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01.12.2017 | Research article | Ausgabe 1/2017 Open Access

BMC Ophthalmology 1/2017

Near work, outdoor activity, and myopia in children in rural China: the Handan offspring myopia study

Zeitschrift:
BMC Ophthalmology > Ausgabe 1/2017
Autoren:
Zhong Lin, Tie Ying Gao, Balamurali Vasudevan, Kenneth J. Ciuffreda, Yuan Bo Liang, Vishal Jhanji, Su Jie Fan, Wei Han, Ning Li Wang
Wichtige Hinweise

Electronic supplementary material

The online version of this article (https://​doi.​org/​10.​1186/​s12886-017-0598-9) contains supplementary material, which is available to authorized users.
Abbreviations
CI
Confidence interval
GEEs
Generalized estimating equations
HES
Handan eye study
HOMS
Handan offspring myopia study
OR
Odds ratio
STARS
Strabismus, amblyopia and refractive error study
X-PRES
Xichang pediatric refractive error study

Background

Myopia is a common vision disorder. The prevalence of myopia in Chinese children living in China [ 1] was reported to be higher compared to children from Nepal, [ 2, 3] India, [ 4, 5] Singapore, [ 6, 7] Africa, [ 8] Chile, [ 9] Australia, [ 10, 11] the United States, [ 12] and England [ 13, 14].
Cross-sectional and longitudinal studies on Chinese urban children have found an association between near work/outdoor activity and myopia/myopic progression. [ 1524] Regarding Chinese rural children, Lu et al. [ 25] reported no association between either outdoor activity or near work with myopia in the Xichang Pediatric Refractive Error Study (X-PRES) in southern rural China. In contrast, Wu et al. reported that more frequent outdoor activity was associated with a lower prevalence of myopia in Taiwanese rural Chinese primary school children [ 26]. Interestingly, data from Chinese rural children are relatively rare and remain controversial.
Therefore, we conducted the Handan Offspring Myopia Study (HOMS), which aimed to assess the relationship between near work/outdoor activity and myopia in a rural population in northern China.

Methods

The HOMS, an offspring study of the Handan Eye Study (HES), primarily aimed to investigate the familial associations for myopia among parents and their offspring aged 6 to 18 years in rural northern China, as well as to assess the myopic shift between the two generations and its putative risk factors [ 27]. Subjects were drawn from the HOMS, which is a part of the offspring of HES [ 28]. The study design, procedures, and characteristics of HOMS are reported elsewhere [ 27]. In brief, the study was undertaken in a rural population in Yongnian County, Handan, which is located in southern Hebei province (about 500 km south of Beijing). This geographic area has demographic characteristics similar to other rural regions of China according to the 2000 National Census [ 28]. Thirteen villages were randomly selected for the HES. Among them, 6 villages with age of parents more than 30 years were selected for the HOMS. From March to June in 2010, 878 of 1238 children eligible for the HOMS (70.9% response rate), aged 6 to 18 years, were examined in the HOMS. There were 462 boys (52.6%) and 416 girls (47.4%), aged 10.4 ± 2.4 and 10.8 ± 2.6 years, respectively. All participants were self-identified Han people. In contrast to the non-participants, children who participated were more likely to be boys, younger, and studying or working near the villages. Information relating to the parents was obtained from the HES.
This study adhered to the Declaration of Helsinki. Written, informed consent was obtained from at least one parent/guardian. Ethics Committee approval was obtained from the Handan Eye Hospital.

Questionnaire

Each participant completed a standard, myopia-based questionnaire in a face-to-face interview by a trained staff member conducted in the local dialect of the study site. This questionnaire was used in the Sydney Myopia Study, and it was slightly modified and translated into Chinese [ 18, 20, 29]. The interview covered a broad range of questions regarding various daily activities. These activities were classified into near work, midworking distance, and outdoor activities. Near work activities were defined as those having less than a 50 cm working distance, including drawing pictures, doing homework, reading books, attending additional classes, and using handheld computers. Activities at the midworking distance included watching television, playing video games and using computers. Outdoor activities included leisure time spent outside (e.g., staying in the backyard, walking, riding a bike/scooter, going shopping) and outdoor sports (e.g., running, playing ball, skipping rope). Activity levels were graded as low, moderate, and high using population tertiles of the average daily hours spent on these different activities.

