Laos, Iran, South Africa,              causes for a reduced BCVA, amblyopia was the most common one
Morocco, Brazil and Poland and Scandinavian countries, in which            in our study population, although the prevalence of amblyopia was
either no increased prevalence of myopia or a considerably less            relatively low (0.73%). The prevalence of amblyopia of 0.73% in
marked increase in the prevalence of myopia has been reported              our study population was in agreement with the prevalence of
[5,8,11–18,21,40,41]. The prevalence of low to medium myopia               0.8% found in the Singaporean Preschoolers Study [47].
was markedly higher in the present Shandong Children Eye Study                UCVA strongly decreased with older age in our study
than in the previous study on adults in the neighboring region of          population. It confirms the recent study by Xiang and colleagues
 Table 5. Distribution of uncorrected and best corrected visual acuity in each visual acuity category, given in number, percentage
 and 95% confidence interval (CI).
Visual Acuity Category Uncorrected Visual Acuity Best Corrected Visual Acuity
doi:10.1371/journal.pone.0082763.t005
who estimated the prevalence of myopia based on reduced                                   prevalence of astigmatism in our study population was relatively
unaided visual acuity in Chinese school children in Guangzhou                             high, with higher rates reported only in studies from Singapore
over the past 20 years [39]. They found that in 1988, over 80%                            and Guangzhou [10,23]. Potential limitations of our study should
of children in grade 1 (age 6 years) and about 30% in Grade 12                            be mentioned. Firstly, Shandong providence in coastal East China
(age 17 years) had normal UCVA. By 2007, these figures                                    is not representative of China as a whole, although our study
dropped to only 60% in grade 1 and about 10% in Grade 12. In                              included an urban part and a rural region. Shandong is
the period from 2003 to 2007, the figures remained unchanged                              economically less developed than the metropolitan regions of
at both the grade 1 and grade 12 levels. The authors concluded                            Beijing, Shanghai and Guangzhou, and it is better developed than
that the prevalence of reduced UCVA increased markedly in                                 the provinces of Inner Mongolia or Western China. Secondly, our
children from Guangzhou over the last 20 years, but stabilized in                         investigation was a cross-sectional study which did not allow
the past few years.                                                                       drawing conclusions on a longitudinal course and causal
   The overall prevalence of mild hyperopia and medium to                                 relationship between parameters. Any statement about an increase
marked hyperopia in our study was 42.8% and 5.8% respectively,                            in the prevalence of myopia in our study was therefore meant only
and as a corollary to the prevalence of myopia, it decreased with                         in a cross sectional manner when comparing younger children
older age (Fig. 3). Again as a corollary to the prevalence of myopia,                     with older children. Thirdly, in a similar manner, the comparison
the prevalence of hyperopia overall was associated with younger                           in the prevalence of myopia in children from Shandong with the
age and rural region of habitation. The decrease in the prevalence                        prevalence of myopia in adults from Beijing is not quite correct in
of hyperopia overall and the increase in the prevalence of myopia                         view of the different locations. The comparison of the data from
with increasing age of the children as found in our study                                 the children from Shandong with the data from the adults from
population from Shandong was similar to changes as described                              Beijing however is however in agreement with the comparison
by Morgan and colleagues in the Guangzhou ‘‘Refractive Error                              from children and adults in Beijing and from children and adults
Study in Children’’ study [37]. Interestingly and in contrast to                          in Guangzhou [23,26,48,49], although also in the latter compar-
myopia, hyperopia overall was not significantly correlated with                           isons, issues about longitudinal changes remained resolved.
gender in our study.                                                                      Fourthly, although the response rate in our study to participate
   Astigmatism was detected in 36.3% of the children in our                               in the cycloplegic examination was relatively high with 94.7%, the
survey. Its mean amount was 0.4360.51 diopters. It was                                    group of 18-years old teenagers had a relatively low response rate
associated with older age and more myopic refractive error. The                           of 70.4% (Table 1). It may have been the reason why the
Table 6. Causes of Uncorrected Visual Acuity (#20/40) in the Shandong Children Eye Study.
