Eye microcirculation in glaucoma. Part 2. Disorders of regional hemodynamics
- Authors: Petrov S.Y.1, Orlova E.N.1, Kiseleva T.N.1, Okhotsimskaya T.D.1, Markelova O.I.1
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Affiliations:
- Helmholtz National Medical Research Center of Eye Diseases
- Issue: Vol 17, No 4 (2024)
- Pages: 99-110
- Section: Reviews
- URL: https://bakhtiniada.ru/ov/article/view/280534
- DOI: https://doi.org/10.17816/OV630422
- ID: 280534
Cite item
Abstract
Glaucoma is one of the leading causes of blindness worldwide. The etiology of primary glaucoma is usually divided into mechanical and vascular mechanisms. Research of the vascular component of glaucoma was going on since the beginning of the last century with continuous improvement of diagnostic methods from invasive to high-tech non-contact ones. Modern and promising methods are: ultrasound examination in color Doppler mapping and pulsed Doppler modes, optical coherence tomography angiography, and laser speckle flowgraphy. The review describes specific for glaucoma blood flow changes in ocular vessels, correlating with functional and structural changes: decrease of vascular density in macular, parafoveolar, and peripapillary areas, decrease of the integral indicator of microcirculation, decrease of the indicators of volume and linear blood flow velocities in retinal and choroidal vessels, impaired retrobulbar blood circulation. The analysis of literature data is presented concerning the investigation of hemodynamic disturbances in ocular vessels in normotensive glaucoma and glaucoma in myopic eyes, in systemic blood flow disturbances (arterial hypertension and hypotension) in patients with glaucomatous optic neuropathy.
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##article.viewOnOriginalSite##About the authors
Sergey Yu. Petrov
Helmholtz National Medical Research Center of Eye Diseases
Email: post@glaucomajournal.ru
ORCID iD: 0000-0001-6922-0464
MD, Dr. Sci. (Medicine)
Russian Federation, 14/19 Sadovaya-Chernogryazskaya st., Moscow, 105062Elena N. Orlova
Helmholtz National Medical Research Center of Eye Diseases
Email: nauka@igb.ru
ORCID iD: 0000-0002-5373-5620
SPIN-code: 1970-4728
MD, Cand. Sci. (Medicine)
Russian Federation, 14/19 Sadovaya-Chernogryazskaya st., Moscow, 105062Tatiana N. Kiseleva
Helmholtz National Medical Research Center of Eye Diseases
Email: tkisseleva@yandex.ru
ORCID iD: 0000-0002-9185-6407
SPIN-code: 5824-5991
MD, Dr. Sci. (Medicine)
Russian Federation, 14/19 Sadovaya-Chernogryazskaya st., Moscow, 105062Tatiana D. Okhotsimskaya
Helmholtz National Medical Research Center of Eye Diseases
Email: tata123@inbox.ru
ORCID iD: 0000-0003-1121-4314
SPIN-code: 9917-7103
MD, Cand. Sci. (Medicine)
Russian Federation, 14/19 Sadovaya-Chernogryazskaya st., Moscow, 105062Oksana I. Markelova
Helmholtz National Medical Research Center of Eye Diseases
Author for correspondence.
