Long-term longitudinal changes in astigmatism and their effect on refraction development in school-age children in southern China

doi:10.21203/rs.3.rs-3400127/v1

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Long-term longitudinal changes in astigmatism and their effect on refraction development in school-age children in southern China

https://doi.org/10.21203/rs.3.rs-3400127/v1

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Objectives: To investigate longitudinal changes in astigmatism in school-age children and to explore the effect of astigmatism on refraction development.
Methods: The medical records of patients with long-term follow-up data from 2006 to 2018 were retrospectively reviewed. Patients who were 6-10 years old at initial visit and 16 years old at last assessment were selected for analysis. The enrolled patients had a cylinder refraction of 0.75 or greater. Astigmatism was analyzed in clinical notation and vector notation(J0, J45). The related factors of changes in astigmatism and sphericalequivalent per year and the interaction between the two were analyzed.

Results: A total of 3101 patients(median age 9 years at initial visit) were followed up for an average of 7 years(IQR, 6–8 years). The mean cylinder refraction at initial examination was 2.11±1.18Dand decreased to 2.08±1.18Dat 16 years old, which was statistically(p=0.034) but not clinically significant. The Oblique astigmatism(J45, 0.005D/y) increased and with-the-rule astigmatism(J0, -0.008D/y) decreased. A lower magnitude of astigmatism and more myopia of the SE at the initial visit were associated with a greater increase in astigmatism magnitude(p<0.001). A higher magnitude of initial astigmatism was associated with less progression in spherical equivalent(p<0.001).

Conclusion: In southern Chinese children, the mean cylinder power decreased slightly from 6-10 to 16 years of age, accompanied by a progression of the oblique axis and a reduction of with-the-rule axis. The presence of myopia at baseline was a risk factor for astigmatism progression. However, high astigmatism seems to prevent reductions in the spherical equivalent.

Health sciences/Signs and symptoms

Health sciences/Diseases

Astigmatism is a highly prevalent refractive error worldwide, frequently coexisting with myopia and hyperopia. There have been population-based reports on the prevalence of astigmatism in children from different ethnic groups, and the prevalence of astigmatism in school-aged children is generally higher in East Asian populations than in other ethnicities.^1–4 Eyelid pressure is most likely to be involved in the development of corneal astigmatism.⁵ Higher lid tension in Asian populations is suggested to be an associated factor leading to a higher prevalence of astigmatism.⁶ Eyelid pressure should change as children age, and the long-term trend of astigmatism in children is not clear.

In addition, Gwiazda et al.⁷ analyzed the functional significance of astigmatism in emmetropization and the development of myopia, finding that infantile astigmatism is associated with increased astigmatism and myopia in childhood. Furthermore, the association of astigmatism with increasing myopia in school-age Asian populations raises the question of whether the presence of astigmatism contributes to the development of myopia.⁸ A few studies have investigated longitudinal changes in refractive astigmatism and their effects on refractive development in children. Most of these studies are short-term and the majority of them focused on pre-school children. For example, Chan et al. ⁹ studied the progression of astigmatism in primary school children and its effect on myopic shift in southern Taiwan over a 1-year period. They found that the astigmatism decreased during the one-year follow-up and was not associated with myopia progression. Fan et al.¹⁰ studied the progression of astigmatism and its effect on refractive development in preschool children in Hong Kong with a follow-up of 55.7 months. They reported that a significant percentage of children had stable and even increased astigmatism. In addition, children with increased astigmatism had greater myopic progression.

The incidences of both astigmatism and myopia are very high in school-age children in southern China^2,11. However, the developmental interplay between the two has not been explored in this population. In this study, data collected in a large cohort with astigmatism of ≤-0.75 D in Wenzhou city were analyzed retrospectively. All patients were evaluated until they were 16 years old based on the Correction of Myopia Evaluation Trial (COMET) study.¹² The longitudinal changes in astigmatism, the factors associated with the changes, and the effects of astigmatism on refraction development were assessed.