Cycloplegic refraction

Refraction was performed using an autorefractor (model KR8800, Topcon, Tokyo, Japan) before and after cycloplegia in the children. Cycloplegic autorefraction was performed 20 min after instilling 3 drops of cyclopentolate 1% (Cyclogyl, Alcon).Three readings were obtained in each eye, and the average was recorded. A fully dilated pupil was defined as one with a diameter of ≥6 mm and having absence of any pupillary light reflex.
Information relating to the parents was obtained from the HES database including non-cycloplegic autorefracion. All examinations were performed using the same protocols and equipment as the HES [ 30].

Data analysis and definitions

No imputations were done for the missing data. Only data from the right eye were used, since there was a high correlation in spherical equivalent (SE) between the right and left eye ( r pearson = 0.94, p < 0.001). Data were analyzed using commercial software (SAS ver. 9.1.3; SAS Institute, Cary, NC) with the significance level set at less than 0.05.
The SE was calculated as the sphere +1/2 cylinder. Myopia, emmetropia, and hyperopia were defined as SE < −0.5 diopters (D), −0.5D ≤ SE ≤0.5D, and SE > 0.5D, respectively [ 27, 30]. Average parental refractive error was defined as the combined average of the non-cycloplegic SE of the father and mother. Average daily hours of activities were presented as the mean ± standard deviation. The daily hours of activities were calculated using the formula: [(average hours spend on weekday) × 5 + (average hours spend on weekends) × 2)]/7. Diopter-hours were calculated using a cumulative near work exposure variable at the near and midworking distances using the formula: 3 × (reading for pleasure hours +study hours) + 2 × (computer hours + video games hours) + watching television hours [ 18, 20]. Activity level was first analyzed continuously as the average daily hours, and then by tertile activity groups. Generalized estimating equations (GEEs) were used to assess the association between the SE and daily activity/confounders (fixed effects), as well as considering the children from the same family (family effect) as a random effect. Parental educational level was categorized as the following: illiterate, primary school, junior high school, and senior high school and above. The joint effect of near work and outdoor activities, as well as family effect, using stepwise logistic regression models was performed after adjusting for the different risk factors using GEEs. Odds ratios (OR) and 95% confidence intervals (CIs) are presented.

Results

A total of 878 (70.9%) of 1238 children aged 6 to 18 years participated in this study. Of these, 598 with completed cycloplegic autorefraction, myopia questionnaire, and parental refractive information were included. Overall, 13 children with either amblyopia or strabismus, 1 child with previous corneal surgery, and 12 children’s parents with either amblyopia or strabismus were excluded. Hence, 572 (65.1%) of 878 children were included in the final analysis. There were 170, 132, 42, and 3 families with one, two, three, and four child(ren). No significant difference was found for the children’s age, prevalence of myopia, and SE between the included and excluded children ( p = 0.44, p = 0.65, and p = 0.63, respectively). However, there were more boys in the included children as compared to the excluded children ( p = 0.03) (Table 1). Fig.  1 presents the distribution of refractive error in children 6–11 years old and 12–17 years old.
Table 1
Characteristics of the included and excluded children
 
Included ( N = 572)
Excluded ( N = 306)
P
Age (years)
10.6 ± 2.5
10.5 ± 2.5
0.44
Gender (boys:girls)
316:256
146:160
0.03
Prevalence of myopia (%) a
     
 Boys
17.1
17.2
0.86
 Girls
32.8
27.3
0.12
 Total
24.1
22.6
0.65
Spherical equivalent (D) a
 Boys
0.15 ± 1.18
0.19 ± 1.44
0.81
 Girls
−0.17 ± 1.27
−0.24 ± 1.75
0.65
 Total
0.01 ± 1.23
−0.05 ± 1.63
0.63
aRefractive error data were missing in 24 boys and 17 girls in the excluded group
Children spent 4.8 ± 1.6 and 2.9 ± 1.4 h per day on near work and outdoor activity, respectively. Regarding the daily near work time in hours, boys and myopic children spent significantly more time on near work than either girls (4.9 ± 1.7 vs. 4.6 ± 1.5, p = 0.042) or non-myopic children (5.0 ± 1.7 vs. 4.7 ± 1.6, p = 0.049), respectively. Although there were significant differences among the paternal educational levels for near work time ( p = 0.018), no significant differences were found in the subsequent pair-wise comparisons. No significant differences were found among the other groups, e.g., number of myopic parents, maternal educational levels (Table  2). Regarding the daily outdoor activity time, only a borderline difference was found among the maternal education levels ( p = 0.054). No significant differences were found among the other groups for outdoor activity. The daily hours spent on mid-work distance activities were also not associated with the mean SE ( r spearman = −0.003, p = 0.94).
Table 2
Near work and outdoor activity time (hours per day) in Handan Offspring Myopia Study children
 
