Changes in retinal vascular geometry in young myopic subjects_Chinese Journal of Ocular Fundus Diseases

Authors：

Chen Tingli ¹ , Sun Caixia ^2,3 , Yang Xiaolong ¹ ,  Yuan Yuanzhi ^2,4,5

1. Department of Ophthalmology, Huadong Sanatorium, Wuxi 214065, China;
2. Department of Ophthalmology, Zhongshan Hospital, Fudan University, Shanghai 200032, China;
3. Department of Ophthalmology, Shanghai Geriatric Medical Center, Shanghai 201104, China;
4. Department of Ophthalmology, Zhongshan Hospital (Xiamen), Fudan University, Xiamen 361015, China;
5. Center for Evidence-based Medicine, Fudan University, Shanghai 200433, China;

Corresponding author：

Yuan Yuanzhi, Email: yuan.yuanzhi@zs-hospital.sh.cn

Keywords：

Myopia; Retinal vascular; Geometry; Young people

DOI：

10.3760/cma.j.cn511434-20230110-00016

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate the effect of myopia on retinal vascular geometry in young subjects. Methods A retrospective cross-sectional study. From June 2018 to December 2018, 235 participants (235 eyes) who took part in routine physical examination in Huadong Sanatorium were included . There were 94 males and 141 females; age was (34.89±6.15) years old; equivalent spherical refraction (SE) was (－3.78±3.25) D. 59 (25.11%, 59/235) were divided into high myopia group (SE≤－6.0 D), along with 131 (55.74%, 131/235) low to moderate myopia group (－0.5 D＞SE＞－6.0 D), and 45 (19.15%, 45/235) emmetropia group (0.5 D≥SE≥－0.5 D). Retinal vascular geometric measurements, including central retinal arteriolar equivalent (CRAE), central retinal venular equivalent (CRVE), fractal dimension arteriole (FDa), fractal dimension venule (FDv), curvature tortuosity arteriole (CTORTa), curvature tortuosity venule, branch angle arteriole (BAa), branch angle venule, branch coefficient arteriole and branching coefficient venule, were extracted by using a validated computer program. One-way analysis of variance and analysis of covariance were performed to compare the measurements across the high myopia, low to moderate myopia, and emmetropia groups. Linear regression analysis was used to explore the relationship between SE and retinal vascular geometric parameters. Results The differences in CRAE (F=65.11), CRVE (F=61.52), FDa (F=14.26), FDv (F=8.31), CTORTa (F=5.07) and BAa (F=6.51) among eys of high myopia group, low to moderate myopia group and emmetropia group remained significant (P＜0.05) after adjusting for age, glycosylated hemoglobin, mean arterial pressure, body mass index, and intraocular pressure. CRAE and CRVE were linearly correlated with the SE (P＜0.05). FDa, FDv, cTORTa and BAa decreased with the decrease of SE in high myopia (P＜0.05). Conclusions Myopia is associated with the change of the retinal vascular geometric characteristics. With the deepening of myopia, the change of retinal vascular geometric characteristics gradually worsens.

Citation： Chen Tingli, Sun Caixia, Yang Xiaolong, Yuan Yuanzhi. Changes in retinal vascular geometry in young myopic subjects. Chinese Journal of Ocular Fundus Diseases, 2023, 39(8): 641-648. doi: 10.3760/cma.j.cn511434-20230110-00016 Copy

