Journal of Pediatric Ophthalmology and Strabismus

Original Article 

Longitudinal Changes in Refractive Error in a Pediatric Referral Population in Korea

Young Shin Kim, MD; Seung-Yup Lee, MS; Song-hee Park, MD, PhD

Abstract

Purpose:

To investigate changes in the spherical equivalent (SE) refractive error and astigmatism in a pediatric referral population in Korea with longitudinal follow-up and to evaluate the effect of risk factors on changes in refractive error.

Methods:

This was a retrospective case series. In total, 221 patients who presented to a tertiary care hospital when aged 3 to 9 years and who underwent at least 10 years of follow-up were enrolled. The patients were divided into groups in terms of the initial extent of SE refractive error, the initial extent of astigmatism, sex, and ocular alignment. Changes in SE and astigmatism were compared among the groups.

Results:

The patients were followed up for a mean of 11.19 ± 1.81 years. An overall negative shift in SE refractive error and increasing tendency in astigmatism during the follow-up period were noted. The negative shift in SE refractive error in the myopia group was significantly greater than those in the emmetropia and hyperopia groups. The change in astigmatism in the myopia group was significantly greater than that in the hyperopia group. The change in astigmatism in the low astigmatism group was significantly greater than those in the moderate and high astigmatism groups. Sex did not influence the changes in SE refractive error or astigmatism.

Conclusions:

A pediatric referral population in Korea showed a negative shift in SE refractive error and increasing tendency in astigmatism during childhood. Changes in refractive error may be influenced by the initial degree of SE refractive error and astigmatism.

[J Pediatr Ophthalmol Strabismus. 2017;54(1):43–51.]

Abstract

Purpose:

To investigate changes in the spherical equivalent (SE) refractive error and astigmatism in a pediatric referral population in Korea with longitudinal follow-up and to evaluate the effect of risk factors on changes in refractive error.

Methods:

This was a retrospective case series. In total, 221 patients who presented to a tertiary care hospital when aged 3 to 9 years and who underwent at least 10 years of follow-up were enrolled. The patients were divided into groups in terms of the initial extent of SE refractive error, the initial extent of astigmatism, sex, and ocular alignment. Changes in SE and astigmatism were compared among the groups.

Results:

The patients were followed up for a mean of 11.19 ± 1.81 years. An overall negative shift in SE refractive error and increasing tendency in astigmatism during the follow-up period were noted. The negative shift in SE refractive error in the myopia group was significantly greater than those in the emmetropia and hyperopia groups. The change in astigmatism in the myopia group was significantly greater than that in the hyperopia group. The change in astigmatism in the low astigmatism group was significantly greater than those in the moderate and high astigmatism groups. Sex did not influence the changes in SE refractive error or astigmatism.

Conclusions:

A pediatric referral population in Korea showed a negative shift in SE refractive error and increasing tendency in astigmatism during childhood. Changes in refractive error may be influenced by the initial degree of SE refractive error and astigmatism.

[J Pediatr Ophthalmol Strabismus. 2017;54(1):43–51.]

Introduction

There is abundant evidence from cross-sectional refractive data of children to determine a statistical trend in refractive changes during childhood. However, relatively few longitudinal studies of children have been performed. Furthermore, most of these studies have focused exclusively on myopic refractive errors.1,2

Changes in refractive error are complex and multifactorial, and there is substantial interest in understanding the roles of genetics and environmental factors in refractive changes.3,4 Furthermore, various factors may affect changes in refractive errors, such as age, sex, initial refractive error, and strabismus. The interactions among these factors have not been fully determined. Thus, differing characteristics of patients in any given study may lead to different results.

In this study, we reviewed changes in the spherical equivalent (SE) refractive error and astigmatism in a pediatric referral population in Korea with longitudinal follow-up and evaluated the effect of risk factors on changes in refractive error.

Patients and Methods

Patients

A retrospective chart review involved patients seen at Soonchunhyang University Seoul Hospital from September 1992 to February 2015. In total, 221 patients aged 3 to 9 years who presented to a tertiary care hospital and were observed for at least 10 years were enrolled. Patients with developmental delay, previous refractive surgery, any form of neurological impairment, or other diseases of the visual pathways were excluded. The study adhered to the tenets of the Declaration of Helsinki. It was approved by the Ethics Committee of Soonchunhyang University Seoul Hospital.

