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Retina  |   November 2014
Macular Measurements Using Spectral-Domain Optical Coherence Tomography in Chinese Myopic Children
Author Affiliations & Notes
  • Si Chen
    Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Peking, People's Republic of China
  • Bingsong Wang
    Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Peking, People's Republic of China
  • Ning Dong
    Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Peking, People's Republic of China
  • Xiaofang Ren
    Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Peking, People's Republic of China
  • Tuohong Zhang
    School of Public Health, Peking University, Peking, People's Republic of China
  • Lin Xiao
    Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Peking, People's Republic of China
  • Correspondence: Lin Xiao, Department of Ophthalmology, Beijing Shijitan Hospital, Capital University of Medical Sciences, Beijing, PR China; wwhbv@163.com
Investigative Ophthalmology & Visual Science November 2014, Vol.55, 7410-7416. doi:10.1167/iovs.14-13894
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      Si Chen, Bingsong Wang, Ning Dong, Xiaofang Ren, Tuohong Zhang, Lin Xiao; Macular Measurements Using Spectral-Domain Optical Coherence Tomography in Chinese Myopic Children. Invest. Ophthalmol. Vis. Sci. 2014;55(11):7410-7416. doi: 10.1167/iovs.14-13894.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose.: To evaluate the macular thickness/volume in Chinese myopic children using spectral-domain optical coherence tomography (SD-OCT) and assess its correlation with spherical equivalent refraction (SER), axial length (AL), sex, and age.

Methods.: A total of 194 eyes from 194 children (aged 6–17 years old) with emmetropia (−0.5 diopters [D] < SER ≤ 0.5 D), low myopia (−3.0 D < SER ≤ −0.5 D), and moderate to high myopia (SER ≤ −3.0 D) were recruited in the study. Each child underwent standardized ophthalmic examinations including visual acuity (VA), cycloplegic refraction, and AL measurement. The macular thickness for the nine Early Treatment Diabetic Retinopathy Study (ETDRS) regions and the average macular thickness/volume were measured and calculated.

Results.: Analyses of macular thickness for the ETDRS regions showed that the fovea was the thinnest of the nine regions, followed by the outer ring; the inner ring was the thickest. When compared to children with emmetropia or low myopia, children with moderate to high myopia tended to have greater foveal thickness, thinner quadrant-specific thickness in the outer ring, and smaller average macular thickness/volume. Also, there were significant differences in foveal, superior outer, inferior outer, and temporal outer quadrants among lowest, middle, and highest AL groups. Boys were found to have greater macular thickness than girls in fovea and inner ring regions.

Conclusions.: Our study highlights the variations and sex differences of macular thickness/volume in Chinese myopic children using SD-OCT.

Introduction
Myopia is a common ocular condition in children, and epidemiologic studies show a progressive increase in the prevalence of the condition, particularly in East Asia in such areas as Singapore, the Chinese mainland, and Hong Kong.1,2 The highest reported prevalence of myopia in children is in urban China, with figures ranging from 5.7% in 5 year olds, 30.1% in 10 year olds, and 78.4% in 15 year olds.1 Myopia is a potentially blinding oculopathy, which is shown to be associated with glaucoma, cataract, and retinal detachment, as well as neovascular macular degeneration.3 The clinical consequences and corresponding economic burden caused by myopia and myopic complications makes it a major and urgent concern.4 Therefore, the assessment of macular parameters such as macular thickness and macular volume in myopic children is of significance when evaluating ocular conditions that are likely to induce macular thickening or thinning.57 
A number of studies have reported the correlation between macular thickness and refractive error or axial length (AL) using a noninvasive method, optical coherence tomography (OCT).6,7 However, the conclusions were partly inconsistent in terms of regional and racial variations. In addition, most of those studies used the time-domain OCT (TD-OCT) modality, which is limited as it fails to include the outer segment (OS) of the photoreceptor inner and outer segment junction (IS/OS) and retinal pigment epithelium (RPE) layers owing to an insufficient axial resolution.8,9 Recently, a new method, spectral-domain OCT (SD-OCT), surpassed the TD-OCT in technology. The advantages of SD-OCT include highly increased image acquisition, approximately twice the axial resolution, relatively reduced motion artifact, and significantly increased signal-to-noise ratio as compared with TD-OCT.8,1015 Accordingly, several studies on macular thickness and volume using SD-OCT have been reported recently among children, young adults, or a wide range of age with one or mixed ethnicity.9,14,1622 However, investigation of macular thickness and its relationship with refractive error or AL in Chinese myopic children using SD-OCT have yet to be reported. 