1.	Ohsugi H, Ikuno Y, Oshima K, et al. 3-D choroidal thickness maps from EDI-OCT in highly myopic eyes[J]. Optom Vis Sci, 2013, 90(6): 599-606. DOI: 10.1097/OPX.0b013e3182924017.
2.	韩泉洪, 刘玉燕, 楚艳华, 等. 高度近视患者后极部视网膜血管曲折度及分叉角变异[J]. 中华眼底病杂志, 2009, 25(5): 360-363. DOI: 10.3760/cma.j.issn.1005-1015.2009.05.10.Han QH, Liu YY, Chu YH, et al. The changes of tortuosity and bifurcation angle of retinal vessels at the posterior pole in the eyes with high myopia[J]. Chin J Ocul Fundus Dis, 2009, 25(5): 360-363. DOI: 10.3760/cma.j.issn.1005-1015.2009.05.10.
3.	Lim LS, Cheung CY, Lin X, et al. Influence of refractive error and axial length on retinal vessel geometric characteristics[J]. Invest Ophthalmol Vis Sci, 2011, 52(2): 669-678. DOI: 10.1167/iovs.10-6184.
4.	Knudtson MD, Lee KE, Hubbard LD, et al. Revised formulas for summarizing retinal vessel diameters[J]. Curr Eye Res, 2003, 27(3): 143-149. DOI: 10.1076/ceyr.27.3.143.16049.
5.	Masters BR. Fractal analysis of the vascular tree in the human retina[J]. Annu Rev Biomed Eng, 2004, 6: 427-452. DOI: 10.1146/annurev.bioeng.6.040803.140100.
6.	Murray CD. The physiological principle of minimum work: I. The Vascular System and the Cost of Blood Volume[J]. Proc Natl Acad Sci USA, 1926, 12(3): 207-214. DOI: 10.1073/pnas.12.3.207.
7.	Li H, Mitchell P, Liew G, et al. Lens opacity and refractive influences on the measurement of retinal vascular fractal dimension[J/OL]. Acta Ophthalmol, 2010, 88(6): e234-e240[2010-09-01]. https://pubmed.ncbi.nlm.nih.gov/20662797/. DOI: 10.1111/j.1755-3768.2010. 01975.x.
8.	Patton N, Maini R, Macgillivary T, et al. Effect of axial length on retinal vascular network geometry[J]. Am J Ophthalmol, 2005, 140(4): 648-653. DOI: 10.1016/j.ajo.2005.04.040.
9.	Li X, Wong WL, Cheung CY, et al. Racial differences in retinal vessel geometric characteristics: a multiethnic study in healthy Asians[J]. Invest Ophthalmol Vis Sci, 2013, 54(5): 3650-3656. DOI: 10.1167/iovs.12-11126.
10.	Parekh T, Pemmasani S, Desai R. Marijuana use among young adults (18-44 years of age) and risk of stroke: a behavioral risk factor surveillance system survey analysis[J]. Stroke, 2020, 51(1): 308-310. DOI: 10.1161/STROKEAHA.119.027828.
11.	Mancia G, Fagard R, Narkiewicz K, et al. 2013 ESH/ESC guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC)[J]. J Hypertens, 2013, 31(7): 1281-1357. DOI: 10.1097/01.hjh.0000431740.32696.cc.
12.	Fonville S, Zandbergen AA, Vermeer SE, et al. Prevalence of prediabetes and newly diagnosed diabetes in patients with a transient ischemic attack or stroke[J]. Cerebrovasc Dis, 2013, 36(4): 283-289. DOI: 10.1159/000353677.
13.	Keller-Ross ML, Johnson BD, Joyner MJ, et al. Influence of the metaboreflex on arterial blood pressure in heart failure patients[J]. Am Heart J, 2014, 167(4): 521-528. DOI: 10.1016/j.ahj.2013.12.021.
14.	Haarman AEG, Enthoven CA, Tideman JWL, et al. The complications of myopia: a review and meta-Analysis[J/OL]. Invest Ophthalmol Vis Sci, 2020, 61(4): 49[2020-04-09]. https://pubmed.ncbi.nlm.nih.gov/32347918/. DOI: 10.1167/iovs.61.4.49.
15.	Huang QF, Wei FF, Zhang ZY, et al. Reproducibility of retinal microvascular traits decoded by the Singapore I vessel assessment software across the human age range[J]. Am J Hypertens, 2018, 31(4): 438-449. DOI: 10.1093/ajh/hpx202.
16.	Fruttiger M. Development of the retinal vasculature[J]. Angiogenesis, 2007, 10(2): 77-88. DOI: 10.1007/s10456-007-9065-1.
17.	Cheung CY, Sabanayagam C, Law AK, et al. Retinal vascular geometry and 6 year incidence and progression of diabetic rretinopathy[J]. Diabetologia, 2017, 60(9): 1770-1781. DOI: 10.1007/s00125-017-4333-0.
18.	Al-Sheikh M, Phasukkijwatana N, Dolz-Marco R, et al. Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2063-2069. DOI: 10.1167/iovs.16-21289.