N
Near work
Outdoor
Mean ± SD
p value
Mean ± SD
p value
Gender
 Boys
316
4.9 ± 1.7
0.042 a
3.0 ± 1.4
0.12 a
 Girls
256
4.6 ± 1.5
 
2.8 ± 1.4
 
Refractive Status
 Myopia
138
5.0 ± 1.7
0.049 a
2.9 ± 1.3
0.38 a
 No myopia
434
4.7 ± 1.6
 
3.0 ± 1.4
 
Number of myopic parents
 None
197
4.6 ± 1.7
0.32 b
2.9 ± 1.3
0.74 b
 Either
272
4.9 ± 1.7
 
2.9 ± 1.4
 
 Both
103
4.7 ± 1.4
 
3.0 ± 1.5
 
Maternal education levels
 Illiteracy
87
4.7 ± 1.6
0.17 b
2.9 ± 1.2
0.054 b
 Primary school
279
4.6 ± 1.7
 
2.8 ± 1.3
 
 Junior high school
189
5.0 ± 1.5
 
3.2 ± 1.6
 
 Senior high school and above
17
4.8 ± 1.6
 
3.1 ± 1.4
 
Paternal education levels
 Illiteracy
21
5.4 ± 2.5
0.018 b
3.0 ± 1.1
0.38 b
 Primary school
166
4.6 ± 1.6
 