Therefore, the purpose of this study is to perform a tentative exploration of macular thickness and volume in Chinese myopic children using SD-OCT (Cirrus HD-OCT; Carl Zeiss Meditec, Dublin, CA, USA) and offer a clue for the macular characteristic in this population. 
Materials and Methods
Study Participants
Participants aged from 6 to 17 years were recruited from the ophthalmology clinic of Beijing Shijitan Hospital from October 2012 to October 2013. This study was approved by the Ethics Committee of Beijing Shijitan Hospital, Capital Medical University, Beijing, People's Republic of China. All procedures adhered to the tenets of the Declaration of Helsinki. Informed consents about the nature of this investigation were explained to the children and legal guardians, and written consents were obtained from one legal guardian before the examination was carried out. 
The inclusion criteria were as follows: age between 6 and 17 years, Chinese ethnicity, best corrected visual acuity (BCVA) ≥ 0.8, intraocular pressure (IOP) < 21 mm Hg, normal optic nerve head without an increased cup-disc ratio (≥0.5) or a narrowed neuroretinal rim, no glaucoma family history, no ocular surgery or trauma history, no ocular diseases except for refractive error, and no systemic diseases, including hypertension and diabetes.22 Also, those who could not cooperate on any of the examination procedures were excluded from our study, and only data from the right eye were used for further statistical analysis. Participants in this research were classified by spherical equivalent refraction (SER) as emmetropia (−0.5 diopter [D] < SER ≤ 0.5 D), low myopia (−3.0 D < SER ≤ −0.5D), moderate to high myopia (SER ≤ −3.0 D).6,23 Moreover, participants were separated into three groups according to the tertile levels of AL.6,23 
Eye Examinations
All participants underwent a comprehensive ophthalmologic examination, including assessment of uncorrected visual acuity and BCVA, slit-lamp biomicroscopy, direct funduscopy, and IOP measurement. Additionally, AL was measured using IOL Master (Carl Zeiss, Jena, Germany), and the average of five measurements was recorded when the values differed by less than 0.1 mm and presented no poor signal,18 or the measurements were repeated. Pupillary dilation was induced by atropine for 3 days, three times per day for participants 12 years old or younger, and by four drops of 1% cyclopentolate 5 minutes apart for those older than 12 years. Cycloplegic refraction was assessed by auto-refractometry (Auto Ref-Keratometer RK-F1; Canon, Tokyo, Japan) after pupillary dilation, and the average refractive error values of three repeated measurements were recorded. The SER values were calculated for analysis (SER = spherical error + 50% of cylindrical error). 
Finally, a macular thickness scan was performed by the same experienced technician (CS) in those included subjects, using Cirrus HD-OCT with the macular cube 512 × 128 protocol through the dilated pupil. The right eye was examined first and then the left for each subject. After the participant was properly seated with the examined eye focusing on an internal fixation target and the fovea centered on the scanning laser image, the data were captured within a 6 × 6-mm2 region. The region was parted automatically corresponding to the Early Treatment Diabetic Retinopathy Study (ETDRS).22 Specifically, the thickness of macula was segmented into three concentric circles with diameter of 1 mm, 3 mm, and 6 mm, the thicknesses of which were termed as fovea, inner ring, and outer ring, respectively. Meanwhile, the inner and outer rings were equally divided into four quadrants: superior, nasal, inferior, and temporal. In all, for each eye, thicknesses of nine quadrants and average thickness/volume of the 6 × 6-mm2 macular cube were calculated and presented by the instrument. In addition, the operator was required to ensure that the scans were completely centered, without eye movement or blinking, before saving the images. Only signal strengths of ≥8 were included in the analysis.19,22 
Statistical Analysis
Univariate analysis of variance (ANOVA) was applied to compare macular thickness across the quadrants. One-way ANOVA was used to identify the difference of each macular parameter among groups with emmetropia, low myopia, and moderate to high myopia, and among groups with AL in the lowest, middle, and highest tertiles. A Bonferroni post hoc test was applied for multiple comparisons when any significant difference was recognized in ANOVA. Pearson correlation analysis and partial correlation analysis were used to identify the correlations between macular parameters and SER, AL, age, and sex for all included subjects. Mean ± 1 SD was calculated in the analysis. A P < 0.05 was considered to be statistically significant. All statistical analyses were performed using SPSS for Windows (Version 16.0; Microsoft Corp., Redmond, WA, USA). 