19.	Wong TY, Knudtson MD, Klein R, et al. Computer-assisted measurement of retinal vessel diameters in the Beaver Dam Eye Study: methodology, correlation between eyes, and effect of eefractive errors[J]. Ophthalmology, 2004, 111(6): 1183-1190. DOI: 10.1016/j.ophtha.2003.09.039.
20.	Wu R, Cheung CY, Saw SM, et al. Retinal vascular geometry and glaucoma: the Singapore Malay Eye Study[J]. Ophthalmology, 2013, 120(1): 77-83. DOI: 10.1016/j.ophtha.2012.07.063.
21.	Cheung CY, Tay WT, Mitchell P, et al. Quantitative and qualitative retinal microvascular characteristics and blood pressure[J]. J Hypertens, 2011, 29(7): 1380-1391. DOI: 10.1097/HJH.0b013e328347266c.
22.	Cheung CY, Ikram MK, Klein R, et al. The clinical implications of recent studies on the structure and function of the retinal microvasculature in diabetes[J]. Diabetologia, 2015, 58(5): 871-885. DOI: 10.1007/s00125-015-3511-1.
23.	Doubal FN, de Haan R, Macgillivray TJ, et al. Retinal arteriolar geometry is associated with cerebral white matter hyperintensities on magnetic resonance imaging[J]. Int J Stroke, 2010, 5(6): 434-439. DOI: 10.1111/j.1747-4949.2010.00483.x.
24.	Mcgrory S, Taylor AM, Kirin M, et al. Retinal microvascular network geometry and cognitive abilities in community-dwelling older people: The Lothian Birth Cohort 1936 Study[J]. Br J Ophthalmol, 2017, 101(7): 993-998. DOI: 10.1136/bjophthalmol-2016-309017.
25.	Klein R, Lee KE, Danforth L, et al. The relationship of retinal vessel geometric characteristics to the incidence and progression of diabetic retinopathy[J]. Ophthalmology, 2018, 125(11): 1784-1792. DOI: 10.1016/j.ophtha.2018.04.023.
26.	Benavente-Pérez A, Hosking SL, Logan NS, et al. Ocular blood flow measurements in healthy human myopic eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2010, 248(11): 1587-1594. DOI: 10.1007/s00417-010-1407-9.
27.	Liew G, Wang JJ, Cheung N, et al. The retinal vasculature as a fractal: methodology, reliability, and relationship to blood pressure[J]. Ophthalmology, 2008, 115(11): 1951-1956. DOI: 10.1016/j.ophtha.2008.05.029.
28.	Daxer A. The fractal geometry of proliferative diabetic retinopathy: implications for the diagnosis and the process of retinal vasculogenesis[J]. Curr Eye Res, 1993, 12(12): 1103-1109. DOI: 10.3109/02713689309033508.
29.	陈晓冲. 高度近视患者视网膜血管几何学特性分析[D]. 天津: 天津医科大学, 2013.Chen XC. The analysis of retinal vascular geometric characteristic in high myopia[D]. Tianjin: Tianjin Medical University, 2013.
30.	Murray CD. The physiological principle of minimum work applied to the angle of branching of arteries[J]. J Gen Physiol, 1926, 9(6): 835-841. DOI: 10.1085/jgp.9.6.835.
31.	Zamir M. Nonsymmetrical bifurcations in arterial branching[J]. J Gen Physiol, 1978, 72(6): 837-845. DOI: 10.1085/jgp.72.6.837.
32.	Tham YC, Cheng CY, Zheng Y, et al. Relationship between retinal vascular geometry with retinal nerve fiber layer and ganglion cell-inner plexiform layer in nonglaucomatous eyes[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7309-7316. DOI: 10.1167/iovs.13-12796.
33.	Ha A, Kim CY, Shim SR, et al. Degree of myopia and glaucoma risk: a dose-response meta-analysis[J]. Am J Ophthalmol, 2022, 236: 107-119. DOI: 10.1016/j.ajo.2021.10.007.
34.	Delaey C, Van De Voorde J. Regulatory mechanisms in the retinal and choroidal circulation[J]. Ophthalmic Res, 2000, 32(6): 249-256. DOI: 10.1159/000055622.
35.	He M, Chen H, Wang W. Refractive errors, ocular biometry and diabetic retinopathy: a comprehensive review[J]. Curr Eye Res, 2021, 46(2): 151-158. DOI: 10.1080/02713683.2020.1789175.
36.	Sasongko MB, Wang JJ, Donaghue KC, et al. Alterations in retinal microvascular geometry in young type 1 diabetes[J]. Diabetes Care, 2010, 33(6): 1331-1336. DOI: 10.2337/dc10-0055.
37.	Deng L, Gwiazda J, Manny RE, et al. Limited change in anisometropia and aniso-axial length over 13 years in myopic children enrolled in the correction of myopia evaluation trial[J]. Invest Ophthalmol Vis Sci, 2014, 55(4): 2097-2105. DOI: 10.1167/iovs.13-13675.