Study population

We retrospectively and inclusively reviewed the clinical records of patients seeking refractive error corrections at Wenzhou Medical University Affiliated Eye Hospital between 2006 and 2018. Patients who were both diagnosed with an astigmatism of ≤-0.75 D in both eyes at 6–10 years old and tracked until the age of 16 years were included. All patients included underwent at least two refractive error evaluations (at the initial visit and at 16 years of age) during this follow-up period. Children with ocular or systemic disorders that are potentially associated with astigmatism and myopia, such as keratoconus and Marfan syndrome, as well as children with chronic eye disorders, such as congenital cataracts and nystagmus, were excluded. Children with a history of wearing corneal contact lenses that may interfere with the characteristics of astigmatism were also excluded. The study was approved by the Ethics Board of Wenzhou Medical University Affiliated Eye Hospital and was performed according to the tenets of the Declaration of Helsinki.

Measurements and definitions

All patients underwent a comprehensive ophthalmologic examination, which included visual acuity (VA), refraction, slit-lamp, fundoscopy, and orthoptic evaluations, at every follow-up. Cycloplegic refractions were performed at the initial visit. Cycloplegia was induced with 2 drops of 1% cyclopentolate hydrochloride instilled 5 minutes apart or 1% atropine ointment administered twice a day for three consecutive days. For the recovery of tonic accommodation, the refraction or prescription was determined in the natural state of the eye after 3 weeks for patients who used atropine ointment and 3 days for patients who used Scyclopentolate hydrochloride. Noncycloplegic refractions were performed at the follow-up visits. Refraction was first performed using an autorefractor (KR8800, Topcon Corp, Tokyo, Japan), followed by subjective refraction. Subjective refractions were performed by 25 optometrists trained to perform assessments with a standardized protocol at Wenzhou Medical University Affiliated Eye Hospital, and the methodology followed was the same as that described in a previous study.¹³ The endpoint was the least myopic spherical power providing the best VA.

The spherical equivalent (SE) and refractive astigmatism were included in the analyses. SE was calculated as the spherical dioptric power plus one-half of the cylindrical dioptric power. Astigmatism data were analyzed in clinical notation (Cyl, representing the magnitude of astigmatism without regard to the axis) and in vector notation (J0 [Jackson cross-cylinder with axes at 180° and 90°] and J45 [Jackson cross-cylinder with axes at 45° and 135°).¹⁴ The axis of the cylinder was classified as against-the-rule if the minus cylinder axis was at 90 ± 22.5°. The axis of the cylinder was classified as with-the-rule if the minus cylinder axis was between 0 and 22.5° or between 157.5 and 180°. All measurements in between these ranges were classified as oblique.⁷ The slope (representing estimated change per year) in the abovementioned refractive errors over the follow-up period was defined as the difference between the final and initial refractive errors divided by the follow-up duration in years.

Statistical Analysis

The data from the right eye were selected for analysis because both astigmatism and SE were highly correlated between the right and left eyes (r = 0.925 and 0.941, respectively, p < 0.001). One-sample t-tests were performed to determine if the mean slope (change/y, D) was significantly different from 0 for each measure of astigmatism (Cyl, J0, and J45). Multivariate analysis of covariance (ANCOVA) was used to determine if slopes for measures of astigmatism and SE differed by the magnitude of the baseline astigmatism measurement (Cyl, low astigmatism [0.75 D to < 1.50 D], moderate astigmatism [1.50 to < 3.00 D], or high astigmatism [≥ 3.00 D]). A second ANCOVA was used to determine if slopes for measures of astigmatism and SE differed by the magnitude of the baseline astigmatism measurement by magnitude of the baseline SE (moderate to high hyperopia [ ≥ + 3.00 D], low hyperopia [+ 0.75 to < + 3.00 D], emmetropia [-0.25 to < + 0.75 D], low myopia [-3.00 to <-0.25 D], or moderate to high myopia [<-3.00 D]). Age at the initial visit and sex were included in ANCOVA as covariates. Multiple linear mixed-effect regression models were used to determine whether the astigmatism measurement, SE, or age at the initial visit or sex were associated with the mean slope in Cyl or SE.