Results
A total of 205 children participated in this study, of which 11 were excluded for the following reasons: poor cooperation for OCT scanning for three boys (two 6 year olds and an 8 year old) and two girls (both aged 7 years), low signal strength in two girls (aged 12 and 15 years) and three boys (two 7 year olds and a 12 year old), and poor scan centration in a 7-year-old boy who had refused to undergo a repeated scan. Finally, 194 children (108 boys, 86 girls) with a mean age of 10.15 ± 2.61 (6–17 years old) were available for further analysis. The mean SER and AL of the 194 eyes from 194 children were −2.25 ± 2.47 D (−11 to 0.5 D) and 24.26 ± 1.39 mm (21.48–27.93 mm), respectively. The mean signal strength of included images was 9.19 ± 0.77 (8–10). 
Analyses of macular thickness for the nine ETDRS regions among all the 194 patients are presented in Figure 1, and the values among different refractive status are presented in Figure 2. Topographically, of the nine regions, the fovea was the thinnest, followed by the outer ring, and the inner ring was the thickest. Quadrant-specific discrepancies were larger in the outer ring compared to the inner ring (P < 0.001). In the inner ring, macular thicknesses in nasal and superior quadrants were the thickest, followed by the inferior quadrant, and macular thickness in temporal quadrant was the thinnest (Univariate ANOVA; P < 0.001). In the outer ring, the nasal macular thickness was the thickest, followed by the superior, inferior, and temporal quadrants (univariate ANOVA; P < 0.001). 
Figure 1
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions using Cirrus HD-OCT. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 1
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions using Cirrus HD-OCT. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 2
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions among different refractive status using Cirrus HD-OCT. (A) Emmetropia, (B) low myopia, (C) moderate to high myopia. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 2
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions among different refractive status using Cirrus HD-OCT. (A) Emmetropia, (B) low myopia, (C) moderate to high myopia. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Comparisons of macular parameters among emmetropia, low myopia, and moderate to high myopia in each ETDRS subfield are presented in Table 1 and Supplementary Figure S1. There were significant differences in the foveal, nasal, inferior, and temporal quadrant in the outer ring among the three study groups (one-way ANOVA; P = 0.045, 0.002, 0.001, and <0.001, respectively). Also, among the three groups, statistically significant differences were identified in the average macular thickness and average macular volume in the 6 × 6-mm2 area (one-way ANOVA; P = 0.004 and 0.004, respectively). No significant differences were detected in the quadrants of the inner ring among the three groups. Further Bonferroni post hoc tests showed that subjects with moderate to high myopia had thicker foveal thickness, thinner macular thickness in outer ring (except for the superior quadrant), and smaller average macular thickness and average macular volume than subjects with emmetropia. 
Table 1
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Emmetropia, Low Myopia, and Moderate to High Myopia
Table 1
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Emmetropia, Low Myopia, and Moderate to High Myopia
Group S1 Group S2 Group S3 P Value* Post Hoc
Emmetropia, n = 58 Low Myopia, n = 74 Moderate to High Myopia, n = 62
Macular thickness, μm
 Fovea 235.22 ± 19.39 240.93 ± 17.35 244.13 ± 22.26 0.045 S3 > S1
 Superior inner ring 319.40 ± 17.95 317.72 ± 14.87 315.50 ± 19.37 0.467
 Nasal inner ring 313.76 ± 27.81 319.09 ± 14.59 315.37 ± 21.06 0.332
 Inferior inner ring 314.36 ± 16.44 313.16 ± 14.72 307.89 ± 18.09 0.067
 Temporal inner ring 306.38 ± 17.16 302.69 ± 14.29 301.97 ± 18.52 0.296
 Superior outer ring 284.31 ± 14.82 283.51 ± 13.03 278.16 ± 24.85 0.122
 Nasal outer ring 302.95 ± 14.56 299.42 ± 14.42 293.40 ± 16.24 0.002 S1 > S3
 Inferior outer ring 269.50 ± 12.14 268.88 ± 15.64 260.85 ± 13.46 0.001 S1 > S3; S2 > S3
 Temporal outer ring 268.31 ± 13.69 263.11 ± 13.00 258.13 ± 14.00 <0.001 S1 > S3
Average macular thickness, μm 285.64 ± 27.95 280.23 ± 11.99 274.34 ± 11.67 0.004 S1 > S3
Average macular volume, mm3 10.00 ± 0.51 10.01 ± 0.43 9.77 ± 0.41 0.004 S1 > S3; S2 > S3
Comparisons of macular parameters among the three groups stratified by tertile of AL in each ETDRS subfield are presented in Table 2 and Supplementary Figure S2. There were significant differences in foveal, superior outer, inferior outer, and temporal outer quadrants among the AL groups (one-way ANOVA; P = 0.011, 0.030, 0.002, and 0.004, respectively). Among the three groups, statistically significant differences were also indentified in the average macular thickness and average macular volume (one-way ANOVA; P = 0.004 and 0.006, respectively). No significant difference was detected in the quadrants of the inner ring. Further Bonferroni post hoc tests showed that subjects with highest AL had thicker foveal thickness, thinner macular thickness in outer ring (except for the nasal quadrant), and smaller average macular thickness and average macular volume than those subjects with lowest AL. 