1. Ohsugi H, Ikuno Y, Oshima K, et al. 3-D choroidal thickness maps from EDI-OCT in highly myopic eyes[J]. Optom Vis Sci, 2013, 90(6): 599-606. DOI: 10.1097/OPX.0b013e3182924017.
2. 韩泉洪, 刘玉燕, 楚艳华, 等. 高度近视患者后极部视网膜血管曲折度及分叉角变异[J]. 中华眼底病杂志, 2009, 25(5): 360-363. DOI: 10.3760/cma.j.issn.1005-1015.2009.05.10.Han QH, Liu YY, Chu YH, et al. The changes of tortuosity and bifurcation angle of retinal vessels at the posterior pole in the eyes with high myopia[J]. Chin J Ocul Fundus Dis, 2009, 25(5): 360-363. DOI: 10.3760/cma.j.issn.1005-1015.2009.05.10.
3. Lim LS, Cheung CY, Lin X, et al. Influence of refractive error and axial length on retinal vessel geometric characteristics[J]. Invest Ophthalmol Vis Sci, 2011, 52(2): 669-678. DOI: 10.1167/iovs.10-6184.
4. Knudtson MD, Lee KE, Hubbard LD, et al. Revised formulas for summarizing retinal vessel diameters[J]. Curr Eye Res, 2003, 27(3): 143-149. DOI: 10.1076/ceyr.27.3.143.16049.
5. Masters BR. Fractal analysis of the vascular tree in the human retina[J]. Annu Rev Biomed Eng, 2004, 6: 427-452. DOI: 10.1146/annurev.bioeng.6.040803.140100.
6. Murray CD. The physiological principle of minimum work: I. The Vascular System and the Cost of Blood Volume[J]. Proc Natl Acad Sci USA, 1926, 12(3): 207-214. DOI: 10.1073/pnas.12.3.207.
7. Li H, Mitchell P, Liew G, et al. Lens opacity and refractive influences on the measurement of retinal vascular fractal dimension[J/OL]. Acta Ophthalmol, 2010, 88(6): e234-e240[2010-09-01]. https://pubmed.ncbi.nlm.nih.gov/20662797/. DOI: 10.1111/j.1755-3768.2010. 01975.x.
8. Patton N, Maini R, Macgillivary T, et al. Effect of axial length on retinal vascular network geometry[J]. Am J Ophthalmol, 2005, 140(4): 648-653. DOI: 10.1016/j.ajo.2005.04.040.
9. Li X, Wong WL, Cheung CY, et al. Racial differences in retinal vessel geometric characteristics: a multiethnic study in healthy Asians[J]. Invest Ophthalmol Vis Sci, 2013, 54(5): 3650-3656. DOI: 10.1167/iovs.12-11126.
10. Parekh T, Pemmasani S, Desai R. Marijuana use among young adults (18-44 years of age) and risk of stroke: a behavioral risk factor surveillance system survey analysis[J]. Stroke, 2020, 51(1): 308-310. DOI: 10.1161/STROKEAHA.119.027828.
11. Mancia G, Fagard R, Narkiewicz K, et al. 2013 ESH/ESC guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC)[J]. J Hypertens, 2013, 31(7): 1281-1357. DOI: 10.1097/01.hjh.0000431740.32696.cc.
12. Fonville S, Zandbergen AA, Vermeer SE, et al. Prevalence of prediabetes and newly diagnosed diabetes in patients with a transient ischemic attack or stroke[J]. Cerebrovasc Dis, 2013, 36(4): 283-289. DOI: 10.1159/000353677.