 *: % refers to the total group of children with uncorrected visual acuity of #20/40 (n = 2046 children).
 doi:10.1371/journal.pone.0082763.t006
prevalence of high myopia was considerably lower in the 18-years                                 In conclusion, in coastal East China, about 14% of the 17-years
old group than in the 17-years old group (13.8% (95%CI: 8.6,                                  olds were highly myopic, and 80% were myopic. Prevalence of
20.5) versus 2.8% (0.7, 7.1), so that we mainly reported on the                               myopia increased with older age, female gender and urban region.
prevalence of high myopia in the 17-years old children. Fifthly, our                          About 0.7% of pre-school children and school children were
study protocol was not completely consistent with the one applied                             amblyopic. The marked increase in the prevalence of myopia, in
by the Refractive Error Study in Children (RESC). We used a                                   particular of high myopia, in the young generation of China as
tumbling E chart, while the RESC used an ETDRS (Early                                         compared to elderly population groups will be of importance for
Treatment of Diabetic Retinopathy Study) Eye Chart. Sixthly,                                  future public health politics and warrants measures to prevent the
while school participation is, for all practical purposes, universal in                       development of myopia.
China, this is not true at the kindergarten level. There may
therefore have been a sampling bias in the 4 and 5 year-olds.                                 Author Contributions
Seventhly, we defined astigmatism as a cylindrical refractive error
                                                                                              Conceived and designed the experiments: JFW HSB SMW YYH HW WS
$0.75D in either eye. Since other studies used a cut-off value of                             TLL XRW JBJ. Performed the experiments: JFW HSB SMW YYH HW
1.00 diopters [6,26], differences in the prevalence of astigmatism                            WS TLL XRW. Analyzed the data: JFW HSB SMW YYH HW WS TLL
between our study and other investigations may also be due to the                             XRW JBJ. Contributed reagents/materials/analysis tools: HSB. Wrote the
difference in the definition of astigmatism.                                                  paper: JFW HSB SMW YYH HW WS TLL XRW JBJ.
References
 1. Xu L, Wang Y, Li Y, Wang Y, Cui T, et al. (2006) Causes of blindness and visual           21. French AN, Morgan IG, Burlutsky G, Mitchell P, Rose KA (2013) Prevalence
    impairment in an urban and rural area in Beijing: the Beijing Eye Study.                      and 5- to 6-year incidence and progression of myopia and hyperopia in
    Ophthalmology 113: 1134.e1–11.                                                                Australian schoolchildren. Ophthalmology 120: 1482–1491.
 2. Morgan IG, Ohno-Matsui K, Saw SM (2012) Myopia. Lancet 379: 1739–1748.                    22. Zhao J, Pan X, Sui R, Munoz SR, Sperduto RD, et al. (2000) Refractive Error
 3. Xu L, Wang Y, Wang S, Wang Y, Jonas JB (2007) High myopia and glaucoma                        Study in Children: results from Shunyi District, China. Am J Ophthalmol 129:
    susceptibility. The Beijing Eye Study. Ophthalmology 114: 216–220.                            427–435.
 4. Liu HH, Xu L, Wang YX, Wang S, You QS, et al. (2010) Prevalence and                       23. He M, Zeng J, Liu Y, Xu J, Pokharel GP, et al. (2004) Refractive error and
    progression of myopic retinopathy in Chinese adults: The Beijing Eye Study.                   visual impairment in urban children in southern China. Invest Ophthalmol Vis
    Ophthalmology 117: 1763–1768.                                                                 Sci 45: 793–799.
 5. Villarreal MG, Ohlsson J, Abrahamsson M, Sjöstrom A, Sjöstrand J (2000)                 24. Tong L, Saw SM, Chia KS, Tan D (2004) Anisometropia in Singapore school
    Myopisation: the refractive tendency in teenagers. Prevalence of myopia among                 children. Am J Opthalmol 137: 474–479.
    young teenagers in Sweden. Acta Ophthalmol Scand 78: 177–181.                             25. Fan DS, Lam DS, Lam RF, Lau JT, Chong KS, et al. (2004) Prevalence,
 6. Murthy GV, Gupta SK, Ellwein LB, Muñoz SR, Pokharel GP, et al. (2002)                        incidence, and progression of myopia of school children in Hong Kong. Invest
    Refractive error in children in an urban population in New Delhi. Invest                      Ophthalmol Vis Sci 45: 1071–1075.
    Ophthalmol Vis Sci 43: 623–631.                                                           26. He M, Huang W, Zheng Y, Huang L, Ellwein LB (2007) Refractive error and
 7. Naidoo KS, Raghunandan A, Mashige KP, Govender P, Holden BA, et al.                           visual impairment in school children in rural southern China. Ophthalmology
    (2003) Refractive error and visual impairment in African children in South                    114: 374–382.