Table 2
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Lowest, Middle, and Highest Tertile of Axial Length
Table 2
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Lowest, Middle, and Highest Tertile of Axial Length
Group A1 Group A2 Group A3 P Value* Post Hoc
Lowest Tertile (Axial length ≤ 23.51 mm), n = 65 Middle Tertile (23.51 mm < Axial Length ≤ 24.63 mm), n = 65 Highest Tertile (Axial Length > 24.63 mm), n = 64
Macular thickness, μm
 Fovea 236.37 ± 17.93 238.25 ± 17.32 246.22 ± 22.81 0.011 A1 < A3
 Superior inner ring 317.60 ± 17.46 319.06 ± 16.95 315.84 ± 17.65 0.575
 Nasal inner ring 313.83 ± 26.34 317.15 ± 17.39 317.97 ± 19.24 0.507
 Inferior inner ring 312.20 ± 15.53 312.26 ± 17.02 311.03 ± 17.20 0.894
 Temporal inner ring 303.69 ± 16.34 303.35 ± 17.47 303.64 ± 16.27 0.992
 Superior outer ring 285.08 ± 14.51 283.78 ± 13.29 277.19 ± 24.20 0.030 A1 > A3
 Nasal outer ring 300.02 ± 14.79 299.68 ± 13.81 295.92 ± 17.50 0.251
 Inferior outer ring 271.48 ± 13.05 265.18 ± 14.35 262.78 ± 14.66 0.002 A1 > A2; A1 > A3
 Temporal outer ring 265.94 ± 13.14 264.80 ± 14.65 258.41 ± 13.32 0.004 A1 > A3; A2 > A3
Average macular thickness, μm 285.51 ± 26.62 279.72 ± 12.17 274.58 ± 11.60 0.004 A1 > A3
Average macular volume, mm3 10.02 ± 0.50 9.99 ± 0.44 9.78 ± 0.41 0.006 A1 > A3; A2 > A3
Comparisons of macular thicknesses stratified by sex in each ETDRS subfield are presented in Table 3 and Supplementary Figure S3. Boys had significantly thicker macular thickness than girls in the foveal, superior inner, nasal inner, inferior inner, temporal inner, and temporal outer quadrants (independent-sample t-test; P = <0.01, 0.01, 0.04, <0.01, <0.01, and 0.01, respectively). There were no significant differences in average macular thickness and average macular volume between boys and girls. 
Table 3
 
Comparisons of Macular Parameters Between Boys and Girls Measured Using Cirrus HD-OCT
Table 3
 
Comparisons of Macular Parameters Between Boys and Girls Measured Using Cirrus HD-OCT
Boys = 107 Girls = 87 P Value*
Macular thickness, μm
 Fovea 244.99 ± 19.84 234.41 ± 18.36 <0.01
 Superior inner ring 320.36 ± 15.00 314.01 ± 19.31 0.01
 Nasal inner ring 319.16 ± 18.95 312.80 ± 23.55 0.04
 Inferior inner ring 315.42 ± 13.90 307.43 ± 18.40 <0.01
 Temporal inner ring 307.39 ± 14.91 298.85 ± 17.47 <0.01
 Superior outer ring 281.94 ± 16.05 282.16 ± 20.65 0.93
 Nasal outer ring 297.48 ± 14.65 299.87 ± 16.40 0.37
 Inferior outer ring 265.85 ± 13.46 267.30 ± 15.59 0.49
 Temporal outer ring 265.40 ± 14.38 260.21 ± 13.15 0.01
Average macular thickness, μm 278.89 ± 11.86 281.29 ± 24.58 0.41
Average macular volume, mm3 9.94 ± 0.43 9.92 ± 0.50 0.73
Correlation analyses between macular parameters and other variables are shown in Table 4. Macular thickness in the foveal, nasal outer, inferior outer, and temporal outer quadrants were significantly correlated with SER (Pearson correlation analysis; P = 0.003, 0.035, 0.026, 0.003, respectively). Also, the average macular thickness and average macular volume were significantly correlated with SER (Pearson correlation analysis; P = 0.003, 0.014, respectively). However, after adjustment for AL, age, and sex, only the macular thickness in nasal outer quadrant remained significantly correlated with SER (partial correlation analysis; P = 0.004). Macular thickness in foveal, inferior outer, and temporal outer quadrants were significantly correlated with AL (Pearson correlation analysis; P = 0.001, 0.004, 0.003, respectively). Also, the average macular thickness and average macular volume were significantly correlated with AL (Pearson correlation analysis; P = 0.001, 0.008, respectively). However, after adjustment for SER, age, and sex, no correlations between macular thickness/volume and AL remained significant. Significant correlations between macular thickness and age were detected in foveal and superior inner and nasal inner quadrants (Pearson correlation analysis; P = 0.007, 0.050, 0.011); after adjustment for SER, AL, and sex, the correlations in the superior inner and nasal inner quadrants remained significant (partial correlation analysis; P = 0.039, 0.031, respectively). There were significant correlations between macular thickness and sex in fovea, all four quadrants of the inner ring and the temporal outer quadrant (Pearson correlation analysis; P = <0.001, 0.011, 0.039, 0.001, <0.001, and 0.010, respectively), and significant correlations were indentified after adjustment for SER, AL, and age, with the exception of the nasal inner quadrant (partial correlation analysis; P = 0.001, 0.012, 0.002, 0.001, and 0.003, respectively). 