A total of 3101 patients were included in the analysis (57.3% male; 42.7% female). The median age of the patients at the initial visit was 9 years (IQR: 8–10 years). There were 159 six-year-olds, 389 seven-year-olds, 614 eight-year-olds, 838 nine-year-olds and 1101 ten-year-olds. All patients were 16 years old at the final visit. The median duration of follow-up was 7 years (IQR, 6–8 years). Twenty nine percent of the patients had refractive evaluation at least once a year, 91.1% had refractive evolution at least once every two years, and 97.5% had refractive evolution at least once every 3 years.

Changes in astigmatism and its influencing factors

From the initial visit to 16 years of age, the proportion of with-the-rule astigmatism decreased while the proportion of against-the-rule and oblique astigmatism increased (p < 0.001, Fig. 1). The astigmatism measurements at the initial examination and at 16 years of age were presented in Table 1 and plotted in Fig. 2. A positive slope of Cyl represents an increase in astigmatism magnitude with age, and vice versa. The mean Cyl slope was − 0.006 D/y, which was significantly different from 0 (p < 0.001). For measurements of J0, a positive slope represents a shift toward an increase in with-the-rule astigmatism and/or a reduction in against-the-rule astigmatism. There was a significant negative mean slope in J0 (-0.008 D/y, p < 0.001). For measurements of J45, a positive slope represents an increase in astigmatism at axis 135° and/or a reduction in astigmatism at axis 45°. There was a significant positive mean slope in J45 (0.005 D/y, p < 0.001).

Table 1

Summary of Sample Characteristics at baseline and the assessment at 16 years of age
Variable	Initial visit	16 years of age	P value
Mean Cyl (D)	-2.11 ± 1.18	-2.08 ± 1.18	0.034
WTR (No. %)	2980(96.1)	2816(90.8)	< 0.001
OBL (No. %)	87(2.8)	235(7.6)	< 0.001
Mean J0 (D)	1.00 ± 0.62	0.94 ± 0.64	0.767
Mean J45 (D)	0.02 ± 0.29	0.06 ± 0.36	< 0.001
SE (D)	+ 0.02 ± 3.55	-3.29 ± 4.28	< 0.001
Cyl: cylinder, WTR: with-the-rule axis, OBL: oblique axis, SE: spherical equivalent

The results of the ANCOVA yielded statistically significant effects of the amount of astigmatism at baseline on the mean Cyl and J0 slope (Table 2). With the increase in baseline astigmatism magnitude, both the Cyl and J0 slopes gradually became negative (p < 0.001). There was no significant difference in the J45 slope among different degrees of astigmatism (p = 0.176). In addition, there was no significant effects of axial direction (with-the-rule, against-the-rule or oblique) on the mean Cyl slope (p = 0.537).