    Africa. Invest Ophthalmol Vis Sci 44: 3764–3770.                                          27. Congdon N, Wang Y, Song Y, Choi K, Zhang M, et al. (2008) Visual disability,
 8. Villarreal GM, Ohlsson J, Cavazos H, Abrahamsson M, Mohamed JH (2003)                         visual function, and myopia among rural chinese secondary school children: the
    Prevalence of myopia among 12- to 13-Year- old schoolchildren in Northern                     Xichang Pediatric Refractive Error Study (X-PRES)–report 1. Invest Ophthal-
    Mexico. Optom Vis Sci 80: 369–373.                                                            mol Vis Sci 49: 2888–2894.
 9. Goh PP, Abqariyah Y, Pokharel GP, Ellwein LB (2005) Refractive error and                  28. You QS, Wu LJ, Duan JL, Luo YX, Liu LJ, et al. (2012) Factors associated with
    visual impairment in school-age children in Gombak District, Malaysia.                        myopia in school children in China: The Beijing Childhood Eye Study. PLoS
    Ophthalmology 112: 678–685.                                                                   One 7: 1–10.
10. Saw SM, Goh PP, Cheng A, Shankar A, Tan DT, et al. (2006) Ethnicity-specific              29. Pi LH, Chen L, Liu Q, Ke N, Fang J, et al. (2012) Prevalence of eye diseases and
    prevalences of refractive errors vary in Asian children in neighbouring Malaysia              causes of visual impairment in school-aged children in western China.
    and Singapore. Br J Ophthalmol 90: 1230–1235.                                                 J Epidemiol 22: 37–44.
11. Fotouhi A, Hashemi H, Khabazkhoob M, Mohammad K (2007) The prevalence                     30. Li Z, Xu K, Wu S, Lv J, Jin D, et al. (2013) Population-based survey of refractive
    of refractive errors among school-children in Dezful, Iran. Br J Ophthalmol 91:               error among school-aged children in rural northern china: the heilongjiang eye
                                                                                                  study. Clin Experiment Ophthalmol. 2013 Aug 16. doi: 10.1111/ceo.12198.
    287–292.
                                                                                                  [Epub ahead of print].
12. Czepita D, Zejmo M, Mojsa A (2007) Prevalence of myopia and hyperopia in a
                                                                                              31. Sun J, Zhou J, Zhao P, Lian J, Zhu H, et al. (2012) High prevalence of myopia
    population of Polish schoolchildren. Ophthalmic Physiol Opt 27: 60–65.
                                                                                                  and high myopia in 5060 Chinese university students in Shanghai. Invest
13. Salomao SR, Cinoto RW, Berezovsky A, Mendieta L, Nakanami CR, et al.
                                                                                                  Ophthalmol Vis Sci 53: 7504–7509.
    (2008) Prevalence and causes of visual impairment in low-middle income school
                                                                                              32. Jung SK, Lee JH, Kakizaki H, Jee D (2012) Prevalence of myopia and its
    children in Sao Paulo, Brazil. Invest Ophthalmol Vis Sci 49: 4308–4313.
                                                                                                  association with body stature and educational level in 19-year-old male
14. Ip JM, Huynh SC, Robaei D, Rose KA, Morgan IG, et al. (2008) Ethnic                           conscripts in Seoul, South Korea. Invest Ophthalmol Vis Sci 53: 5579–5583.
    differences in refraction and ocular biometry in a population-based sample of
                                                                                              33. Lee SJ, Urm SH, Yu BC, Sohn HS, Hong YS, et al. (2011) [The prevalence of
    11-15-year-old Australian children. Eye 22: 649–656.
                                                                                                  high myopia in 19 year-old men in Busan, Ulsan and Gyeongsangnam-do]. J
15. Anera RG, Soler M, de la Cruz Cardona J, Salas C, Ortiz C (2009) Prevalence                   Prev Med Public Health.;44: 56–64.
    of refractive errors in school-age children in Morocco. Clin Experiment                   34. http://www.stats.gov.cn/english/statisticaldata/censusdata/rkpc2010/indexch.
    Ophthalmol 37: 191–196.                                                                       htm; Assessed: May 27th, 2013.
16. Jamali P, Fotouhi A, Hashemi H, Younesian M, Jafari A (2009) Refractive errors            35. McKean-Cowdin R, Cotter SA, Tarczy-Hornoch K, Wen G, Kim J, et al.
    and amblyopia in children entering school: Shahrood, Iran. Optom Vis Sci 86:                  (2013) Prevalence of amblyopia or strabismus in Asian and Non-Hispanic white
    364–369.                                                                                      preschool children: Multi-Ethnic Pediatric Eye Disease Study. Ophthalmology
17. Yekta A, Fotouhi A, Hashemi H, Dehghani C, Ostadimoghaddam H, et al.                          120: 2117–2124.
    (2010) Prevalence of refractive errors among schoolchildren in Shiraz, Iran. Clin         36. Tarczy-Hornoch K, Cotter SA, Borchert M, McKean-Cowdin R, Lin J, et al.
