Abstract
Purpose
The aim of this study is to determine and compare the changes in the retinal vasculature in eyes with high-tension glaucoma (HTG) or normal-tension glaucoma (NTG).
Methods
The right eyes of 43 HTG subjects, 33 NTG subjects, and 51 age- and sex-matched normal subjects were included in this cross-sectional study. Signals were projected from the internal limiting membrane to retinal pigment epithelium. The retinal perfused vessel densities in the peripapillary and parafoveal regions were measured automatically with optic coherence tomography angiography and the split-spectrum amplitude-decorrelation angiography algorithm.
Results
Compared with normal eyes, glaucomatous eyes had a smaller retinal nerve fibre layer (RNFL) thickness, smaller full parafoveal retinal thickness, and lower retinal perfused vessel density (PVD) in the peripapillary and parafoveal regions (all P < 0.01). The visual field, RNFL and retinal thicknesses, and PVD in the parafoveal region in the HTG eyes were similar to those in the NTG eyes. However, the NTG eyes had a significantly lower mean PVD than the HTG eyes in the peripapillary region. When the different sectors of the peripapillary region were studied, the difference was still significant in most sectors (all P < 0.05), except the inferotemporal sector (P = 0.676).
Conclusions
The retinal perfused vessel density is significantly reduced in HTG and NTG eyes, and more prominently in the peripapillary region in NTG eyes.
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References
Shields MB (2008) Normal-tension glaucoma: is it different from primary open-angle glaucoma? Curr Opin Ophthalmol 19:85–88. https://doi.org/10.1097/ICU.0b013e3282f3919b
Kiriyama N, Ando A, Fukui C et al (2003) A comparison of optic disc topographic parameters in patients with primary open angle glaucoma, normal tension glaucoma, and ocular hypertension. Graefes Arch Clin Exp Ophthalmol Albrecht Von Graefes Arch Klin Exp Ophthalmol 241:541–545. https://doi.org/10.1007/s00417-003-0702-0
Martus P, Stroux A, Budde WM et al (2005) Predictive factors for progressive optic nerve damage in various types of chronic open-angle glaucoma. Am J Ophthalmol 139:999–1009. https://doi.org/10.1016/j.ajo.2004.12.056
Park H-YL, Jeon SH, Park CK (2012) Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma. Ophthalmology 119:10–20. https://doi.org/10.1016/j.ophtha.2011.07.033
Yang JG, Park KH (1997) A comparison of optic nerve head topography in primary open-angle glaucoma and normal-tension glaucoma in Korean. Korean J Ophthalmol KJO 11:79–83. https://doi.org/10.3341/kjo.1997.11.2.79
Caprioli J (2007) Intraocular pressure fluctuation: an independent risk factor for glaucoma? Arch Ophthalmol 125:1124–1125. https://doi.org/10.1001/archopht.125.8.1124
Caprioli J, Coleman AL (2008) Intraocular pressure fluctuation a risk factor for visual field progression at low intraocular pressures in the advanced glaucoma intervention study. Ophthalmology 115:1123–1129.e3. https://doi.org/10.1016/j.ophtha.2007.10.031
Heijl A, Leske MC, Bengtsson B et al (2002) Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol Chic Ill 1960 120:1268–1279
Collaborative Normal-Tension Glaucoma Study Group (1998) The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 126:498–505
Musch DC, Gillespie BW, Lichter PR et al (2009) Visual field progression in the Collaborative Initial Glaucoma Treatment Study the impact of treatment and other baseline factors. Ophthalmology 116:200–207. https://doi.org/10.1016/j.ophtha.2008.08.051
Gugleta K, Orgül S, Hasler PW et al (2003) Choroidal vascular reaction to hand-grip stress in subjects with vasospasm and its relevance in glaucoma. Invest Ophthalmol Vis Sci 44:1573–1580
Grunwald JE, Piltz J, Hariprasad SM, DuPont J (1998) Optic nerve and choroidal circulation in glaucoma. Invest Ophthalmol Vis Sci 39:2329–2336