Table 2

Summary of mean astigmatism measurements and SE slope (D/Y) by amount of astigmatism and SE at baseline
Amount of astigmatism at baseline	n	Cyl slope	J0 slope	J45 slope	SE slope
0.75 D to < 1.50 D	1040	0.025 ± 0.03	0.011 ± 0.002	0.05 ± 0.001	0.570 ± 0.010
1.50 to < 3.00 D	1251	-0.008 ± 0.02	-0.009 ± 0.009	0.003 ± 0.002	0.538 ± 0.009
≥ 3.00 D	801	-0.048 ± 0.03	-0.035 ± 0.002	0.007 ± 0.002	0.519 ± 0.011
p		< 0.001	< 0.001	0.176	0.003
Amount of SE at baseline
≥+3.00 D	500	-0.016 ± 0.004	-0.019 ± 0.003	-0.006 ± 0.003	0.530 ± 0.015
+ 0.75 to < + 3.00 D	467	-0.023 ± 0.004	-0.018 ± 0.003	-0.004 ± 0.003	0.510 ± 0.015
-0.25 to < + 0.75 D	582	-0.020 ± 0.004	-0.016 ± 0.003	0.008 ± 0.002	0.561 ± 0.013
-3.00 to < -0.25 D	1186	0.000 ± 0.003	-0.004 ± 0.002	0.004 ± 0.002	0.549 ± 0.009
<-3.00 D	366	0.019 ± 0.005	0.004 ± 0.003	0.024 ± 0.003	0.568 ± 0.017
p		< 0.001	< 0.001	< 0.001	0.041
Cyl: cylinder, SE: spherical equivalent

The results of the ANCOVA also yielded statistically significant effects of the amount of SE on slopes for measures of astigmatism (Table 2). The mean Cyl slopes for the myopic groups were significantly more positive than those for the emmetropia and hyperopic groups (p ≤ 0.001). In the myopic groups, this value for moderate to high myopia was more positive than that for low myopia (p < 0.001). The J0 slope for myopia groups were significantly more positive than that for hyperopia groups (p ≤ 0.032). The J45 slope for the moderate to high hyperopic group was significantly more negative than other groups (p ≤ 0.001). This value for moderate to high myopia was more positive than that for low myopia and emmetropia (p ≤ 0.002).

Changes in SE and its influencing factors

The mean SE at the initial and last examination was presented in Table 1. A positive slope represents a decrease (shift toward more myopia with age) in SE and the mean SE slope was 0.54 ± 0.33 D per year.

The results of the ANCOVA yielded statistically significant effects of the amount of astigmatism at baseline on the mean SE slope (Table 2). The mean SE slope for low astigmatism was more positive than for moderate (p = 0.022) and high astigmatism (p = 0.001. The amount of SE at baseline also had statistically significant effects on the SE slope. The mean SE slopes for myopia and emmetropia groups were more positive than that for the low hyperopia group (p ≤ 0.026). The results of the ANCOVA did not show statistically significant effects of axial direction (with-the-rule, against-the-rule or oblique) on the mean SE slope (p = 0.966).

To investigate the related factors of in slope of Cyl and SE, multivariate linear mixed-effect models were applied to examine age, SE, and Cyl at the initial visit as well as sex (see Table 3). The correlation between the initial Cyl or SE and the slope of them were consistent with the above ANCOVA results. Interestingly, sex was related to the rate of change in Cyl (p < 0.001), with girls showing a decrease in Cyl (-0.019 D/y) and boys showing the opposite (0.04 D/y). Figures 3 and 4 show the association between initial cylinder refraction or SE with the slope of astigmatism measurements and SE, respectively.

Table 3

Linear mixed-effect models for the associations of the slope for astigmatism and SE with sex and age, astigmatism and SE at the initial visit
	Cyl slope		SE slope
Characteristics	β (95% CI)	p	β (95% CI)	p
Initial Cyl	-0.025(-0.028,0.023)	< 0.001	-0.019(-0.030, -0.008)	0.001
Initial SE	-0.004(-0.005, -0.003)	< 0.001	-0.004(-0.007, -0.001)	0.023
Age	0(-0.002,0.002)	0.983	0.059(0.049,0.068)	< 0.001
Sex	-0.023(-0.029,0.017)	< 0.001	0.003(-0.020.0.026)	0.814
Cyl: cylinder, SE: spherical equivalent, CI: confidence interval

The present longitudinal study has the largest sample size and the longest study period among studies investigating the changes in astigmatism as well as the interrelationship between astigmatism and spherical equivalent in school-age children. It was found that astigmatism decreased between 6–10 and 16 years of age, especially in those with a high magnitude of astigmatism. Furthermore, astigmatism and spherical equivalents may influence each other’s progression.