Procedure

At the initial visit, all patients underwent a full ophthalmological assessment, including visual acuity testing, cycloplegic refraction, evaluation of ocular alignment status, slit-lamp biomicroscopy, and a fundus examination. Cycloplegia was accomplished by the administration of three drops of topical 1% (w/v) cyclopentolate to each eye, with a 5-minute interval between each drop. Cycloplegic measurements were performed 30 minutes after the last drop was instilled. Autorefraction tests were performed using an autokeratorefractometer (KR-8900; Topcon Co., Tokyo, Japan).

Data

Refractive data were collected for the first 13 years of follow-up on the initial degree of SE refractive error, initial degree of astigmatism, sex, and ocular alignment. To evaluate the initial degree of SE refractive error, eyes were categorized as having myopia (< −0.50 D), emmetropia (−0.50 to 0.75 D), or hyperopia (> 0.75 D). To evaluate the initial degree of astigmatism, eyes were categorized as having low (< 1.00 D), moderate (1.00 to 3.00 D), or high (> 3.00 D) astigmatism. To assess the ocular alignment, eyes were categorized as having esotropia (> 10 prism diopters [PD] of esotropia), orthotropia (10 PD or less of esotropia and exotropia), or exotropia (> 10 PD of exotropia).

Statistical Analysis

Statistical analysis was performed using SPSS for Windows software (version 21; SPSS, Inc., Chicago, IL). Because the correlation between the two eyes in terms of refractive error was close to unity, only data from right eyes were used in our analyses. A linear mixed model was used to analyze longitudinal changes in SE refractive error and astigmatism over time and to estimate the relationships between longitudinal changes in refractive error over time and potentially relevant factors. Each refractive error served as a dependent variable. The fixed effects were time (the time in years between the baseline refractive error measurement and each follow-up visit), the initial degree of SE refractive error, the initial degree of astigmatism, sex, ocular alignment, and the interactions of these factors with time. The random effect was the individual patient. To explore whether potential confounders affected longitudinal changes in refractive error over time, Model 1 was adjusted for both time and each variable. The final multivariable model (Model 2) was adjusted for time, those variables associated with P values less than .05 in Model 1, and the interactions of the variables with time. A P value of less than .05 was considered to indicate statistical significance.

Results

In total, 221 patients were assessed. The mean age at the initial visit was 4.42 ± 1.57 years (range: 3 to 9 years), and the mean length of follow-up was 11.19 ± 1.81 years (range: 10 to 18 years). There were 94 boys and 127 girls. The correlation between the two eyes in terms of SE refractive error was 0.91, whereas that of astigmatism was 0.90. The clinical characteristics and demographics of the patients are summarized in Table 1.


Clinical Characteristics and Demographics of the 221 Patients

Table 1:

Clinical Characteristics and Demographics of the 221 Patients

Changes in SE Refractive Error

An overall negative shift in SE refractive error during the follow-up period was noted (F = 762.515, P < .001) (Figures 1A–1B). In Model 1, the initial extent of SE refractive error and ocular alignment correlated significantly with changes in the SE refractive error. However, in the final multivariable model (Model 2) (adjusted for confounders with P < .05 in Model 1), the only significant predictor of SE refractive error was the initial extent of SE refractive error (F = 14.163, P < .001) (Table 2, Figure 2). Changes in SE refractive error were not associated with either sex or the initial degree of astigmatism.


Boxplots showing changes in the right eye (A) spherical equivalent (SE) refractive errors and (C) astigmatism by age. The error bars represent 95% confidence intervals. Regression models are also presented (B and D, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1. The annual rates of change in refractive error are presented as means ± standard errors. D = diopters

Figure 1.

Boxplots showing changes in the right eye (A) spherical equivalent (SE) refractive errors and (C) astigmatism by age. The error bars represent 95% confidence intervals. Regression models are also presented (B and D, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1. The annual rates of change in refractive error are presented as means ± standard errors. D = diopters


Results of Linear Mixed Modeling of Changes in SE Refractive Error

Table 2:

Results of Linear Mixed Modeling of Changes in SE Refractive Error


Boxplots showing changes in the right eye spherical equivalent (SE) refractive errors by age. The error bars represent 95% confidence intervals. Patients were divided into groups by (A) the initial degree of SE refractive error, (C) the initial degree of astigmatism, (E) sex, and (G) ocular alignment. Regression models for these groups are also presented (B, D, F, and H, respectively). Each P value represents the probability of an interaction between each variable and time in both Model 1 (D, F) and Model 2 (B, H). The annual rates of change in refractive error are presented as means ± standard errors. Asterisks denote a significant difference among subgroups (Model 2 with the Bonferroni correction, P < .05). D = diopters

Figure 2.