Table 4
 
Correlations Between Macular Parameters and Spherical Equivalent, Axial Length, Age, or Sex Using Pearson Correlation Analysis and Partial Correlation Analysis
Table 4
 
Correlations Between Macular Parameters and Spherical Equivalent, Axial Length, Age, or Sex Using Pearson Correlation Analysis and Partial Correlation Analysis
Spherical Equivalent Axial Length Age Sex
r R r R§ r R|| r R
Macular thickness, μm
 Fovea −0.209* −0.038 0.240* 0.057 0.192* 0.115 −0.266* −0.241†
 Superior inner ring <0.001 0.013 0.009 −0.030 0.141* 0.150† −0.183* −0.181†
 Nasal inner ring −0.088 −0.006 0.093 0.001 0.181* 0.157† −0.149* −0.138
 Inferior inner ring 0.048 0.106 0.024 0.059 0.094 0.122 −0.241* −0.218†
 Temporal inner ring 0.003 0.061 0.056 0.045 0.076 0.079 −0.256* −0.235†
 Superior outer ring 0.001 −0.134 −0.096 −0.178 0.050 0.053 0.006 −0.040
 Nasal outer ring 0.194* 0.206† −0.110 0.123 −0.070 0.025 0.077 0.106
 Inferior outer ring 0.160* 0.007 −0.205* −0.123 0.028 0.104 0.050 0.016
 Temporal outer ring 0.214* 0.047 −0.210* −0.113 −0.001 0.090 −0.184* −0.216†
Average macular thickness, μm 0.209* 0.050 −0.228* −0.085 −0.050 0.040 0.064 0.036
Average macular volume, mm3 0.176* 0.044 −0.190* −0.089 0.020 0.99 −0.025 −0.050
Discussion
In this study, macular measurements were performed to investigate the characteristics of macular thickness and volume in Chinese myopic children using SD-OCT. 
Compared with macular measurements from studies using Heidelberg SD-OCT8,18,20 and Topcon SD-OCT,9,21 the macular thicknesses obtained in the present research using Cirrus HD-OCT were thinner than those using Heidelberg SD-OCT, but were thicker than those using Topcon SD-OCT. The discrepancy among the different SD-OCT devices is probably due to the differences in the way the instruments identify the outer boundary of the retina. The Cirrus HD-OCT measures retinal thickness between the internal limiting membrane (ILM) and the outer border of RPE. In contrast, the Topcon SD-OCT measures retinal thickness from the ILM to the anterior border of RPE, while the Heidelberg SD-OCT measures from the ILM to the RPE-Bruch's membrane–choriocapillaris complex.8,9 Compared with published data on Cirrus HD-OCT,14,19,22 we found that the macular thicknesses in most of the ETDRS regions and average macular thickness/volume in our study were smaller than those in previous reports, especially in the foveal subfield (the difference being 12–14 μm). While we are not sure of the reasons for the difference, we speculate that race, sex, and age might play a role since two of the previous studies focused on Caucasian children14,19 and the other was on young myopic Korean males aged 19 to 25.22 The variations in macular parameters among different races, sex, and age groups need further clarification. 