Email: levinaoi@mail.ru
ORCID iD: 0000-0002-8090-6034
SPIN-code: 6381-9851
MD
Russian Federation, 14/19 Sadovaya-Chernogryazskaya st., Moscow, 105062References
- Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90(3):262–267. doi: 10.1136/bjo.2005.081224
- Neroev VV, Kiseleva OA, Bessmertny AM. The main results of a multicenter study of epidemiological features of primary open-angle glaucoma in the Russian Federation. Russian Ophthalmological Journal. 2013;6(3):43–46. EDN: QIWMDX
- Sotimehin AE, Ramulu PY. Measuring disability in glaucoma. J Glaucoma. 2018;27(11):939–949. doi: 10.1097/IJG.000000000001068
- Flammer J, Orgul S, Costa VP, et al. The impact of ocular blood flow in glaucoma. Prog Retin Eye Res. 2002;21(4):359–393. doi: 10.1016/s1350-9462(02)00008-3
- Chen HS, Liu CH, Wu WC, et al. Optical coherence tomography angiography of the superficial microvasculature in the macular and peripapillary areas in glaucomatous and healthy eyes. Invest Ophthalmol Vis Sci. 2017;58(9):3637–3645. doi: 10.1167/iovs.17-21846
- Cano J, Rahimi M, Xu BY, et al. Relationship between macular vessel density and total retinal blood flow in primary open-angle glaucoma. J Glaucoma. 2021;30(8):666–671. doi: 10.1097/IJG.0000000000001880
- Yarmohammadi A, Zangwill LM, Manalastas PIC, et al. Peripapillary and macular vessel density in patients with primary open-angle glaucoma and unilateral visual field loss. Ophthalmology. 2018;125(4):578–587. doi: 10.1016/j.ophtha.2017.10.029
- Xu H, Kong XM. Study of retinal microvascular perfusion alteration and structural damage at macular region in primary open-angle glaucoma patients. Zhonghua Yan Ke Za Zhi. 2017;53(2):98–103. doi: 10.3760/cma.j.issn.0412-4081.2017.02.006
- Tao A, Liang Y, Chen J, et al. Structure-function correlation of localized visual field defects and macular microvascular damage in primary open-angle glaucoma. Microvasc Res. 2020;130:104005. doi: 10.1016/j.mvr.2020.104005
- Li F, Lin F, Gao K, et al. Association of foveal avascular zone area with structural and functional progression in glaucoma patients. Br J Ophthalmol. 2022;106(9):1245–1251. doi: 10.1136/bjophthalmol-2020-318065
- Zhang Y, Zhang S, Wu C, et al. Optical coherence tomography angiography of the macula in patients with primary angle-closure glaucoma. Ophthalmic Res. 2021;64(3):440–446. doi: 10.1159/000512756
- Triolo G, Rabiolo A, Shemonski ND, et al. Optical coherence tomography angiography macular and peripapillary vessel perfusion density in healthy subjects, glaucoma suspects, and glaucoma patients. Invest Ophthalmol Vis Sci. 2017;58(13):5713–5722. doi: 10.1167/iovs.17-22865
- Son KY, Han JC, Kee C. Parapapillary deep-layer microvasculature dropout is only found near the retinal nerve fibre layer defect location in open-angle glaucoma. Acta Ophthalmol. 2022;100(1): e174–e180. doi: 10.1111/aos.14856
- Shin JW, Song MK, Kook MS. Association between progressive retinal capillary density loss and visual field progression in open-angle glaucoma patients according to disease stage. Am J Ophthalmol. 2021;226:137–147. doi: 10.1016/j.ajo.2021.01.015
- Wang X, Chen J, Kong X, et al. Quantification of retinal microvascular density using optic coherence tomography angiography in primary angle closure disease. Curr Eye Res. 2021;46(7):1018–1024. doi: 10.1080/02713683.2020.1849728
- Petrov SYu, Okhotsimskaya TD, Filippova OM, et al. The influence of post-COVID-19 syndrome on microcirculation of the optic nerve head among patients with primary open-angle glaucoma. Ophthalmology Reports. 2024;17(1):29–37. (In Russ.) EDN: LPROFU doi: 10.17816/OV625738