13. Keller-Ross ML, Johnson BD, Joyner MJ, et al. Influence of the metaboreflex on arterial blood pressure in heart failure patients[J]. Am Heart J, 2014, 167(4): 521-528. DOI: 10.1016/j.ahj.2013.12.021.
14. Haarman AEG, Enthoven CA, Tideman JWL, et al. The complications of myopia: a review and meta-Analysis[J/OL]. Invest Ophthalmol Vis Sci, 2020, 61(4): 49[2020-04-09]. https://pubmed.ncbi.nlm.nih.gov/32347918/. DOI: 10.1167/iovs.61.4.49.
15. Huang QF, Wei FF, Zhang ZY, et al. Reproducibility of retinal microvascular traits decoded by the Singapore I vessel assessment software across the human age range[J]. Am J Hypertens, 2018, 31(4): 438-449. DOI: 10.1093/ajh/hpx202.
16. Fruttiger M. Development of the retinal vasculature[J]. Angiogenesis, 2007, 10(2): 77-88. DOI: 10.1007/s10456-007-9065-1.
17. Cheung CY, Sabanayagam C, Law AK, et al. Retinal vascular geometry and 6 year incidence and progression of diabetic rretinopathy[J]. Diabetologia, 2017, 60(9): 1770-1781. DOI: 10.1007/s00125-017-4333-0.
18. Al-Sheikh M, Phasukkijwatana N, Dolz-Marco R, et al. Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2063-2069. DOI: 10.1167/iovs.16-21289.
19. Wong TY, Knudtson MD, Klein R, et al. Computer-assisted measurement of retinal vessel diameters in the Beaver Dam Eye Study: methodology, correlation between eyes, and effect of eefractive errors[J]. Ophthalmology, 2004, 111(6): 1183-1190. DOI: 10.1016/j.ophtha.2003.09.039.
20. Wu R, Cheung CY, Saw SM, et al. Retinal vascular geometry and glaucoma: the Singapore Malay Eye Study[J]. Ophthalmology, 2013, 120(1): 77-83. DOI: 10.1016/j.ophtha.2012.07.063.
21. Cheung CY, Tay WT, Mitchell P, et al. Quantitative and qualitative retinal microvascular characteristics and blood pressure[J]. J Hypertens, 2011, 29(7): 1380-1391. DOI: 10.1097/HJH.0b013e328347266c.
22. Cheung CY, Ikram MK, Klein R, et al. The clinical implications of recent studies on the structure and function of the retinal microvasculature in diabetes[J]. Diabetologia, 2015, 58(5): 871-885. DOI: 10.1007/s00125-015-3511-1.
23. Doubal FN, de Haan R, Macgillivray TJ, et al. Retinal arteriolar geometry is associated with cerebral white matter hyperintensities on magnetic resonance imaging[J]. Int J Stroke, 2010, 5(6): 434-439. DOI: 10.1111/j.1747-4949.2010.00483.x.
24. Mcgrory S, Taylor AM, Kirin M, et al. Retinal microvascular network geometry and cognitive abilities in community-dwelling older people: The Lothian Birth Cohort 1936 Study[J]. Br J Ophthalmol, 2017, 101(7): 993-998. DOI: 10.1136/bjophthalmol-2016-309017.
25. Klein R, Lee KE, Danforth L, et al. The relationship of retinal vessel geometric characteristics to the incidence and progression of diabetic retinopathy[J]. Ophthalmology, 2018, 125(11): 1784-1792. DOI: 10.1016/j.ophtha.2018.04.023.