2.8 ± 1.4
 
 Junior high school
343
4.7 ± 1.5
 
3.0 ± 1.5
 
 Senior high school and above
42
5.3 ± 2.1
 
2.8 ± 1.3
 
Total
572
4.8 ± 1.6
 
2.9 ± 1.4
 
at-test
bgeneralized linear models
Table  3 and Table  4 present the mean SE of the children and their associations with daily activity hours, after being divided into tertile groups among the different subgroups. A high myopic refractive error was found in the fathers with the primary school education level subgroup if their children spent more time on near work ( p = 0.01). The combined effects of outdoor and near work activities on the odds for myopia are presented in Fig.  2. Children with a high level of outdoor activity and low level of near work were used as the reference group (OR 1.0). Children with moderate outdoor activity and high near work had higher odds for myopia than the reference group (OR, 2.16; 95% CI, 0.69–6.77). However, none of the other subgroups had significant odds for myopia compared to the reference group (Fig.  2).
Table 3
Mean spherical equivalent (diopter) a as a function of near work activity (tertiles of hours per day)
Near work activity (hours per day) b
Low (0~4.0) N = 185
Moderate (4.0~5.1) N = 196
High (>5.1) N = 191
P value
Gender
 Boys
0.33
0.08
0.06
0.17
 Girls
−0.15
−0.19
−0.20
0.96
Refractive Status
 Myopia
−1.73
−1.74
−1.80
0.95
 No myopia
0.63
0.52
0.53
0.25
Number of myopic parents
 None
0.09
−0.04
0.04
0.80
 Either
0.30
0.04
0.01
0.17
 Both
−0.29
−0.32
−0.46
0.89
Maternal education level
 Illiteracy
0.15
0.19
0.12
0.97
 Primary school
−0.01
−0.01
0.00
0.99
 Junior high school
0.39 c
−0.13
−0.04
0.06
 Senior high school and above
−1.30
−0.68
−0.85
0.88
Paternal education level
 Illiteracy
0.08
0.27
0.53
0.50
 Primary school
0.38 c
−0.11
−0.15
0.01
 Junior high school
−0.06
−0.05
0.04
0.78
 Senior high school and above
0.11
−0.01
−0.61
0.50
Total
0.10
−0.04
−0.06
0.35
aAdjusted for children’s age, gender, average parental refractive error, maternal and paternal education level, and outdoor activity time as fixed effects, and family effect as a random effect
bIncludes drawing, homework, reading, and handheld computer use. Cut-off points were based on population tertiles for average daily hours spent at near
cSignificant (Bonferroni test) compared with the highest tertile of activity as the reference group
Table 4
Mean spherical equivalent (diopter) a as a function of outdoor activity (tertiles of hours per day)
Outdoor activity (hours per day) b
Low (0~2.3) N = 191
Moderate (2.3~3.2) N = 187
High (>3.2) N = 194
P value
Gender
 Boys
0.05
0.10
0.27
0.32
 Girls
−0.13
−0.30
−0.10
0.49
Refractive Status
 Myopia
−1.69
−1.76
−1.84
0.82
 No myopia
0.54
0.53
0.61
0.52
Number of myopic parents
 None
0.03
−0.19
0.25
0.10
 Either
0.08
−0.01
0.26
0.24
 Both
−0.53
−0.09
−0.46
0.32
Maternal education level
 Illiteracy
0.16
−0.10
0.40
0.09
 Primary school
−0.09
−0.05
0.14
0.37
 Junior high school
0.01
−0.07
0.11
0.68
 Senior high school and above
0.11
−0.94
−1.68
0.52
Paternal education level
 Illiteracy
−0.01
0.22
0.54
0.62
 Primary school
0.07
−0.11
0.22
0.30
 Junior high school
−0.06
−0.11
0.10
0.31
 Senior high school and above
−0.27
−0.12
−0.25
0.97
Total
−0.04
−0.09
0.12
0.20
aAdjusted for children’s age, gender, average parental refractive error, maternal and paternal education level, and near work time as fixed effects, and family effect as a random effect
bIncludes outdoor sports, playing out of doors, and other outdoor leisure activities. Cut-off points were based on population tertiles for average daily hours spent outside
Stepwise multiple logistic models were used to analyze the correlation between daily near work/ outdoor activity hours and myopia (Table  5). In a univariate model, children who spent more time on near work were 1.12 (95% CI 1.01–1.25) times more likely to be myopic. However, no significant association between daily near work hours and myopia was found after adjusting for confounders, such as the children’s age, gender, average parental refractive error, parental education level, and daily outdoor activity hours. Outdoor activity had no protective effect for myopia (OR, 0.93; 95% CI, 0.82–1.07) in the univariate model. However, after adjusting for children’s age, gender, average parental refractive error, parental education level, and daily near work hours, outdoor activity showed a weak protective effect for myopia (OR, 0.82; 95% CI, 0.70–0.96).
Table 5
Stepwise logistic analysis of daily near work and outdoor activity hours for myopia
 
Near work
Outdoor
 
OR
95% CI
OR
95% CI
Model 1
1.12
1.01–1.25
0.93
0.82–1.07
Model 2
1.07
0.94–1.21
0.86
0.74–1.00
Model 3
1.05
0.92–1.21
0.86
0.75–1.00
Model 4
1.10
0.94–1.27
0.82
0.70–0.96
Model 1 for near work: adjusted for near work time as a fixed effects, and family effect as a random effect; Model 1 for outdoor: adjusted for outdoor activity time as fixed effect, and family effect as a random effect
Model 2: model 1 + children’s age and gender
Model 3: model 2 + average parental refractive error
Model 4 for near work: model 3 + maternal and paternal education level, and outdoor activity time; Model 4 for outdoor: model 3 + maternal and paternal education level, and near work time