- Jo YH, Sung KR, Shin JW. Comparison of peripapillary choroidal microvasculature dropout in primary open-angle, primary angle-closure, and pseudoexfoliation glaucoma. J Glaucoma. 2020;29(12):1152–1157. doi: 10.1097/IJG.0000000000001650
- Rao HL, Sreenivasaiah S, Riyazuddin M, et al. Choroidal microvascular dropout in primary angle closure glaucoma. Am J Ophthalmol. 2019;199:184–192. doi: 10.1016/j.ajo.2018.11.021
- Kim J.A., Lee E.J., Kim T.W. Evaluation of parapapillary choroidal microvasculature dropout and progressive retinal nerve fiber layer thinning in patients with glaucoma. JAMA Ophthalmol. 2019;137(7):810–816. doi: 10.1001/jamaophthalmol.2019.1212
- Lin S, Cheng H, Zhang S, et al. Parapapillary choroidal microvasculature dropout is associated with the decrease in retinal nerve fiber layer thickness: a prospective study. Invest Ophthalmol Vis Sci. 2019;60(2):838–842. doi: 10.1167/iovs.18-26115
- Kim JA, Son DH, Lee EJ, et al. Intereye comparison of the characteristics of the peripapillary choroid in patients with unilateral normal-tension glaucoma. Ophthalmol Glaucoma. 2021;4(5):512–521. doi: 10.1016/j.ogla.2021.02.003
- Lee EJ, Han JC, Kee C. Intereye comparison of ocular factors in normal tension glaucoma with asymmetric visual field loss in Korean population. PLoS One. 2017;12(10):e0186236. doi: 10.1371/journal.pone.0186236
- Jo YH, Shin JW, Song MK, et al. Baseline choroidal microvasculature dropout as a predictor of subsequent visual field progression in open-angle glaucoma. J Glaucoma. 2021;30(8):672–681. doi: 10.1097/IJG.0000000000001853
- Park HY, Shin DY, Jeon SJ, et al. Association between parapapillary choroidal vessel density measured with optical coherence tomography angiography and future visual field progression in patients with glaucoma. JAMA Ophthalmol. 2019;137(6):681–688. doi: 10.1001/jamaophthalmol.2019.0422
- Bhalla M, Heisler M, Mammo Z, et al. Investigation of the peripapillary choriocapillaris in normal tension glaucoma, primary open-angle glaucoma, and control eyes. J Glaucoma. 2021;30(8):682–689. doi: 10.1097/IJG.0000000000001861
- Hashemi H, Fotouhi A, Yekta A, et al. Global and regional estimates of prevalence of refractive errors: Systematic review and meta-analysis. J Curr Ophthalmol. 2018;30(1):3–22. doi: 10.1016/j.joco.2017.08.009
- Erichev VP, Onishchenko AL, Kuroyedov AV, et al. Ophthalmologic risk factors for the development of primary open-angle glaucoma. Russian Journal of Clinical Ophthalmology. 2019;19(2):81–86. (In Russ.) EDN: ZSFTZJ doi: 10.32364/2311-7729-2019-19-2-81-86
- Jonas JB, Ohno-Matsui K, Panda-Jonas S. Optic nerve head histopathology in high axial myopia. J Glaucoma. 2017;26(2):187–193. doi: 10.1097/IJG.0000000000000574
- Wong YZ, Lam AK. The roles of cornea and axial length in corneal hysteresis among emmetropes and high myopes: a pilot study. Curr Eye Res. 2015;40(3):282–289. doi: 10.3109/02713683.2014.922193
- Wong TY, Klein BE, Klein R, et al. Refractive errors, intraocular pressure, and glaucoma in a white population. Ophthalmology. 2003;110(1):211–217. doi: 10.1016/s0161-6420(02)01260-5
- Samra WA, Pournaras C, Riva C, et al. Choroidal hemodynamic in myopic patients with and without primary open-angle glaucoma. Acta Ophthalmol. 2013;91(4):371–375. doi: 10.1111/j.1755-3768.2012.02386.x
- Lin F, Li F, Gao K, et al. Longitudinal changes in macular optical coherence tomography angiography metrics in primary open-angle glaucoma with high myopia: a prospective study. Invest Ophthalmol Vis Sci. 2021;62(1):30. doi: 10.1167/iovs.62.1.30
- Suwan Y, Fard MA, Geyman LS, et al. Association of myopia with peripapillary perfused capillary density in patients with glaucoma: an optical coherence tomography angiography study. JAMA Ophthalmol. 2018;136(5):507–513. doi: 10.1001/jamaophthalmol.2018.0776