    Experiment Ophthalmol 38: 242–248.                                                            (2013) Prevalence and causes of visual impairment in Asian and Non-Hispanic
18. Ostadimoghaddam H, Fotouhi A, Hashemi H, Yekta A, Heravian J, et al. (2011)                   white preschool children: Multi-Ethnic Pediatric Eye Disease Study. Ophthal-
    Prevalence of the refractive errors by age and gender: the Mashhad eye study of               mology 120: 1220–1226.
    Iran. Clin Experiment Ophthalmol 39: 743–751.                                             37. Morgan IG, Rose KA, Ellwein LB; Refractive Error Study in Children Survey
19. Casson RJ, Kahawita S, Kong A, Muecke J, Sisaleumsak S, et al. (2012)                         Group (2010) Is emmetropia the natural endpoint for human refractive
    Exceptionally low prevalence of refractive error and visual impairment in                     development? An analysis of population-based data from the refractive error
    schoolchildren from Lao People’s Democratic Republic. Ophthalmology 119:                      study in children (RESC). Acta Ophthalmol 88: 877–884.
    2021–2027.                                                                                38. Negrel AD, Maul E, Pokharel GP, Zhao J, Ellwein LB. Refractive error study in
20. O’Donoghue L, McClelland JF, Logan NS, Rudnicka AR, Owen CG, et al.                           children: sampling and measurement methods for a multi-country survey.
    (2013) Profile of anisometropia and aniso-astigmatism in children: prevalence                 Am J Ophthalmol 2000;129: 421–426.
    and association with age, ocular biometric measures, and refractive status. Invest        39. Xiang F, He M, Zeng Y, Mai J, Rose KA, et al. (2013) Increases in the
    Ophthalmol Vis Sci 54: 602–608.                                                               prevalence of reduced visual acuity and myopia in Chinese children in
      Guangzhou over the past 20 years. Eye (Lond) 2013 Sep 6. doi: 10.1038/                   45. Xiang F, He M, Morgan IG (2012) The impact of severity of parental myopia on
      eye.2013.194. [Epub ahead of print].                                                         myopia in Chinese children. Optom Vis Sci 89: 884–891.
40.   Fledelius HC (2000) Myopia profile in Copenhagen medical students 1996–98.               46. Murray CJ, Vos T, Lozano R, Naghavi M, Flaxman AD, et al. (2012) Disability-
      Refractive stability over a century is suggested. Acta Ophthalmol Scand 78: 501–             adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–
      505.                                                                                         2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet
41.   Midelfart A, Kinge B, Midelfart S, Lydersen S (2002) Prevalence of refractive                380: 2197–223.
      errors in young and middle-aged adults in Norway. Acta Ophthalmol Scand 80:              47. Chia A, Lin X, Dirani M, Gazzard G, Ramamurthy D, et al. (2013) Risk factors
      501–505.                                                                                     for strabismus and amblyopia in young Singapore Chinese children. Ophthalmic
42.   Xu L, Li J, Cui T, Hu A, Fan G, et al. (2005) Refractive error in urban and rural            Epidemiol 20: 138–147.
      adult Chinese in Beijing. Ophthalmology 112: 1676–1683.                                  48. He M, Huang W, Li Y, Zheng Y, Yin Q, et al. (2009) Refractive error and
43.   Liang YB, Lin Z, Vasudevan B, Jhanji V, Young A, et al. (2013) Generational                  biometry in older Chinese adults: the Liwan eye study. Invest Ophthalmol Vis
      difference of refractive error in the baseline study of the Beijing Myopia                   Sci 50: 5130–5136.
      Progression Study. Br J Ophthalmol 97: 765–769.                                          49. Liang YB, Lin Z, Vasudevan B, Jhanji V, Young A, et al. (2013) Generational
44.   Xiang F, He M, Morgan IG (2012) The impact of parental myopia on myopia in                   difference of refractive error in the baseline study of the Beijing Myopia
      Chinese children: population-based evidence. Optom Vis Sci 89: 1487–1496.                    Progression Study. Br J Ophthalmol 97: 765–769.