Analysis of macular vascular density and retinal thickness of school-age children_Chinese Journal of Ocular Fundus Diseases

Authors：

 Gao Shasha ¹ , Shang Lili ¹ , Fu Aicun ¹ , Chang Minghang ¹ , He Yin ¹ , Wang Ming ¹ , Jin Xuemin ¹ , Lei Bo ² , Zhang Fengyan ¹

1. The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450000, China;
2. Henan Eye Institute, Henan Eye Hospital, Henan Provincial People's Hospital, Zhengzhou 450003, China;

Corresponding author：

Gao Shasha, Email: shashag@126.com

Keywords：

Swept-source optical coherence tomography angiography; Child; Macular vascular density; Retinal thickness

DOI：

10.3760/cma.j.cn511434-20230612-00262

Video：

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Objective To observe the correlation between retinal capillary density and retinal thickness in the macula and spherical equivalent (SE) in school-age children. Methods A cross-sectional study. From May to December 2022, 182 school-age children who visited the ophthalmology department of the First Affiliated Hospital of Zhengzhou University were included . There were 95 males and 87 females. The age ranged from 6 to 12 years, and the spherical equivalent (SE) was +0.50 to －6.00 D. They were divided into three groups based on the SE of the right eyes: 54 eyes in emmetropia group (+0.50≤SE＜－0.50 D), 71 eyes in low myopia group (－0.50≤SE＜－3.00 D), and 57 eyes in moderate myopia group (－3.00≤SE≤－6.00 D). The macular area of 6 mm×6 mm was scanned using swept-source optical coherence tomography angiography and was divided into three concentric rings centered on the fovea, including the macular central fovea (0-1 mm diameter), inner ring (1-3 mm diameter) and outer ring (3-6 mm diameter). The retinal thickness and blood flow density of superficial vascular plexus (SVP) and deep vascular plexus (DVP) in different zones within 6 mm of the macular area were measured. The relationships between SE and SVP, DVP and retinal thickness in each ring region were investigated by univariate and multivariate linear regression analyses, smooth curve fitting, and threshold effects. Results There were significant differences in the SVP (F=6.64, 26.06, 22.69) and DVP (F=7.97, 25.01, 5.09) of macular central fovea, inner ring and outer ring among the emmetropia, low myopia and moderate myopia groups (P＜0.05). Univariate linear regression analysis showed that the SVP (β=－0.56, －1.17, －0.79) and DVP (β=－1.03, －0.93, －0.45) of the three regions were positively correlated with SE (P＜0.05). After smooth curve fitting, threshold effect analysis and multivariate linear regression analysis, the SVP and DVP in the macular central fovea were linearly positively correlated with SE (β=－0.91, －1.40; P＜0.05), and SVP and DVP in the inner ring and outer ring showed an inverted U-shaped curve relationship with SE with the inflection (＜3.00 D). When the SE was less than ＜3.00 D, the SVP and DVP in the inner ring and outer ring were positively correlated with SE (P＜0.05). When the SE was higher than －3.00 D, except for the DVP in the inner ring region, the other parameters were negatively correlated with SE (P＜0.05). There were significant differences in retinal thickness of the inner ring and outer ring (F=5.47, 16.36; P＜0.05), and no significant difference in the macular central fovea among the emmetropia, low and moderate myopia groups (F=2.16, P＞0.05). By using univariate and multivariate linear regression analyses, the retinal thickness in the inner ring and outer ring were negatively correlated with SE (β =1.99, 3.05; P＜0.05). However, no correlation was found between retinal thickness and SE in the macular central fovea (β=－1.65, P＞0.05). Conclusions In school-age children with SE between +0.50 D and －6.00 D, the retinal capillaries density of the macular central fovea gradually increase, and increase first and then decrease in the inner ring and outer ring with increasing SE. The retinal thickness of inner ring and outer ring gradually decrease and not change significantly in the macular central fovea.

Citation： Gao Shasha, Shang Lili, Fu Aicun, Chang Minghang, He Yin, Wang Ming, Jin Xuemin, Lei Bo, Zhang Fengyan. Analysis of macular vascular density and retinal thickness of school-age children. Chinese Journal of Ocular Fundus Diseases, 2024, 40(1): 44-51. doi: 10.3760/cma.j.cn511434-20230612-00262 Copy