Boxplots showing changes in the right eye spherical equivalent (SE) refractive errors by age. The error bars represent 95% confidence intervals. Patients were divided into groups by (A) the initial degree of SE refractive error, (C) the initial degree of astigmatism, (E) sex, and (G) ocular alignment. Regression models for these groups are also presented (B, D, F, and H, respectively). Each P value represents the probability of an interaction between each variable and time in both Model 1 (D, F) and Model 2 (B, H). The annual rates of change in refractive error are presented as means ± standard errors. Asterisks denote a significant difference among subgroups (Model 2 with the Bonferroni correction, P < .05). D = diopters

In Model 2 with the Bonferroni correction, when patients were divided into three groups in terms of the initial degree of SE refractive error, the negative shift in SE refractive error in the myopia group was significantly greater than those in the emmetropia (F = 15.048, P < .001) and hyperopia (F = 29.169, P < .001) groups. However, the changes did not differ significantly between the emmetropia and hyperopia groups (F = 0.866, P = .352) (Figures 2A–2B).

Changes in Astigmatism

An overall increase in astigmatism during the follow-up period was noted (F = 67.859, P < .001) (Figures 1C–1D). In Model 1, the initial degree of SE refractive error, the initial extent of astigmatism, and ocular alignment were significantly correlated with changes in astigmatism. However, in the final multivariable model (Model 2) (adjusting for confounders with P < .05 in Model 1), the remaining significant predictors of astigmatism were the initial degree of SE refractive error (F = 4.790, P = .008) and the initial degree of astigmatism (F = 12.860, P < .001) (Table 3, Figure 3). Changes in astigmatism were not affected by sex.


Boxplots showing changes in the right eye (A) spherical equivalent (SE) refractive errors and (C) astigmatism by age. The error bars represent 95% confidence intervals. Regression models are also presented (B and D, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1. The annual rates of change in refractive error are presented as means ± standard errors. D = diopters

Figure 1.

Boxplots showing changes in the right eye (A) spherical equivalent (SE) refractive errors and (C) astigmatism by age. The error bars represent 95% confidence intervals. Regression models are also presented (B and D, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1. The annual rates of change in refractive error are presented as means ± standard errors. D = diopters


Results of Linear Mixed Modeling of Changes in Astigmatism

Table 3:

Results of Linear Mixed Modeling of Changes in Astigmatism


Boxplots showing changes in the right eye astigmatism by age. The error bars represent 95% confidence intervals. Patients were divided into groups by (A) the initial extent of spherical equivalent refractive error, (C) the initial extent of astigmatism, (E) sex, and (G) ocular alignment. Regression models for these groups are also presented, (B, D, F, and H, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1 (F) and Model 2 (B, D, and H). Annual rates of change in refractive error are presented as means ± standard errors. Asterisks denote a significant difference among the subgroups (Model 2 with the Bonferroni correction, P < .05). D = diopters

Figure 3.

Boxplots showing changes in the right eye astigmatism by age. The error bars represent 95% confidence intervals. Patients were divided into groups by (A) the initial extent of spherical equivalent refractive error, (C) the initial extent of astigmatism, (E) sex, and (G) ocular alignment. Regression models for these groups are also presented, (B, D, F, and H, respectively). Each P value represents the probability of an interaction between each variable and time in Model 1 (F) and Model 2 (B, D, and H). Annual rates of change in refractive error are presented as means ± standard errors. Asterisks denote a significant difference among the subgroups (Model 2 with the Bonferroni correction, P < .05). D = diopters

In Model 2 with the Bonferroni correction, when the patients were divided into three groups in terms of the initial degree of SE refractive error, the change in astigmatism in the myopia group was significantly greater than that in the hyperopia group (F = 9.258, P = .002). However, the myopia and emmetropia groups and the emmetropia and hyperopia groups did not differ (F = 2.568, P < .109; F = 3.469, P < .063, respectively) (Figures 3A–3B).

In Model 2 with the Bonferroni correction, when the patients were divided into three groups in terms of the initial degree of astigmatism, the change in astigmatism in the low astigmatism group was significantly greater than those in the moderate (F = 19.520, P < .001) and high (F = 16.790, P < .001) astigmatism groups. However, the change in the moderate and high astigmatism groups did not differ (F = 1.262, P = .262) (Figures 3C–3D).