- Na HM, Lee EJ, Lee SH, et al. Evaluation of peripapillary choroidal microvasculature to detect glaucomatous damage in eyes with high myopia. J Glaucoma. 2020;29(1):39–45. doi: 10.1097/IJG.0000000000001408
- Shin JW, Kwon J, Lee J, et al. Choroidal microvasculature dropout is not associated with myopia, but is associated with glaucoma. J Glaucoma. 2018;27(2):189–196. doi: 10.1097/IJG.0000000000000859
- Chakraborty R, Read SA, Collins MJ. Diurnal variations in axial length, choroidal thickness, intraocular pressure, and ocular biometrics. Invest Ophthalmol Vis Sci. 2011;52(8):5121–5129. doi: 10.1167/iovs.11-7364
- Fujiwara T, Imamura Y, Margolis R, et al. Enhanced depth imaging optical coherence tomography of the choroid in highly myopic eyes. Am J Ophthalmol. 2009;148(3):445–450. doi: 10.1016/j.ajo.2009.04.029
- Ho M, Liu DT, Chan VC, et al. Choroidal thickness measurement in myopic eyes by enhanced depth optical coherence tomography. Ophthalmology. 2013;120(9):1909–1914. doi: 10.1016/j.ophtha.2013.02.005
- Li XQ, Larsen M, Munch IC. Subfoveal choroidal thickness in relation to sex and axial length in 93 Danish university students. Invest Ophthalmol Vis Sci. 2011;52(11):8438–8441. doi: 10.1167/iovs.11-8108
- Banitt M. The choroid in glaucoma. Curr Opin Ophthalmol. 2013;24(2):125–129. doi: 10.1097/ICU.0b013e32835d9245
- Hirooka K, Fujiwara A, Shiragami C, et al. Relationship between progression of visual field damage and choroidal thickness in eyes with normal-tension glaucoma. Clin Exp Ophthalmol. 2012;40(6): 576–582. doi: 10.1111/j.1442-9071.2012.02762.x
- Hirooka K, Tenkumo K, Fujiwara A, et al. Evaluation of peripapillary choroidal thickness in patients with normal-tension glaucoma. BMC Ophthalmol. 2012;12:29. doi: 10.1186/1471-2415-12-29
- Kurysheva NI, Kiseleva TN, Ardzhevnishvily TD, et al. The choroid and glaucoma: choroidal thickness measurement by means of optical coherence tomography. National Journal Glaucoma. 2013; (3–2):73–82. EDN: RRRAUX
- Usui S, Ikuno Y, Miki A, et al. Evaluation of the choroidal thickness using high-penetration optical coherence tomography with long wavelength in highly myopic normal-tension glaucoma. Am J Ophthalmol. 2012;153(1):10–16.e1. doi: 10.1016/j.ajo.2011.05.037
- Eskina EN, Zykova AV. Early glaucoma risk factors in myopia. Ophthalmology. 2014;11(2):59–63. EDN: SFOWRD46.
- Mamikonyan VR, Shmeleva-Demir OA, Makashova NV, et al. Volume indicators of ocular hemodynamics in eyes with glaucoma associated with myopia with “normalized” pressure. National Journal Glaucoma. 2015;14(2):14–21. EDN: UBEYQT
- Konoplyannik EV, Dravitsa LV. Hemodynamic parameters and peripapillary retinal thickness in patients with primary open-angle glaucoma on the background of myopic refraction and in patients with myopia. Russian Journal of Clinical Ophthalmology. 2012;13(4):121–123. (In Russ.) EDN: PUURCP
- Aizawa N, Kunikata H, Shiga Y, et al. Correlation between structure/function and optic disc microcirculation in myopic glaucoma, measured with laser speckle flowgraphy. BMC Ophthalmol. 2014;14:113. doi: 10.1186/1471-2415-14-113
- Yokoyama Y, Aizawa N, Chiba N, et al. Significant correlations between optic nerve head microcirculation and visual field defects and nerve fiber layer loss in glaucoma patients with myopic glaucomatous disk. Clin Ophthalmol. 2011;5:1721–1727. doi: 10.2147/OPTH.S23204
- Plange N, Remky A, Arend O. Colour Doppler imaging and fluorescein filling defects of the optic disc in normal tension glaucoma. Br J Ophthalmol. 2003;87(6):731–736. doi: 10.1136/bjo.87.6.731