Our study showed that, as a whole, the fovea was the thinnest region, followed by the outer ring, while the inner ring was the thickest, which is in accordance with most of the previous reports using TD-OCT6,2325 or SD-OCT.9,14,22 Regardless of age, sex, SER, and AL, there was no wide variation in macular thickness among the inner four quadrants, whereas there was a large diversity among the outer four quadrants, with the macular thickness in the outer nasal quadrant being much thicker than the other three quadrants. Ooto et al.9 and Zhang et al.23 deduced that the greater discrepancy of the macular thickness in the outer ring may be owing to the anatomic nature of the retinal nerve fiber layer (RNFL), with vertical symmetry but horizontal asymmetry. Superior and inferior arcuate bundles of nerve fibers were crowded within the inner region of the macula and were relatively dispersed within the outer ring, and the papillomacular bundle within the outer nasal region of the macula led to the nasal quadrant being much thicker than the other three quadrants of the outer ring.9,23 
The comparison of macular thickness in the ETDRS regions among SER groups in our study showed that with worsening degree of myopia, there was a trend toward increasing thickness in the foveal region and thinning in both the inner and outer rings, which was in accordance with most of the previously published studies.6,22,23,25,26 In the comparison of macular thickness among the three tertiles of AL, the fovea was thickest and the outer ring the thinnest in the highest tertile. The outcomes from the present study indicate that the fovea tends to be thicker and the inner and outer rings thinner with increasing degree of myopia or AL. It has been hypothesized that the thinning in the inner and outer rings is due to the mechanical stretching of a similar volume of retina over a larger area, a decrease in the number of photoreceptors, and/or even the early occurrence of chorioretinal atrophy in highly myopic eyes.6,23,26 In contrast, the thickening in the fovea is likely due to myopia-induced pathologic subfoveal chorioretinal changes. The subfoveal blood–retinal barrier permeability has been shown to be significantly higher in form-deprived myopic tree shrews when compared to normal animals.6,23,27 Another possibility supported by myopia modeling in young primates is the alteration of anatomic characteristics of the macula, such as the absence of vasculature leaving the foveal pits deformable in response to retinal stretching induced by ocular growth.23,28,29 
While there was significant correlation between foveal thickness and both SER and AL in the Pearson correlation analysis, there was no significant correlation in the partial correlation analysis. A number of studies have reported significant correlation between macular thickness and SER or AL,6,7,9,22,23,25 but the analyses were not controlled for other possible confounding variables. Our study showed that after adjustment for the other factors, the association between macular thickness and SER or AL was insignificant. Our results concur with the findings of the multivariate analyses of the multicenter Spanish study that evaluated the similar age range (from 4 to 17 years) of subjects and used the same OCT device (Cirrus HD-OCT).14 Neither SER nor AL was independently related to macular thickness after adjusting for other confounding factors. The results indicate that the correlation is more complicated than expected. Many factors, including refractive status, AL, age, sex, race, and other myopia-related biological factors may collectively play a role in determining the macular thickness. 
The sex comparison of macular parameters in the present study showed that boys had significantly thicker macular thickness at the fovea, the four inner quadrants, and the temporal outer quadrant when compared to girls. While significant differences were noted in some quadrants between boys and girls, however, there was no significant difference in average macular thickness and volume. The possible explanation is that the quadrants that have no differences enjoy more weight than the quadrants that have some differences. Taken together, no significant difference was found in average macular thickness and volume. The sex differences were consistent with previous studies conducted both in children and in adults.9,14,2023,30,31 It has been speculated that the intersex discrepancy may be due to differences in the anatomic configurations of the retinal layers beneath the RNFL that constitute most of the retina, and the lack of intersex differences in the outer ring might be attributed to the arcuate (superior and inferior) configuration of RNFL, as the RNFL is relatively thinner in the inner ring compared with the outer ring.9,23 Additionally, Ooto et al.9 attributed the intersex difference in the temporal outer quadrant to the smallest RNFL thickness in the temporal raphe of parafoveal region. As there is relatively insufficient quadrant-related evidence, particularly in SD-OCT reports,9,18,2023,32 further investigations are needed to reveal if the layers of retina or other factors are responsible for the intersex difference. 
There was no significant correlation between age and most quadrants of ETDRS regions when the data were adjusted for SER, AL, and sex in this study. It was in accordance with previous reports on Chinese children, but the results were different when compared to those obtained from Chinese adults using stratus OCT.23,32 Researchers have demonstrated histologically that the decreased number of ganglion cell axons leads to the thinner RNFL in the older age groups,33,34 which may result in a decrease in macular thickness among adults. Barrio-Barrio and colleagues' study in Caucasian children using the Cirrus HD-OCT also identified a significant correlation between age and fovea.14 They recruited children 4 to 17 years old, and 28% (80/283) of them were 4 to 7 years old, whereas the children recruited in our research were older (6–17 years) and 18% (35/196) of them were ≤7 years old. It is possible that some younger eyeballs were still in the physical growth period. Also the mean SER in their study was +0.63 ± 1.65 D (−4.88 to +5.25 D), while the mean SER in ours was −2.25 ± 2.47 D (−11 to 0.5 D). Besides, it has been speculated that ethnicity affects the foveal morphology, and melanin in RPE could alter OCT low-coherence laser light signal by absorbing and scattering light.35,36 The differences in age, SER, as well as ethnicity, may all play a role in the variation of macular measurements.14,18,20,23,3537 
The limitations of the present study include the relatively insufficient number of high myopic children, which may have limited our exploration of their macular characteristics. Also, the results from a monocentric clinic-based study may be less representative than a multicenter- and population-based one. Although the relatively large sample with an even distribution of age and sex in our study may have partly compensated for the shortage, our results need to be further confirmed. Besides, differences in SER might lead to differences in OCT image size. Although too minor to be detected, these differences might have affected our results to some degree. In addition, similar to previously published work,22,23 we have also included only the right eye of each individual for analysis. The biases that may be induced are likely to be minor. 