Discussion

We investigated changes in the SE refractive error and astigmatism in a pediatric referral population in Korea with longitudinal follow-up. The results of this study demonstrated an overall negative shift in SE refractive error and increasing tendency in astigmatism from age 3 to 16 years. Moreover, the initial degree of SE refractive error showed a significant association with changes in SE refractive error, and the initial degrees of SE refractive error and astigmatism showed a significant association with changes in astigmatism.

Changes in SE Refractive Error

We suggest that the negative shift may be the result of complex interactions between genetic and environmental factors. Previous studies have shown that the prevalence of myopia and the rate of myopic progression in East Asian children are higher than those in Western children.1 Intense nearsighted work,5 limited outdoor activity,7 and growing up in an urban environment7 are factors suspected to contribute to myopic shift. Unlike previous studies,8,9 an initial increase in the mean SE refractive error was not observed in our study, and there was a greater annual decrease in SE refractive error throughout the follow-up period. In the myopia group, a slightly increased SE refractive error was observed between age 3 and 4 years. After this point, the value started to decrease continuously.

In the current study, the initial degree of SE refractive error affected the negative shift in SE refractive error. Compared with the emmetropia and hyperopia groups, the myopia group was more likely to have a significant negative shift in SE refractive error, consistent with previous reports showing significantly greater myopic shift in children with myopia.1,10 These findings indicate that initially myopic eyes are more likely to have a faster rate of change toward high myopia. However, the annual rate of change was so variable that the refractive outcome could hardly be predicted for an individual child.

Previous studies have provided conflicting data regarding the influence of sex on changes in SE refractive error. From the age of 5 to 15 years, several studies found a higher prevalence of myopia among girls and a faster rate of progression among girls with myopia.11 Another study found no difference in the progression of myopia based on sex.10 In the current study, there was no difference in the mean SE refractive error or changes in SE refractive error due to sex.

There are several reports on refractive error changes in children with strabismus. Longitudinal studies of accommodative esotropia have revealed that refractive errors show a slow negative shift over time.12,13 Regarding exotropia, a significant myopic shift over time compared with similarly aged non-strabismic children was reported in a population-based study.14 In the current study, compared to the orthotropia and exotropia groups, the esotropia group exhibited slower changes in SE refractive error. Because esotropia occurs more frequently in children with hyperopia, the hyperopic refractive error in the esotropia group might have caused the negative shift to be less than that in the other groups, as discussed previously. However, in the final multivariable model adjusting for the initial extent of SE refractive error, ocular alignment was not a significant predictor of SE refractive error.

Changes in Astigmatism

Many potential risk factors for astigmatism are still not well understood. Findings in some studies have suggested that astigmatism is dominantly inherited,15 whereas others have shown low heritability.16 Saw et al.17 suggested that environmental influences have a major impact on astigmatism. Thus, the relative contribution of genetic and environmental influences to astigmatism requires further analysis. In previous studies, investigators have consistently found that there is a rapid decline in astigmatism in the first 2 years of life,18,19 followed by slower changes occurring between ages 2 and 6 years.1 However, findings in other studies lead to inconsistent conclusions concerning later developmental changes in astigmatism. Anstice20 reported a significant decrease in astigmatism up to age 14 years. In contrast, a longitudinal study of astigmatism in Tohono O'odham Native American children21 showed that highly astigmatic children aged 3 to 11 years and children older than 11 years show a small increase in astigmatism with age. In the current study, an increasing tendency in astigmatism during the follow-up period was noted.

We evaluated the effects of potential risk factors on an increasing tendency in astigmatism. Any association between astigmatism and myopia remains controversial. In the current study, the change in astigmatism in the myopia group was significantly greater than that in the hyperopia group. Gwiazda et al.22 suggested that spherically asymmetric forces operative in tense ciliary muscles or zonules could induce astigmatism associated with the development of myopia. Moreover, optical blurring caused by uncorrected astigmatism may trigger myopic development. Although the initial degree of astigmatism was not associated with changes in the SE refractive error, greater astigmatism was associated with more myopic refraction in the current study. Our results support the hypothesis that an increase in myopia in children can enhance the development and progression of astigmatism.

The initial degree of astigmatism showed a significant association with changes in astigmatism. The low astigmatism group was more likely to have a significant increase in astigmatism than were the moderate and high astigmatism groups. These findings indicate that eyes with moderate to high astigmatism are relatively stable initially and that eyes with low astigmatism are more likely to have an increasing tendency in astigmatism.