26. Benavente-Pérez A, Hosking SL, Logan NS, et al. Ocular blood flow measurements in healthy human myopic eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2010, 248(11): 1587-1594. DOI: 10.1007/s00417-010-1407-9.
27. Liew G, Wang JJ, Cheung N, et al. The retinal vasculature as a fractal: methodology, reliability, and relationship to blood pressure[J]. Ophthalmology, 2008, 115(11): 1951-1956. DOI: 10.1016/j.ophtha.2008.05.029.
28. Daxer A. The fractal geometry of proliferative diabetic retinopathy: implications for the diagnosis and the process of retinal vasculogenesis[J]. Curr Eye Res, 1993, 12(12): 1103-1109. DOI: 10.3109/02713689309033508.
29. 陈晓冲. 高度近视患者视网膜血管几何学特性分析[D]. 天津: 天津医科大学, 2013.Chen XC. The analysis of retinal vascular geometric characteristic in high myopia[D]. Tianjin: Tianjin Medical University, 2013.
30. Murray CD. The physiological principle of minimum work applied to the angle of branching of arteries[J]. J Gen Physiol, 1926, 9(6): 835-841. DOI: 10.1085/jgp.9.6.835.
31. Zamir M. Nonsymmetrical bifurcations in arterial branching[J]. J Gen Physiol, 1978, 72(6): 837-845. DOI: 10.1085/jgp.72.6.837.
32. Tham YC, Cheng CY, Zheng Y, et al. Relationship between retinal vascular geometry with retinal nerve fiber layer and ganglion cell-inner plexiform layer in nonglaucomatous eyes[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7309-7316. DOI: 10.1167/iovs.13-12796.
33. Ha A, Kim CY, Shim SR, et al. Degree of myopia and glaucoma risk: a dose-response meta-analysis[J]. Am J Ophthalmol, 2022, 236: 107-119. DOI: 10.1016/j.ajo.2021.10.007.
34. Delaey C, Van De Voorde J. Regulatory mechanisms in the retinal and choroidal circulation[J]. Ophthalmic Res, 2000, 32(6): 249-256. DOI: 10.1159/000055622.
35. He M, Chen H, Wang W. Refractive errors, ocular biometry and diabetic retinopathy: a comprehensive review[J]. Curr Eye Res, 2021, 46(2): 151-158. DOI: 10.1080/02713683.2020.1789175.
36. Sasongko MB, Wang JJ, Donaghue KC, et al. Alterations in retinal microvascular geometry in young type 1 diabetes[J]. Diabetes Care, 2010, 33(6): 1331-1336. DOI: 10.2337/dc10-0055.
37. Deng L, Gwiazda J, Manny RE, et al. Limited change in anisometropia and aniso-axial length over 13 years in myopic children enrolled in the correction of myopia evaluation trial[J]. Invest Ophthalmol Vis Sci, 2014, 55(4): 2097-2105. DOI: 10.1167/iovs.13-13675.

Chinese Journal of Ocular Fundus Diseases

Changes in retinal vascular geometry in young myopic subjects

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