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5.	Jia Y, Bailey ST, Wilson DJ, et al. Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration[J]. Ophthalmology, 2014, 121(7): 1435-1444. DOI: 10.1016/j.ophtha.2014.01.034.
6.	Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography[J]. JAMA Ophthalmol, 2015, 133(1): 45-50. DOI: 10.1001/jamaophthalmol.2014.3616.
7.	Gołębiewska J, Biała-Gosek K, Czeszyk A, et al. Optical coherence tomography angiography of superficial retinal vessel density and foveal avascular zone in myopic children[J/OL]. PLoS One, 2019, 14(7): e0219785[2019-07-18]. https://pubmed.ncbi.nlm.nih.gov/31318910/. DOI: 10.1371/journal.pone.0219785.
8.	刘玉婷, 雷颖庆, 田敏, 等. 不同屈光度近视青少年儿童黄斑区血管密度和视网膜厚度的比较[J]. 国际眼科杂志, 2021, 21(5): 789-795. DOI: 10.3980/j.issn.1672-5123.2021.5.08.Liu YT, Lei YQ, Tian M, et al. Comparison of macular vascular density and retinal thickness in children with different degrees of myopia[J]. Int Eye Sci, 2021, 21(5): 789-795. DOI: 10.3980/j.issn.1672-5123.2021.5.08.
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11.	Kur J, Newman EA, Chan-Ling T. Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease[J]. Prog Retin Eye Res, 2012, 31(5): 377-406. DOI: 10.1016/j.preteyeres.2012.04.004.
12.	徐珊珊, 陈一芳, 端宁茜, 等. 基于OCTA的单眼近视患儿黄斑区视网膜毛细血管血流密度及厚度分析[J]. 国际眼科杂志, 2022, 22(6): 926-930. DOI: 10.3980 /j.issn.1672-5123.2022.6.08. DOI: 10.3980/j.issn.1672-5123.2022.6.08.Xu SS, Chen YF, Duan NQ, et al. Analysis of vascular density and thickness in macular retina of monocular myopic adolescents using OCTA[J]. Int Eye Sci, 2022, 22(6): 926-930. DOI: 10.3980/j.issn.1672-5123.2022.6.08.
13.	Laties AM. Central retinal artery innervation. Absence of adrenergic innervation to the intraocular branches[J]. Arch Ophthalmol, 1967, 77(3): 405-409. DOI: 10.1001/archopht.1967.00980020407021.
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15.	Ivanova E, Toychiev AH, Yee CW, et al. Intersublaminar vascular plexus: the correlation of retinal blood vessels with functional sublaminae of the inner plexiform layer[J]. Invest Ophthalmol Vis Sci, 2014, 55(1): 78-86. DOI: 10.1167/iovs.13-13196.
16.	Tani T, Nagaoka T, Nakabayashi S, et al. Autoregulation of retinal blood flow in response to decreased ocular perfusion pressure in cats: comparison of the effects of increased intraocular pressure and systemic hypotension[J]. Invest Ophthalmol Vis Sci, 2014, 55(1): 360-367. DOI: 10.1167/iovs.13-12591.
17.	Xu H, Deng G, Jiang C, et al. Microcirculatory responses to hyperoxia in macular and peripapillary regions[J]. Invest Ophthalmol Vis Sci, 2016, 57(10): 4464-4468. DOI: 10.1167/iovs.16-19603.
18.	Wanek J, Teng PY, Blair NP, et al. Inner retinal oxygen delivery and metabolism under normoxia and hypoxia in rat[J]. Invest Ophthalmol Vis Sci, 2013, 54(7): 5012-5019. DOI: 10.1167/iovs.13-11887.
19.	Chen R, Lian H, McAlinden C, et al. Normative data and determinants of macular, disc, and peripapillary vascular density in healthy myopic children using optical coherence tomography angiography[J/OL]. Front Med (Lausanne), 2022, 9: 890294[2022-06-21]. https://pubmed.ncbi.nlm.nih.gov/35801213/. DOI: 10.3389/fmed.2022.890294.
20.	Yu JJ, Camino A, Liu L, et al. Signal strength reduction effects in OCT angiography[J]. Ophthalmol Retina, 2019, 3(10): 835-842. DOI: 10.1016/j.oret.2019.04.029.
21.	Li T, Jiang B, Zhou X. Axial length elongation in primary school-age children: a 3-year cohort study in Shanghai[J/OL]. BMJ Open, 2019, 9(10): e029896[2019-10-31]. https://pubmed.ncbi.nlm.nih.gov/31676647/. DOI: 10.1136/bmjopen-2019-029896.
22.	Fan Q, Wang H, Jiang Z. Axial length and its relationship to refractive error in Chinese university students[J/OL]. Cont Lens Anterior Eye, 2022, 45(2): 101470[2021-05-22]. https://pubmed.ncbi.nlm.nih.gov/34030907/. DOI: 10.1016/j.clae.2021.101470.
23.	Zhao E, Wang X, Zhang H, et al. Ocular biometrics and uncorrected visual acuity for detecting myopia in Chinese school students[J/OL]. Sci Rep, 2022, 12(1): 18644[2022-11-04]. https://pubmed.ncbi.nlm.nih.gov/36333404/. DOI: 10.1038/s41598-022-23409-0.
24.	Jin P, Zou H, Xu X, et al. Longitudinal changes in choroidal and retinal thichknesses in children with myopic shift[J]. Retina, 2019, 39(6): 1091-1099. DOI: 10.1097/IAE.0000000000002090.
25.	Khan MH, Lam AKC, Armitage JA, et al. Impact of axial eye size on retinal microvasculature density in the macular region[J/OL]. J Clin Med, 2020, 9(8): 2539[2020-08-06]. https://pubmed.ncbi.nlm.nih.gov/32781548/. DOI: 10.3390/jcm9082539.
26.	Mo J, Duan A, Chan S, et al. Vascular flow density in pathological myopia: an optical coherence tomography angiography study[J/OL]. BMJ Open, 2017, 7(2): e013571[2017-02-03]. https://pubmed.ncbi.nlm.nih.gov/28159853/. DOI: 10.1136/bmjopen-2016-013571.
27.	Wu PC, Chen YJ, Chen CH, et al. Assessment of macular retinal thickness and volume in normal eyes and highly myopic eyes with third-generation optical coherence tomography[J]. Eye (Lond), 2008, 22(4): 551-555. DOI: 10.1038/sj.eye.6702789.