In conclusion, our study showed that the Chinese myopic children, especially those with moderate to high myopia, have thicker fovea, thinner macular thickness in the inner and outer rings, and smaller average macular thickness/volume in the 6 × 6-mm2 area. However, after adjustment for age, sex, and AL, the correlation between macular thickness/volume and SER were nonsignificant. Furthermore, boys had a thicker central macular thickness compared to girls. Our study demonstrates the characteristics of macular thicknesses in Chinese myopic children. 
Acknowledgments
The authors thank Monisha E. Nongpiur, PhD, for her helpful advice and writing support in the preparation of this manuscript. 
Disclosure: S. Chen, None; B. Wang, None; N. Dong, None; X. Ren, None; T. Zhang, None; L. Xiao, None 
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Footnotes
 SC and BW contributed equally to the work presented here and should therefore be regarded as equivalent authors.
Figure 1
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions using Cirrus HD-OCT. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 1
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions using Cirrus HD-OCT. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 2
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions among different refractive status using Cirrus HD-OCT. (A) Emmetropia, (B) low myopia, (C) moderate to high myopia. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Figure 2
 
Macular thickness for the nine Early Treatment Diabetic Retinopathy Study regions among different refractive status using Cirrus HD-OCT. (A) Emmetropia, (B) low myopia, (C) moderate to high myopia. F, fovea; SI, superior inner quadrant; NI, nasal inner quadrant; II, inferior inner quadrant; TI, temporal inner quadrant; SO, superior outer quadrant; NO, nasal outer quadrant; IO, inferior outer quadrant; TO, temporal outer quadrant.
Table 1
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Emmetropia, Low Myopia, and Moderate to High Myopia
Table 1
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Emmetropia, Low Myopia, and Moderate to High Myopia
Group S1 Group S2 Group S3 P Value* Post Hoc
Emmetropia, n = 58 Low Myopia, n = 74 Moderate to High Myopia, n = 62
Macular thickness, μm
 Fovea 235.22 ± 19.39 240.93 ± 17.35 244.13 ± 22.26 0.045 S3 > S1
 Superior inner ring 319.40 ± 17.95 317.72 ± 14.87 315.50 ± 19.37 0.467
 Nasal inner ring 313.76 ± 27.81 319.09 ± 14.59 315.37 ± 21.06 0.332
 Inferior inner ring 314.36 ± 16.44 313.16 ± 14.72 307.89 ± 18.09 0.067
 Temporal inner ring 306.38 ± 17.16 302.69 ± 14.29 301.97 ± 18.52 0.296
 Superior outer ring 284.31 ± 14.82 283.51 ± 13.03 278.16 ± 24.85 0.122
 Nasal outer ring 302.95 ± 14.56 299.42 ± 14.42 293.40 ± 16.24 0.002 S1 > S3
 Inferior outer ring 269.50 ± 12.14 268.88 ± 15.64 260.85 ± 13.46 0.001 S1 > S3; S2 > S3
 Temporal outer ring 268.31 ± 13.69 263.11 ± 13.00 258.13 ± 14.00 <0.001 S1 > S3
Average macular thickness, μm 285.64 ± 27.95 280.23 ± 11.99 274.34 ± 11.67 0.004 S1 > S3
Average macular volume, mm3 10.00 ± 0.51 10.01 ± 0.43 9.77 ± 0.41 0.004 S1 > S3; S2 > S3
Table 2
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Lowest, Middle, and Highest Tertile of Axial Length
Table 2
 