Discussion

Although cross-sectional and longitudinal studies on Chinese urban children have found an association between near work/outdoor activity and myopia/myopic progression, [ 1520] studies related to the association of near work and outdoor activity with myopia are rare and equivocal among Chinese rural children [ 24]. In Taiwan, Wu et al. reported that more frequent outdoor activity was associated with a lower prevalence of myopia in rural Chinese primary school children [ 16, 26]. In contrast, in the Strabismus, Amblyopia and Refractive Error Study (STARS) in Singaporean preschool Chinese children, and in the X-PRES in Chinese rural teenagers, negative results were reported related to both near work and outdoor activity [ 25, 31]. A meta-analysis that included 7 cross-sectional studies (including STARS and X-PRES) have reported that one additional hour per week spent outdoors would reduce the odds by 2% (odds ratio, 95% confidence interval: 0.98, 0.97–0.99) of having myopia in children and adolescents.
The current study performed in Handan reports the effect and possible interaction of near work and outdoor activity on myopia in a wide age range among the Chinese rural population. In the present study, the parental refractive error, one of the important confounding factors for children’s myopia, [ 31, 32] was obtained directly. We found that myopic children spent more time on near work compared to non-myopic children. However, in general, the daily near work was not associated with the children’s myopia as per the multiple logistic analysis, after adjusting for the children’s age, gender, average parental refractive error, parental education level, and outdoor activity time. This was consistent with previous studies conducted in Caucasians, [ 23, 33, 34] and East Asians, living in Sydney [ 23]. This was also consistent with findings in Singaporean preschool Chinese children in STARS, and in X-PRES in Chinese rural teenagers [ 25, 31]. However, our results were different from those reported in Beijing urban students [ 16, 17, 20].
A weak protective effect of outdoor activity for myopia was found in the present study. The association between more time outdoors and either a lower prevalence of myopia, or more hyperopic refractive error, was reported in Caucasians [ 23, 34, 35] as well as Singaporean teenagers [ 24]. Furthermore, this association was also found in the Chinese [ 16, 17, 26]. In Taiwan, Wu et al. reported that more frequent outdoor activity was associated with a lower prevalence of myopia (OR, 0.3; 95% CI, 0.1–0.9) in rural Chinese school children aged 7–12 years [ 26]. Guo et al. also reported that less outdoor activity and more time spent indoors studying was associated with myopia progression and elongation of axial length in primary students in grades 1 and grade 4 in Beijing (age range: 5–13 years) [ 17]. However, the association was not found either in X-PRES in Chinese rural teenagers (mean age: 14.6 years) [ 25] or in another study involving Beijing urban school children (aged 6–17 years) [ 20]. It is noteworthy that the protective effect of outdoor activity in our study was not found after the children were divided into two groups by the age cut-off point of 12 (data not shown).
The inconsistent findings of the different studies in both Chinese urban and rural children may be attributed to the different living environments between rural and urban areas. Lin et al. reported the generational myopic shift was estimated to 1D more in Beijing urban area compared to that in Handan rural area [ 36, 37]. The less urbanized environment and more time outdoors were reported to be associated with lower prevalence of myopia [ 23, 3537]. These may be attributed to more time spent outdoors in the sun by rural children [ 23, 38]. Hence, the rural children are exposed to a less myopigenic living environment compared to their urban counterparts.
There were some limitations in the present study. First, the population sample used was obtained from the offspring of the participants in the HES. Consequently, the sample size was relatively small. Second, the activities were self-reported by the children. Although this method was predominant in previously reported studies, the estimation of activity time could be subject to recall bias. However, we randomly reassessed 50 children who completed the questionnaire over a one-month period, and the weighted kappa value was acceptable (0.82) comparing the two questionnaires findings. Third, the information on activities of the children who did not respond (nearly 30%) was unknown.
In summary, in general, the association between near work and myopia was not found in this study. However, a very weak protective effect of outdoor activity on myopia in Chinese rural children was suggested. Further longitudinal studies are warranted.

Conclusion

In summary, in this sample of rural Chinese rural children, no association between near work and myopia was found, except for children with high near work and moderate outdoor activity load. Furthermore, a weak protective effect of outdoor activity on myopia in Chinese rural children was observed.

Acknowledgements

The authors thank Dr. Lei Li, Dr. Peng Zhang and Dr. Qian Jia (Handan Eye Hospital), and Dr. Xiao Dong Yang (Nanjing Tongren Hospital), for their invaluable assistance in data collection.

Funding

The study was supported by the Key Technologies Research Development Program (No.1113108019) from the Bureau of Science and Technology of Handan City, Hebei Province, China, the Beijing Science & Technology Novel Star Program (2009B44), and Zhejiang Health Innovation Talents Program 2016025.

Availability of data and materials

The dataset supporting the conclusion of this article is available in the Additional file  1.

Ethics approval and consent to participate

The study followed the tenets of the Declaration of Helsinki and was approved by the Ethics Committee of the Handan Eye Hospital. Written, informed-consent of the parents was obtained.

Consent for publication

Written, informed-consent of the parents was obtained.

Competing interests

The authors declare that they have no competing interests.

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