Jpn J Ophthalmol DOI 10.1007/s10384-014-0328-2

CLINICAL INVESTIGATION

Refractive error change and its association with ocular and general parameters in junior high school students in Taiwan Chia-Chin Liao • Li-Ju Chen Jy-Haw Yu • Jen-Chieh Lin



Received: 14 November 2013 / Accepted: 28 April 2014 Ó Japanese Ophthalmological Society 2014

Abstract Purpose To assess the relationships between refractive error and ocular and general parameters in Taiwanese junior high school students and to identify the predictive factors associated with the changes in refractive error. Methods This was a prospective, school-based study. A total of 687 students (357 boys and 330 girls) from a municipal junior high school in Taipei were enrolled. The students’ refractive status, intraocular pressure, and ocular parameters were measured first in 2010 and again 1 year later. Data were analyzed using multiple linear regression models and generalized estimating equations (GEEs). Results Significant differences were found between the baseline (2010) and 1-year follow-up (2011) mean anterior chamber depths, mean axial lengths, and mean horizontal and vertical corneal refractive powers. GEE models revealed that vertical and horizontal corneal refractive powers, axial length, and anterior chamber depth were significantly associated with refractive error change. Conclusions Students with a longer axial length, steeper corneal radius, and shallower anterior chamber depth had an increased risk of myopic refractive errors. Keywords Anterior chamber  Axial length  Crystalline lens  Refractive errors

C.-C. Liao  L.-J. Chen  J.-H. Yu  J.-C. Lin (&) Department of Ophthalmology, Taipei City Hospital, Heping Fuyou Branch, No. 33, Section 2 Chung-Hwa Road, Taipei City 10065, Taiwan e-mail: [email protected] J.-C. Lin Graduate Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan

Introduction Over 70 % of children in Taiwan become myopic during their school years [1]. This high prevalence of myopia among school children has become a public health problem. Despite the prescription of spectacles to correct refractive errors and the administration of pharmacologic interventions, such as atropine and tropicamide, to slow the myopia progression and axial elongation, the prevalence among school children of myopia due to refractive error has increased in recent decades, from 64.2 % in 1983 to 81 % in 2000 [1]. In Taiwan, a basic competence test is required to gain entrance into senior high school, and students face substantial academic pressure, in addition to competitive examinations throughout junior high school. The pressure continues to increase once they are enrolled in senior high school, and children spend little time participating in outdoor activities. This is unfortunate considering the results of a systemic review and meta-analysis that suggest that increasing time spent outdoors may be an effective strategy for reducing the development and progression of myopia [2]. It is likely that decreased time spent outdoors and increased academic pressure associated with age and educational progress are underlying factors causing faster shifts in refractive errors among junior high school students than among elementary and senior high school students in Taiwan [3]. To achieve effective and targeted therapies for decreasing the number of children experiencing increased risks of retinal detachment [4], cataract [5], or glaucoma [6] associated with increasing axial length, an early and noninvasive test could be used to identify children at risk of developing myopia. Although indicators such as parental myopia and baseline refractive error [7] have moderate validity in predicting the onset of later myopia, it is

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impractical to measure parental myopia in the context of school-based programs. Several recent studies have investigated the associations between ocular and general systemic parameters and refractive error. Factors associated with myopia included female sex [8], lower body mass index [9], longer axial length [10], deep anterior chamber depth [10], and higher corneal refractive power [11], whereas correlations between refractive error and other parameters, such as intraocular pressure (IOP) [12, 13] and lens thickness [8, 14], are controversial. Additionally, inferences of causality between biometric parameters and refraction error change from such cross-sectional studies are difficult to ascertain. The rate of progression or the trend of the changes of each ocular biometric parameter has been discussed in previous studies [3, 15]. However, whether the altered ocular or general parameters predispose an individual to changes in refractive error remains to be clarified. The Orinda Longitudinal Study of Myopia (OLSM) showed an association between a child’s refractive error and ocular components before the onset of juvenile myopia [16]. Mean sphere, corneal power, Gullstrand lens power, and axial length were used to predict myopia onset in children. The Collaborative Longitudinal Evaluation of Ethnicity and Refractive Error (CLEERE) Study also reported that early childhood refractive error may be used as a predictor of myopia onset [17]. However, these longitudinal studies did not mention the predictors associated with the trends in refractive error change, such as myopic shifting. Therefore, the goals of our study were to determine whether ocular parameters could be used as predictors of refractive error change among junior high school students and to identify the best predictor for an early intervention program against rapid myopic shifting.