Comparison of Macular Parameters Measured Using Cirrus HD-OCT Among Lowest, Middle, and Highest Tertile of Axial Length
Group A1 Group A2 Group A3 P Value* Post Hoc
Lowest Tertile (Axial length ≤ 23.51 mm), n = 65 Middle Tertile (23.51 mm < Axial Length ≤ 24.63 mm), n = 65 Highest Tertile (Axial Length > 24.63 mm), n = 64
Macular thickness, μm
 Fovea 236.37 ± 17.93 238.25 ± 17.32 246.22 ± 22.81 0.011 A1 < A3
 Superior inner ring 317.60 ± 17.46 319.06 ± 16.95 315.84 ± 17.65 0.575
 Nasal inner ring 313.83 ± 26.34 317.15 ± 17.39 317.97 ± 19.24 0.507
 Inferior inner ring 312.20 ± 15.53 312.26 ± 17.02 311.03 ± 17.20 0.894
 Temporal inner ring 303.69 ± 16.34 303.35 ± 17.47 303.64 ± 16.27 0.992
 Superior outer ring 285.08 ± 14.51 283.78 ± 13.29 277.19 ± 24.20 0.030 A1 > A3
 Nasal outer ring 300.02 ± 14.79 299.68 ± 13.81 295.92 ± 17.50 0.251
 Inferior outer ring 271.48 ± 13.05 265.18 ± 14.35 262.78 ± 14.66 0.002 A1 > A2; A1 > A3
 Temporal outer ring 265.94 ± 13.14 264.80 ± 14.65 258.41 ± 13.32 0.004 A1 > A3; A2 > A3
Average macular thickness, μm 285.51 ± 26.62 279.72 ± 12.17 274.58 ± 11.60 0.004 A1 > A3
Average macular volume, mm3 10.02 ± 0.50 9.99 ± 0.44 9.78 ± 0.41 0.006 A1 > A3; A2 > A3
Table 3
 
Comparisons of Macular Parameters Between Boys and Girls Measured Using Cirrus HD-OCT
Table 3
 
Comparisons of Macular Parameters Between Boys and Girls Measured Using Cirrus HD-OCT
Boys = 107 Girls = 87 P Value*
Macular thickness, μm
 Fovea 244.99 ± 19.84 234.41 ± 18.36 <0.01
 Superior inner ring 320.36 ± 15.00 314.01 ± 19.31 0.01
 Nasal inner ring 319.16 ± 18.95 312.80 ± 23.55 0.04
 Inferior inner ring 315.42 ± 13.90 307.43 ± 18.40 <0.01
 Temporal inner ring 307.39 ± 14.91 298.85 ± 17.47 <0.01
 Superior outer ring 281.94 ± 16.05 282.16 ± 20.65 0.93
 Nasal outer ring 297.48 ± 14.65 299.87 ± 16.40 0.37
 Inferior outer ring 265.85 ± 13.46 267.30 ± 15.59 0.49
 Temporal outer ring 265.40 ± 14.38 260.21 ± 13.15 0.01
Average macular thickness, μm 278.89 ± 11.86 281.29 ± 24.58 0.41
Average macular volume, mm3 9.94 ± 0.43 9.92 ± 0.50 0.73
Table 4
 
Correlations Between Macular Parameters and Spherical Equivalent, Axial Length, Age, or Sex Using Pearson Correlation Analysis and Partial Correlation Analysis
Table 4
 
Correlations Between Macular Parameters and Spherical Equivalent, Axial Length, Age, or Sex Using Pearson Correlation Analysis and Partial Correlation Analysis
Spherical Equivalent Axial Length Age Sex
r R r R§ r R|| r R
Macular thickness, μm
 Fovea −0.209* −0.038 0.240* 0.057 0.192* 0.115 −0.266* −0.241†
 Superior inner ring <0.001 0.013 0.009 −0.030 0.141* 0.150† −0.183* −0.181†
 Nasal inner ring −0.088 −0.006 0.093 0.001 0.181* 0.157† −0.149* −0.138
 Inferior inner ring 0.048 0.106 0.024 0.059 0.094 0.122 −0.241* −0.218†
 Temporal inner ring 0.003 0.061 0.056 0.045 0.076 0.079 −0.256* −0.235†
 Superior outer ring 0.001 −0.134 −0.096 −0.178 0.050 0.053 0.006 −0.040
 Nasal outer ring 0.194* 0.206† −0.110 0.123 −0.070 0.025 0.077 0.106
 Inferior outer ring 0.160* 0.007 −0.205* −0.123 0.028 0.104 0.050 0.016
 Temporal outer ring 0.214* 0.047 −0.210* −0.113 −0.001 0.090 −0.184* −0.216†
Average macular thickness, μm 0.209* 0.050 −0.228* −0.085 −0.050 0.040 0.064 0.036
Average macular volume, mm3 0.176* 0.044 −0.190* −0.089 0.020 0.99 −0.025 −0.050
Supplementary Figures
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