Similar to earlier studies, with-the-rule astigmatism was predominant in the present study.^8,15 Leung et al.⁸ reported that with-the-rule and against-the-rule astigmatism showed dramatic changes between childhood (3–10 years old) and 60 years of age, from 92.6–2.7% and from 2.9–79.7%, respectively. They also reported that the proportion of patients with oblique astigmatism changed less dramatically across the age cohorts compared with those of patients with against-the-rule and with-the-rule astigmatism. Specifically, oblique astigmatism increased in the youngest age group from 4.4% to a peak at 23.6%. The current study tracked the changes in astigmatism in school-age children from 6–10 years of age to 16 years of age. With-the-rule astigmatism and oblique astigmatism change in opposite ways to almost the same extent, while the increase in against-the-rule astigmatism was very slight. Analyzed in junction with the study by Leung et al.⁸, it can be implied that the with-the-rule axis tends to develop toward the oblique axis from childhood to adolescence and later shifts to the against-the-rule axis. Grosvenor¹⁶ proposed a theory for the etiology of astigmatism which states that the band of pressure from the upper eyelid on the cornea causes the eye to exhibit with-the-rule astigmatism. The shift in the astigmatic axis from with-the-rule in children to oblique in adolescents and against-the-rule in older adults could be explained by a reduction in lid tension with age, leading to a reduction in WTR corneal astigmatism.

Results on the development of astigmatism with age are mixed, and there are very few long-term longitudinal studies of school-age children. Huynh et al.¹⁷ reported that astigmatism is stable between ages 6 and 12 years. Tong et al.¹⁸ investigated the progression in children of various ethnicities aged 7 to 9 years over a 4-year period, and found that, while astigmatism progressed from 0.44 D to 0.53 D and the J0 change per year was 0.012 D, J45 did not show a significant change. Sherrill et al.¹⁹ observed that in children aged 3 to 11 years, astigmatism tended to show a reduction with age, whereas children aged 12 to 19 years showed a consistent increase. Furthermore, the younger and older cohorts also differed significantly on J0 and J45 slopes for astigmatism. Since age and ethnicity affects astigmatism and its progression^17,18, the inconsistency of the above-mentioned studies could be contributed to sample differences in age or ethnicity. The results of the current study indicate that astigmatism decreased by 0.03D from age 6–10 to 16 years in southern China, while accompanied by a reduction in J0 and a progression in J45. Age and ethnicity may also explain the inconsistency of the present study with the above studies.

In addition to age and ethnicity, sex could also affect changes in astigmatism. Findings of previous studies on sex differences in astigmatism have been inconsistent. Several studies reported slightly higher prevalence rates of refractive astigmatism in girls than in boys^15,20, some found the opposite^21,22, and several other studies reported no sex differences^23,24. There was no difference in the percentage of boys and girls in the present study. Interestingly, astigmatism decreased in girls but increased in boys during the study period. This is consistent with the results from Tong et al.¹⁸, which suggested that the 3-year cumulative incidence rate of astigmatism for boys was slightly higher than that for girls. However, results from the present study are not consistent with the results from Zhao et al.²⁵, which showed that the reduction in the cylinder was not associated with sex on multiple regression.

Additionally, the current study investigated the effects of basic astigmatism magnitude on astigmatism progression and found that both astigmatism magnitude and J0 decreased more as the basic astigmatism magnitude increased. These results were inconsistent with the results reported by Harvey et al.¹⁹, which implied that both the clinical and vector notation of astigmatism progressed more for high astigmatism. Future studies should be conducted to elucidate the effects of basic astigmatism magnitude on astigmatism progression. Myopic children were found to had increased astigmatism, while nonmyopic children had reduced astigmatism in the current study. Nevertheless, J0 and J45 also tended to progress more in children with higher myopic SE. These results agreed with Tong et al.¹⁸, who indicated that the incidence of astigmatism was five times greater in patients with myopia than in those without myopia. Liang et al.²⁶ also reported a significant increase in astigmatism and myopia in children after studying at home during COVID-19 lockdown. The findings from the present study are in line with these studies suggesting that myopia may be associated with increased astigmatism.