Canon). The ocular parameters of central corneal thickness (CCT), anterior chamber depth (ACD), lens thickness (LT), axial length (AXL), horizontal corneal refractive power (K1), and vertical corneal refractive power (K2) were measured before cycloplegia by means of an optical low coherence reflectometer (Lenstar LS900; Haag Streit, Koeniz, Switzerland). Cycloplegia was induced with one drop of 0.5 % proparacaine and then with two drops of 1 % cyclopentolate administered 5 min apart. The ocular parameters were measured at least 30 min after the final drop of cyclopentolate. If the pupil size was less than 6 mm or reflective to light, an additional drop of cyclopentolate was administered every 5 min until acceptable dilation was achieved. The students’ body height and weight were also measured. The same procedures were conducted for the students 1 year later. The data obtained from the right eye were analyzed at baseline in 2010 and at the 1-year follow-up in 2011. Refraction was expressed as the spherical equivalent (SE), calculated as the sphere plus a half cylinder. Body mass index was defined as the individual’s weight in kilograms divided by his or her height in square meters. Myopia was defined as an SE refractive error of at least -0.50 D. Data were analyzed using a paired t test to reveal the differences in ocular parameters between the sample years, and the correlation between possible predictive factors and refractive error over the year was analyzed using multiple linear regression models. Finally, generalized estimating equations (GEEs) were used to uncover possible predictive factors of refractive error change. A p value of less than 0.05 was considered significant. Statistical analyses were conducted with IBM SPSS 20.0 software (IBM, Chicago, IL, USA). The study protocol was approved by the institutional review board of Taipei City Hospital and conducted in accordance with the tenets of the Declaration of Helsinki.

Methods First-year students (aged approximately 13 years) of a Taipei municipal junior high school were examined in March 2010, and follow-up examinations were conducted in March 2011. Students with histories of diagnosed glaucoma, congenital cataract, ocular surgery, and orthokeratology lens wear were excluded. All enrolled students underwent a series of examinations, including best-corrected visual acuity using the Landolt C chart as described in an existing protocol [18] and of refractive power using an automated refractometer (RK-F1; Canon) under cycloplegic conditions. Five consecutive automated refractometer readings were obtained on each eye of all students, and the mean of the five values was used for the analysis. The IOP was measured before cycloplegia by means of a noncontact tonometer (TX-F,

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Results Among the 714 students enrolled in 2010, ten transferred to different schools during the 1-year period, and 17 failed to complete all examinations owing to personal reasons. As a result, complete examination data for both years was available for a total of 687 students, comprising 357 boys (52 %) and 330 girls (48 %). The mean age was 14.1 ± 0.7 years in 2011 (range 13–15 years). The ocular biometric characteristics of the students’ right eyes for both years were analyzed using paired t tests, the results of which are given in Table 1. Significant differences in the mean cycloplegic SE refraction was observed (p \ 0.001): -2.64 ± 2.32 D in 2010 and -2.92 ± 2.36 D in 2011. The distribution of refractive error in the students and the

Refraction changes in Taiwan students Table 1 General and ocular biometric characteristics of 687 junior high school children in Taiwan Parameter

Mean ± SD (2010)

Mean ± SD (2011)

p value

Height (cm)

NA

162.54 ± 7.91

NA

Weight (kg)

NA

57.89 ± 13.48

BMI (kg/m2)

NA

21.51 ± 4.87

ACD (mm)

3.17 ± 0.26

AXL (mm)

24.64 ± 1.14

CCT (lm)

562.58 ± 31.09

IOP (mmHg) K1 (D)

NA NA

3.18 ± 0.26

\0.01

24.86 ± 1.20

\0.001

562.13 ± 31.47

0.955

15.91 ± 3.03 42.54 ± 1.40

18.27 ± 3.44 42.53 ± 1.43

\0.001 \0.001

K2 (D)

44.09 ± 1.59

44.03 ± 1.64

\0.01

LT (mm)

3.41 ± 0.21

3.40 ± 0.18

\0.01

SE (D)