- Volkov VV, Sukhinina LB, Ustinova EI. Glaucoma, preglaucoma, ophthalmic hypertension. Leningrad: Meditsina; 1985. 216 p. (In Russ.) EDN: ZDPXEJ
- Tielsch JM, Katz J, Sommer A, et al. Hypertension, perfusion pressure, and primary open-angle glaucoma. A population-based assessment. Arch Ophthalmol. 1995;113(2):216–221. doi: 10.1001/archopht.1995.01100020100038
- Kosior-Jarecka E, Wrobel-Dudzinska D, Lukasik U, et al. Ocular and systemic risk factors of different morphologies of scotoma in patients with normal-tension glaucoma. J Ophthalmol. 2017:1480746. doi: 10.1155/2017/1480746
- Nesterov AP, Aliab’eva Z, Lavrent’ev AV. Normal-pressure glaucoma: a hypothesis of pathogenesis. Russian Annals of Ophthalmology. 2003;119(2):3–6. (In Russ.) EDN: TUDHHD
- Tarasova LN, Grigor’eva EG, Abaimov MA, et al. Certain aspects of normal pressure glaucoma. Russian Annals of Ophthalmology. 2003;119(3):8–11. (In Russ.) EDN: TUDHUP
- Konieczka K, Erb C. Diseases potentially related to Flammer syndrome. EPMA J. 2017;8(4):327–332. doi: 10.1007/s13167-017-0116-4
- Konieczka K, Flammer J, Sternbuch J, et al. Leber‘s Hereditary Optic Neuropathy, Normal Tension Glaucoma, and Flammer Syndrome: Long Term Follow-up of a Patient. Klin Monbl Augenheilkd. 2017;234(4):584–587. doi: 10.1055/s-0042-119564
- Kwon J, Lee J, Choi J, et al. Association between nocturnal blood pressure dips and optic disc hemorrhage in patients with normal-tension glaucoma. Am J Ophthalmol. 2017;176:87–101. doi: 10.1016/j.ajo.2017.01.002
- Kim JH, Lee TY, Lee JW, et al. Comparison of the thickness of the lamina cribrosa and vascular factors in early normal-tension glaucoma with low and high intraocular pressures. Korean J Ophthalmol. 2014;28(6):473–478. doi: 10.3341/kjo.2014.28.6.473
- Koch EC, Arend KO, Bienert M, et al. Arteriovenous passage times and visual field progression in normal tension glaucoma. Scientific World Journal. 2013;2013:726912. doi: 10.1155/2013/726912
- Plange N, Kaup M, Remky A, et al. Prolonged retinal arteriovenous passage time is correlated to ocular perfusion pressure in normal tension glaucoma. Graefes Arch Clin Exp Ophthalmol. 2008;246(8):1147–1152. doi: 10.1007/s00417-008-0807-6
- Duijm HF, van den Berg TJ, Greve EL. A comparison of retinal and choroidal hemodynamics in patients with primary open-angle glaucoma and normal-pressure gaucoma. Am J Ophthalmol. 1997;123(5):644–656. doi: 10.1016/s0002-9394(14)71077-3
- Butt Z, O’Brien C, McKillop G, et al. Color Doppler imaging in untreated high- and normal-pressure open-angle glaucoma. Invest Ophthalmol Vis Sci. 1997;38(3):690–696.
- Galassi F, Sodi A, Ucci F, et al. Ocular hemodynamics and glaucoma prognosis: a color Doppler imaging study. Arch Ophthalmol. 2003;121(12):1711–1715. doi: 10.1001/archopht.121.12.1711
- Martinez A, Sanchez M. Ocular blood flow and glaucoma. Br J Ophthalmol. 2008;92(9):1301.
- Martinez A, Sanchez M. Ocular haemodynamics in pseudoexfoliative and primary open-angle glaucoma. Eye (Lond). 2008;22(4): 515–520. doi: 10.1038/sj.eye.6702676
- Yamazaki Y, Drance SM. The relationship between progression of visual field defects and retrobulbar circulation in patients with glaucoma. Am J Ophthalmol. 1997;124(3):287–295. doi: 10.1016/s0002–9394(14)70820-7
- Ong K, Farinelli A, Billson F, et al. Comparative study of brain magnetic resonance imaging findings in patients with low-tension glaucoma and control subjects. Ophthalmology. 1995;102(11): 1632–1638. doi: 10.1016/s0161-6420(95)30816-0
- Stroman GA, Stewart WC, Golnik KC, et al. Magnetic resonance imaging in patients with low-tension glaucoma. Arch Ophthalmol. 1995;113(2):168–172. doi: 10.1001/archopht.1995.01100020050027