1. Jonas JB, Wang YX, Dong L, et al. Advances in myopia research anatomical findings in highly myopic eyes[J]. Eye Vis (Lond), 2020, 7: 45. DOI: 10.1186/s40662-020-00210-6.
2. Cheng D, Chen Q, Wu Y, et al. Deep perifoveal vessel density as an indicator of capillary loss in high myopia[J]. Eye (Lond), 2019, 33(12): 1961-1968. DOI: 10.1038/s41433-019-0573-1.
3. O'Bryhim BE, Apte RS, Kung N, et al. Association of preclinical Alzheimer disease with optical coherence tomographic angiography findings[J]. JAMA Ophthalmol, 2018, 136(11): 1242-1248. DOI: 10.1001/jamaophthalmol.2018.3556.
4. Durbin MK, An L, Shemonski ND, et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy[J]. JAMA Ophthalmol, 2017, 135(4): 370-376. DOI: 10.1001/jamaophthalmol.2017.0080.
5. Jia Y, Bailey ST, Wilson DJ, et al. Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration[J]. Ophthalmology, 2014, 121(7): 1435-1444. DOI: 10.1016/j.ophtha.2014.01.034.
6. Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography[J]. JAMA Ophthalmol, 2015, 133(1): 45-50. DOI: 10.1001/jamaophthalmol.2014.3616.
7. Gołębiewska J, Biała-Gosek K, Czeszyk A, et al. Optical coherence tomography angiography of superficial retinal vessel density and foveal avascular zone in myopic children[J/OL]. PLoS One, 2019, 14(7): e0219785[2019-07-18]. https://pubmed.ncbi.nlm.nih.gov/31318910/. DOI: 10.1371/journal.pone.0219785.
8. 刘玉婷, 雷颖庆, 田敏, 等. 不同屈光度近视青少年儿童黄斑区血管密度和视网膜厚度的比较[J]. 国际眼科杂志, 2021, 21(5): 789-795. DOI: 10.3980/j.issn.1672-5123.2021.5.08.Liu YT, Lei YQ, Tian M, et al. Comparison of macular vascular density and retinal thickness in children with different degrees of myopia[J]. Int Eye Sci, 2021, 21(5): 789-795. DOI: 10.3980/j.issn.1672-5123.2021.5.08.
9. Lv L, Li M, Chang X, et al. Macular retinal microvasculature of hyperopia, emmetropia, and myopia in children[J/OL]. Front Med (Lausanne), 2022, 9: 900486[2022-05-20]. https://pubmed.ncbi.nlm.nih.gov/35669923/. DOI: 10.3389/fmed.2022.900486.
10. Laíns I, Wang JC, Cui Y, et al. Retinal applications of swept source optical coherence tomography (OCT) and optical coherence tomography angiography (OCTA)[J/OL]. Prog Retin Eye Res, 2021, 84: 100951[2021-01-28]. https://pubmed.ncbi.nlm.nih.gov/33516833/. DOI: 10.1016/j.preteyeres.2021.100951.
11. Kur J, Newman EA, Chan-Ling T. Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease[J]. Prog Retin Eye Res, 2012, 31(5): 377-406. DOI: 10.1016/j.preteyeres.2012.04.004.
12. 徐珊珊, 陈一芳, 端宁茜, 等. 基于OCTA的单眼近视患儿黄斑区视网膜毛细血管血流密度及厚度分析[J]. 国际眼科杂志, 2022, 22(6): 926-930. DOI: 10.3980 /j.issn.1672-5123.2022.6.08. DOI: 10.3980/j.issn.1672-5123.2022.6.08.Xu SS, Chen YF, Duan NQ, et al. Analysis of vascular density and thickness in macular retina of monocular myopic adolescents using OCTA[J]. Int Eye Sci, 2022, 22(6): 926-930. DOI: 10.3980/j.issn.1672-5123.2022.6.08.
13. Laties AM. Central retinal artery innervation. Absence of adrenergic innervation to the intraocular branches[J]. Arch Ophthalmol, 1967, 77(3): 405-409. DOI: 10.1001/archopht.1967.00980020407021.
14. Jandrasits K, Luksch A, Söregi G, et al. Effect of noradrenaline on retinal blood flow in healthy subjects[J]. Ophthalmology, 2002, 109(2): 291-295. DOI: 10.1016/s0161-6420(01)00880-6.