–2.64 ± 2.32

–2.92 ± 2.36

\0.001

No. of students

BMI body mass index, ACD anterior chamber depth, AXL axial length, CCT central corneal thickness, IOP intraocular pressure, K1 horizontal corneal refractive power, K2 vertical corneal refractive power, LT lens thickness, SE spherical equivalent

change in this refractive error at the 1-year follow-up examination are shown in Figs. 1 and 2. Multiple linear regression analysis was performed with the cycloplegic SE in 2010 as the dependent variable. The independent variables were the systemic and ocular parameters, including sex, horizontal and vertical corneal refractive powers, IOP, axial length, central corneal thickness, anterior chamber depth, and lens thickness. Of the systemic parameters, only female sex was significantly associated with refractive error (Table 2). Several ocular biometric parameters were significantly associated with refractive error, including horizontal and vertical corneal refractive powers, axial length, anterior chamber depth, and lens thickness (Table 2). When the cycloplegic SE in 2011 was taken as the dependent variable in the multivariate analysis, it was significantly associated with female sex, horizontal and vertical corneal refractive powers, axial length, anterior chamber depth, lens thickness, and IOP (Table 3).

Baseline refractive error, D Fig. 1 Distribution of students’ refractive errors in 2010 (baseline)

Fig. 2 Distribution of students’ refractive error changes in 2011

180 160

No. of students

140 120 100 80 60 40 20 0

-1.5

-1.25

-1

-0.75

-0.5

-0.25

0

0.25

0.5

0.75

Refractive error change, D

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C.-C. Liao et al. Table 2 Association between refractive error and ocular and general parameters of 687 Taiwanese junior high school children in 2010 Parameter

Beta

p value

95 % CI

Female

–0.394

\0.001a

–0.572, –0.217

Male

0





K1 (D)

–0.554

\0.001a

–0.689, –0.418

K2 (D)

–0.423

\0.001a

–0.534, –0.312

0.008

0.690

–0.031, 0.04724

ACD (mm)

–1.443

\0.001a

–1.931, –0.955

AXL (mm) LT (mm)

–2.220 0.855

\0.001a \0.001a

–2.331, –2.109 0.400, 1.310

CCT (lm)

0.001

0.601

–0.002, 0.004

IOP (mmHg)

K1 horizontal corneal refractive power, K2 vertical corneal refractive power, IOP intraocular pressure, ACD anterior chamber depth, AXL axial length, LT lens thickness, CCT central corneal thickness, CI confidence interval a

Value was significant at the p \ 0.05 level

Table 3 Association between refractive error and ocular and general parameters of 687 junior high school children in 2011 Parameter

Beta

Female

–0.292

p value 0.004a

95 % CI –0.489, –0.096

Male

0





Height (cm)

0.020

0.583

–0.051, 0.090

Weight (kg)

0.003

0.951

–0.101, 0.095

2

BMI (kg/m ) K1 (D)

0.015 –0.473

0.915 \0.001a

–0.252, 0.281 –0.664, –0.282

K2 (D)

–0.348

\0.001a

–0.497, –0.199

IOP (mmHg)

–0.062

0.014a

–0.111, –0.012

ACD (mm)

–0.950

0.006a

–1.625, –0.275

AXL (mm)

–1.942

\0.001a

–2.065, –1.820

LT (mm)

0.900

a

0.003

0.317, 1.483

CCT (lm)

0.001

0.485

–0.002, 0.005

BMI body mass index, K1 horizontal corneal refractive power, K2 vertical corneal refractive power, IOP intraocular pressure, ACD anterior chamber depth, AXL axial length, LT lens thickness, CCT central corneal thickness, CI confidence interval a

Value was significant at the p \ 0.05 level

Table 4 Factors that potentially predict refractive error change in 687 Taiwanese junior high school children according to GEE models Predictor

Beta

p value

95 % CI

K1 (D)

–0.426

\0.001a

–0.527, –0.324

K2 (D)

–0.500

\0.001a

–0.581, –0.420

ACD (mm)

–1.306

\0.001a

–1.687, –0.924

AXL (mm)

–2.061

\0.001a

–2.183, –1.938

0.297

0.240

–0.198, 0.793

LT (mm)

K1 horizontal corneal refractive power, K2 vertical corneal refractive power, ACD anterior chamber depth, AXL axial length, LT lens thickness, CI confidence interval a

Value was significant at the p \ 0.05 level

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Generalized estimating equation (GEE) models were applied for all variants with statistical significance in the multiple regression analysis in both 2010 and 2011. The results indicated that the horizontal and vertical corneal refractive powers, axial length, and anterior chamber depth were significantly associated with myopic shifting, with the exception of lens thickness (p = 0.240; Table 4).