Findings in previous studies on differences in astigmatism between sexes have been inconsistent. Several large population-based studies reported slightly higher prevalence rates of refractive astigmatism in girls than in boys,23 although several other studies reported no difference based on sex.1,24 In our study, the mean astigmatism and changes in astigmatism throughout the follow-up period were not significantly different between boys and girls.

There have been few studies on the association between strabismus and astigmatism. In previous studies, astigmatism increased the risk of developing exotropia.25 Longitudinal changes in astigmatism according to ocular alignment have not been reported. In the current study, ocular alignment was significantly correlated with changes in astigmatism in a univariable linear mixed model. However, in the final multivariable model adjusting for the initial extents of SE refractive error and astigmatism, ocular alignment was not a significant predictor of astigmatism.

Our study had several limitations. First, our population was a referral population; therefore, referral bias may have been present, which limits the generalizability of the findings. Although referral bias is indeed a limitation, the study design did allow changes in refractive error to be examined in a large group of patients over an extended follow-up period. Second, this study was retrospective in design; thus, there were different follow-up intervals for different patients. Third, several risk factors known to influence changes in refractive error were not included: the parental history of refractive errors, environmental factors, age when spectacles were first prescribed, and amount of correction. Longitudinal studies of accommodative esotropia have revealed that changes in refractive errors were mostly related to the age when spectacles were first prescribed and the amount of correction.12,13 Further study of the effect of these risk factors on changes in refractive error is needed.

We found that a pediatric referral population in Korea showed a negative shift in SE refractive error and increasing tendency in astigmatism during childhood. Changes in refractive error may be influenced by the initial degree of SE refractive error and astigmatism.

References

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Clinical Characteristics and Demographics of the 221 Patients

VariableInitial No.Initial SE (Mean ± SD) (D)Initial Astigmatism (Mean ± SD) (D)Length of Follow-up (Mean ± SD) (y)
Initial extent of SE
  < −0.50 D57−1.78 ± 1.301.71 ± 1.1611.14 ± 1.80
   −0.50 to 0.75 D780.19 ± 0.661.00 ± 1.0511.21 ± 1.74
  > 0.75 D863.36 ± 2.030.92 ± 0.7311.22 ± 1.89
Initial extent of astigmatism
  < 1.00 D1021.30 ± 2.490.33 ± 0.3011.02 ± 1.73
  1.00 to 3.00 D1020.72 ± 2.631.61 ± 0.6611.36 ± 1.86
  > 3.00 D17−0.19 ± 2.243.38 ± 0.3911.24 ± 1.92
Sex
  Male940.81 ± 2.591.13 ± 0.9811.04 ± 1.71
  Female1271.00 ± 2.551.17 ± 1.0511.31 ± 1.88
Ocular alignment
  Esotropia603.05 ± 2.090.93 ± 0.8711.50 ± 2.01
  Orthotropia960.34 ± 2.721.42 ± 1.0811.00 ± 1.66
  Exotropia65−0.20 ± 1.260.98 ± 1.0011.22 ± 1.80

Results of Linear Mixed Modeling of Changes in SE Refractive Error

VariableModel 1bModel 2c


df Numdf DenFPdf Numdf DenFP
Initial degree of SE × timea22,28923.808< .00122,27714.163< .001
Initial degree of astigmatism × timea22,3780.379.684
Sex × timea12,3790.120.729
Ocular alignment × timea22,38711.504< .00122,2742.491.083

Results of Linear Mixed Modeling of Changes in Astigmatism

VariableModel 1bModel 2c


df Numdf DenFPdf Numdf DenFP
Initial degree of SE × timea22,2003.221.04021,7434.790.008
Initial degree of astigmatism × timea21,82111.369< .00121,74812.860< .001
Sex × timea12,2651.366.243
Ocular alignment × timea22,2473.972.01921,7341.150.317
Authors

From the Department of Ophthalmology, Soonchunhyang University College of Medicine, Soonchunhyang University Seoul Hospital, Seoul, Korea.

Supported by the Soonchunhyang University Research Fund.

The authors have no financial or proprietary interest in the materials presented herein.

Correspondence: Song-hee Park, MD, PhD, Department of Ophthalmology, Soonchunhyang University College of Medicine, Soonchunhyang University Seoul Hospital, 59, Daesagwan-ro, Yongsan-gu, Seoul, 140-743, Korea. E-mail: scheye@hosp.sch.ac.kr

Received: January 28, 2016
Accepted: June 10, 2016
Posted Online: September 27, 2016

10.3928/01913913-20160823-01

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