15. Ivanova E, Toychiev AH, Yee CW, et al. Intersublaminar vascular plexus: the correlation of retinal blood vessels with functional sublaminae of the inner plexiform layer[J]. Invest Ophthalmol Vis Sci, 2014, 55(1): 78-86. DOI: 10.1167/iovs.13-13196.
16. Tani T, Nagaoka T, Nakabayashi S, et al. Autoregulation of retinal blood flow in response to decreased ocular perfusion pressure in cats: comparison of the effects of increased intraocular pressure and systemic hypotension[J]. Invest Ophthalmol Vis Sci, 2014, 55(1): 360-367. DOI: 10.1167/iovs.13-12591.
17. Xu H, Deng G, Jiang C, et al. Microcirculatory responses to hyperoxia in macular and peripapillary regions[J]. Invest Ophthalmol Vis Sci, 2016, 57(10): 4464-4468. DOI: 10.1167/iovs.16-19603.
18. Wanek J, Teng PY, Blair NP, et al. Inner retinal oxygen delivery and metabolism under normoxia and hypoxia in rat[J]. Invest Ophthalmol Vis Sci, 2013, 54(7): 5012-5019. DOI: 10.1167/iovs.13-11887.
19. Chen R, Lian H, McAlinden C, et al. Normative data and determinants of macular, disc, and peripapillary vascular density in healthy myopic children using optical coherence tomography angiography[J/OL]. Front Med (Lausanne), 2022, 9: 890294[2022-06-21]. https://pubmed.ncbi.nlm.nih.gov/35801213/. DOI: 10.3389/fmed.2022.890294.
20. Yu JJ, Camino A, Liu L, et al. Signal strength reduction effects in OCT angiography[J]. Ophthalmol Retina, 2019, 3(10): 835-842. DOI: 10.1016/j.oret.2019.04.029.
21. Li T, Jiang B, Zhou X. Axial length elongation in primary school-age children: a 3-year cohort study in Shanghai[J/OL]. BMJ Open, 2019, 9(10): e029896[2019-10-31]. https://pubmed.ncbi.nlm.nih.gov/31676647/. DOI: 10.1136/bmjopen-2019-029896.
22. Fan Q, Wang H, Jiang Z. Axial length and its relationship to refractive error in Chinese university students[J/OL]. Cont Lens Anterior Eye, 2022, 45(2): 101470[2021-05-22]. https://pubmed.ncbi.nlm.nih.gov/34030907/. DOI: 10.1016/j.clae.2021.101470.
23. Zhao E, Wang X, Zhang H, et al. Ocular biometrics and uncorrected visual acuity for detecting myopia in Chinese school students[J/OL]. Sci Rep, 2022, 12(1): 18644[2022-11-04]. https://pubmed.ncbi.nlm.nih.gov/36333404/. DOI: 10.1038/s41598-022-23409-0.
24. Jin P, Zou H, Xu X, et al. Longitudinal changes in choroidal and retinal thichknesses in children with myopic shift[J]. Retina, 2019, 39(6): 1091-1099. DOI: 10.1097/IAE.0000000000002090.
25. Khan MH, Lam AKC, Armitage JA, et al. Impact of axial eye size on retinal microvasculature density in the macular region[J/OL]. J Clin Med, 2020, 9(8): 2539[2020-08-06]. https://pubmed.ncbi.nlm.nih.gov/32781548/. DOI: 10.3390/jcm9082539.
26. Mo J, Duan A, Chan S, et al. Vascular flow density in pathological myopia: an optical coherence tomography angiography study[J/OL]. BMJ Open, 2017, 7(2): e013571[2017-02-03]. https://pubmed.ncbi.nlm.nih.gov/28159853/. DOI: 10.1136/bmjopen-2016-013571.
27. Wu PC, Chen YJ, Chen CH, et al. Assessment of macular retinal thickness and volume in normal eyes and highly myopic eyes with third-generation optical coherence tomography[J]. Eye (Lond), 2008, 22(4): 551-555. DOI: 10.1038/sj.eye.6702789.

Chinese Journal of Ocular Fundus Diseases

Analysis of macular vascular density and retinal thickness of school-age children

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