Discussion Many previous cross-sectional studies have reported associations between ocular and general biometric parameters and refraction error change, but these were only observed in multivariate models and in correlation analyzes [8–14]. The OLSM [16] and CLEERE [17] studies investigated the predictive factors for the onset of myopia in children. The results of those studies indicated a lack of significant relationship between refraction error change and ocular and general biometric parameters among junior high school children. Changes in the relationship between the ocular biometric component and the refractive error change may be associated with the process of emmetropization, whereby, during myopic shifting and axial length elongation, each component of the eye adjusts to match another component to reduce refractive error change [16, 19]. The findings of our study indicated that female sex, higher corneal refractive power (K1, K2), longer axial length, deeper anterior chamber, and thinner lens were significantly associated with greater myopic refractive errors at baseline (2010) and after 1-year follow-up (2011). Higher levels of IOP were significantly associated with greater myopic refractive errors only in the follow-up. Our results were generally consistent with those of previous cross-sectional surveys [11, 14, 20, 21]. Similar to the Beijing Eye Study [21], which reported that more hyperopic participants had shallower anterior chamber depths, this study found an association between myopia and anterior chamber depth. The relationship between myopia and lens thickness revealed in our study was also comparable to the results of a previous cross-sectional study conducted in Taiwan [14]. In an attempt to examine the correlations between ocular parameters and the refraction error change using a GEE model, we found that the possible factors influencing refraction error change were longer axial length, steeper corneal radius, and deeper anterior chamber depth. However, lens thickness was no longer a predictor of refraction error change in the GEE model. One possible explanation is that lens thickness does not follow a linear pattern of change with age and refraction error. In a previous nationwide survey among school children in Taiwan, the anterior chamber depth and axial length were found to increase with age and myopic progression; however, the lens thickness

Refraction changes in Taiwan students

decreased from the ages of 7–11, remained unchanged until age 15, and increased thereafter [14]. The results of our study on 13- to 15-year-old students showed that anterior chamber depth and axial length increased with myopic progression, which is comparable to previous research results. However, lens thickness decreased slightly with an increase in myopia. The Singapore Cohort Study of the Risk Factors for Myopia (SCORM) suggested that the changes in lens thickness were faster in the newly developed myopia group than in the persistent myopia group [22]. We thus divided our sample into newly developed myopia and persistent myopia groups, and, using an independent t test, analyzed the changes over the 2 years between the ocular biometric parameters and the SE. The results revealed a significant difference (p = 0.01) only for the change in SE. Several potential limitations of our study bear mentioning. First, the participants of our study were from one junior high school only, resulting in a potential selection bias. Thus, the results might not be representative of the entire junior high school population in Taiwan. Second, no information was collected on the socioeconomic background or lifestyle of the study participants, so no information on potential differences between rural and urban regions could be obtained. Third, our study was a longitudinal investigation with a relatively short follow-up period (1 year), which does not impart confidence in the associations between refraction error change and each biometric parameter. Fourth, only a limited number of ocular and general parameters were included. Other ocular factors, such as corneal hysteresis, could also be potential predictive factors of refractive error [19]. Besides, other factors, such as parental educational and refractive status [19], time spent outdoors [2], and near work [23], might generate more comprehensive results. In a future study, we hope to obtain more comprehensive data and to compare ethnic differences between Asian and white populations. In conclusion, we suggest that junior high school students in Taiwan with longer axial length, steeper corneal radius, and deeper anterior chamber depth are at high risk for myopic refraction error change. Early interventions against myopia and more frequent follow-ups are necessary for these children. Acknowledgments The authors thank Principal May-Jen Lin and her colleagues at Taipei Municipal Junior High School for their considerable assistance in facilitating the eye research and data collection. Conflicts of interest C.-C. Liao, None; L.-J. Chen, None; J.-H. Yu, None; J.-C. Lin; None.

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Refractive error change and its association with ocular and general parameters in junior high school students in Taiwan.

To assess the relationships between refractive error and ocular and general parameters in Taiwanese junior high school students and to identify the pr...
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