An important objective of this study was to evaluate the effects of basic refraction, especially astigmatism, on the development of refraction. The refraction of children with myopia was found to be changed more than that of children with hyperopia, which implied that the degree of myopia progression in children was greater than the degree of hyperopia regression. This is consistent with previous studies reporting that myopic children have a greater myopic shift than those without myopia.^10,27,28 However, a higher magnitude of astigmatism at the initial visit was associated with less progression in the spherical equivalent in the current study, which is inconsistent with previous studies. Infantile astigmatism was thought to be correlated with increasing myopia in childhood.⁷ Fulton et al.²⁹ found that younger children (< 3 years) with astigmatism tended to have increased myopia. Fan et al.¹⁰ also reported that the presence of astigmatism, particularly with increasing astigmatism, appeared to predispose preschool children to progressive myopia. Therefore, astigmatism is thought to blur visual images and thus may promote the development of myopia. It is important to note that all of these studies involved preschoolers, although Gwiazda et al.⁷ reported that infantile astigmatism could influence myopia progression in childhood. Chan et al.⁹ found that subjects without astigmatism had more myopic changes in childhood, which agrees with results from the present study. There are two possible explanations for the present results. First, less astigmatism is associated with more positive SE, which is calculated as sphere plus cylinder. Astigmatism decreased more as the magnitude of basic astigmatism increased in the present study, which may explain the result that children with higher astigmatism experienced less myopic shift. Second, Vyas and Kee³⁰ studied the effects of optically imposed astigmatism on myopia development in chickens and found that compared to spherical lenses, the presence of astigmatic blur imposed by sphero-cylindrical lenses induced fewer myopic errors. Nevertheless, chickens that wore high cylinder lenses developed less myopia, which was consistent with results from the present study. More clinical and animal trials are needed to confirm the results.

There are some limitations of the current study. First, the refractive error was determined by noncycloplegic autorefraction followed by subjective refraction at the follow-up visit. Assessing refractive error in the absence of cycloplegia may lead to overestimations of myopic power³¹ and shifts of J0 or J45³², even when subjective refraction is performed. Second, although each child was observed for a long time, the differences in astigmatism and SE changes in children of different age groups could not be distinguished due to an insufficient number of examinations. Third, the sample in this study was taken from optometry clinics. These clinics may have higher levels of astigmatism than the general population. Despite these limitations, however, the present study is helpful in understanding the longitudinal development of astigmatism and the relationship of astigmatism to spherical equivalent development.

To summarize, in southern Chinese school children, the mean cylinder power decreased slightly from 6–10 to 16 years of age, which is accompanied by a reduction in J0 and a progression in J45. The changes in astigmatism and spherical equivalent were related. The present study supports that the presence of myopia at baseline is a risk factor for astigmatism progression. Interestingly, the higher the basic astigmatism, the slower the SE reduction. The present study would support future investigations of clinical interventions for altering the course of increasing astigmatism or to control myopia progression during childhood.

Funding/Support: Funded by Wenzhou Municipal Science and Technology Bureau (Grant No. Y20210974).

Author Contribution Statement: ZEQ was responsible for preparing material, collecting and analyzing data. QLZ was responsible for creating tables and figures. She also contributed to collecting and analyzing data. WHC was responsible for designing the research and writing the manuscript. XPY was responsible for designing the research. JC contributed to revising the manuscript.

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Long-term longitudinal changes in astigmatism and their effect on refraction development in school-age children in southern China

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Study population

Measurements and definitions

Statistical Analysis

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Changes in astigmatism and its influencing factors

Changes in SE and its influencing factors

Discussion

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