- Yuksel N, Anik Y, Altintas O, et al. Magnetic resonance imaging of the brain in patients with pseudoexfoliation syndrome and glaucoma. Ophthalmologica. 2006;220(2):125–130. doi: 10.1159/000090578
- Suzuki J, Tomidokoro A, Araie M, et al. Visual field damage in normal-tension glaucoma patients with or without ischemic changes in cerebral magnetic resonance imaging. Jpn J Ophthalmol. 2004;48(4):340–344. doi: 10.1007/s10384-004-0072-0
- Shiga Y, Omodaka K, Kunikata H, et al. Waveform analysis of ocular blood flow and the early detection of normal tension glaucoma. Invest Ophthalmol Vis Sci. 2013;54(12):7699–706. doi: 10.1167/iovs.13-12930
- Mursch-Edlmayr AS, Luft N, Podkowinski D, et al. Laser speckle flowgraphy derived characteristics of optic nerve head perfusion in normal tension glaucoma and healthy individuals: a Pilot study. Sci Rep. 2018;8(1):5343. doi: 10.1038/s41598-018-23149-0
- Takeyama A, Ishida K, Anraku A, et al. Comparison of optical coherence tomography angiography and laser speckle flowgraphy for the diagnosis of normal-tension glaucoma. J Ophthalmol. 2018;2018:1751857. doi: 10.1155/2018/1751857
- Leeman M, Kestelyn P. Glaucoma and blood pressure. Hypertension. 2019;73(5):944–950. doi: 10.1161/HYPERTENSIONAHA.118.11507
- Yilmaz KC, Sur Gungor S, Ciftci O, et al. Relationship between primary open angle glaucoma and blood pressure. Acta Cardiol. 2020;75(1):54–58. doi: 10.1080/00015385.2018.1549004
- Yoshikawa T, Obayashi K, Miyata K, et al. Increased nighttime blood pressure in patients with glaucoma: cross-sectional analysis of the LIGHT study. Ophthalmology. 2019;126(10):1366–1371. doi: 10.1016/j.ophtha.2019.05.019
- Skrzypecki J, Ufnal M, Szaflik JP, et al. Blood pressure and glaucoma: at the crossroads between cardiology and ophthalmology. Cardiol J. 2019;26(1):8–12. doi: 10.5603/CJ.2019.0008
- Holappa M, Vapaatalo H, Vaajanen A. Many faces of renin-angiotensin system — focus on eye. Open Ophthalmol J. 2017;11:122–142. doi: 10.2174/1874364101711010122
- Grzybowski A, Och M, Kanclerz P, et al. Primary open angle glaucoma and vascular risk factors: a review of population based studies from 1990 to 2019. J Clin Med. 2020;9(3):761. doi: 10.3390/jcm9030761
- Gangwani RA, Lee JWY, Mo HY, et al. The correlation of retinal nerve fiber layer thickness with blood pressure in a chinese hypertensive population. Medicine (Baltimore). 2015;94(23):e947. doi: 10.1097/MD.0000000000000947
- Bowe A, Grunig M, Schubert J, et al. Circadian variation in arterial blood pressure and glaucomatous optic neuropathya systematic review and meta-analysis. Am J Hypertens. 2015;28(9):1077–1082. doi: 10.1093/ajh/hpv016
- Jammal AA, Berchuck SI, Mariottoni EB, et al. Blood pressure and glaucomatous progression in a large clinical population. Ophthalmology. 2022;129(2):161–170. doi: 10.1016/j.ophtha.2021.08.021
- Melgarejo JD, Lee JH, Petitto M, et al. Glaucomatous optic neuropathy associated with nocturnal dip in blood pressure: findings from the Maracaibo aging study. Ophthalmology. 2018;125(6): 807–814. doi: 10.1016/j.ophtha.2017.11.029
- Raman P, Suliman NB, Zahari M, et al. Low nocturnal diastolic ocular perfusion pressure as a risk factor for NTG progression: a 5-year prospective study. Eye (Lond). 2018;32(7):1183–1189. doi: 10.1038/s41433-018-0057-8
- Pillunat KR, Spoerl E, Jasper C, et al. Nocturnal blood pressure in primary open-angle glaucoma. Acta Ophthalmol. 2015;93(8): e621–e626. doi: 10.1111/aos.12740
- Lee K, Yang H, Kim JY, et al. Risk factors associated with structural progression in normal-tension glaucoma: intraocular pressure, systemic blood pressure, and myopia. Invest Ophthalmol Vis Sci. 2020;61(8):35. doi: 10.1167/iovs.61.8.35
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