Flammer J, Orgül S (1998) Optic nerve blood-flow abnormalities in glaucoma. Prog Retin Eye Res 17:267–289
Feke GT, Pasquale LR (2008) Retinal blood flow response to posture change in glaucoma patients compared with healthy subjects. Ophthalmology 115:246–252. https://doi.org/10.1016/j.ophtha.2007.04.055
Kaiser HJ, Schoetzau A, Stümpfig D, Flammer J (1997) Blood-flow velocities of the extraocular vessels in patients with high-tension and normal-tension primary open-angle glaucoma. Am J Ophthalmol 123:320–327
Su W-W, Cheng S-T, Hsu T-S, Ho W-J (2006) Abnormal flow-mediated vasodilation in normal-tension glaucoma using a noninvasive determination for peripheral endothelial dysfunction. Invest Ophthalmol Vis Sci 47:3390–3394. https://doi.org/10.1167/iovs.06-0024
Gasser P, Flammer J (1991) Blood-cell velocity in the nailfold capillaries of patients with normal-tension and high-tension glaucoma. Am J Ophthalmol 111:585–588
Mahler F, Saner H, Würbel H, Flammer J (1989) Local cooling test for clinical capillaroscopy in Raynaud’s phenomenon, unstable angina, and vasospastic visual disorders. VASA Z Für Gefässkrankh 18:201–204
Suh MH, Park KH (2011) Period prevalence and incidence of optic disc haemorrhage in normal tension glaucoma and primary open-angle glaucoma. Clin Exp Ophthalmol 39:513–519. https://doi.org/10.1111/j.1442-9071.2010.02482.x
Drance SM, Douglas GR, Wijsman K et al (1988) Response of blood flow to warm and cold in normal and low-tension glaucoma patients. Am J Ophthalmol 105:35–39
Hamard P, Hamard H, Dufaux J, Quesnot S (1994) Optic nerve head blood flow using a laser Doppler velocimeter and haemorheology in primary open angle glaucoma and normal pressure glaucoma. Br J Ophthalmol 78:449–453
Stalmans I, Harris A, Fieuws S et al (2009) Color Doppler imaging and ocular pulse amplitude in glaucomatous and healthy eyes. Eur J Ophthalmol 19:580–587
Yamazaki Y, Hayamizu F (1995) Comparison of flow velocity of ophthalmic artery between primary open angle glaucoma and normal tension glaucoma. Br J Ophthalmol 79:732–734
Jia Y, Wei E, Wang X et al (2014) Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121:1322–1332. https://doi.org/10.1016/j.ophtha.2014.01.021
Piltz-seymour JR, Grunwald JE, Hariprasad SM, Dupont J (2001) Optic nerve blood flow is diminished in eyes of primary open-angle glaucoma suspects. Am J Ophthalmol 132:63–69
Burgansky-Eliash Z, Bartov E, Barak A et al (2015) Blood-flow velocity in glaucoma patients measured with the retinal function imager. Curr Eye Res 41:1–6. https://doi.org/10.3109/02713683.2015.1080278
Tan O, Chopra V, Lu AT-H et al (2009) Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography. Ophthalmology 116:2305–2314–2. https://doi.org/10.1016/j.ophtha.2009.05.025
Flammer J, Konieczka K, Flammer AJ (2013) The primary vascular dysregulation syndrome: implications for eye diseases. EPMA J 4:14. https://doi.org/10.1186/1878-5085-4-14
Furlanetto RL, De Moraes CG, Teng CC et al (2014) Risk factors for optic disc hemorrhage in the low-pressure glaucoma treatment study. Am J Ophthalmol 157:945–952. https://doi.org/10.1016/j.ajo.2014.02.009
Mozaffarieh M, Flammer J (2013) New insights in the pathogenesis and treatment of normal tension glaucoma. Curr Opin Pharmacol 13:43–49. https://doi.org/10.1016/j.coph.2012.10.001
Lee YG, Kim TH, Kim CY, Hong YJ (1999) A comparison of optic nerve head and peripapillary retinal blood flow in normal, primary open angle glaucoma, and normal tension glaucoma. J Korean Ophthalmol Soc 40:1934–1943
Mroczkowska S, Benavente-Perez A, Negi A et al (2013) Primary open-angle glaucoma vs normal-tension glaucoma: the vascular perspective. JAMA Ophthalmol 131:36–43. https://doi.org/10.1001/2013.jamaophthalmol.1
Scripsema NK, Garcia PM, Bavier RD et al (2016) Optical coherence tomography angiography analysis of perfused peripapillary capillaries in primary open-angle glaucoma and normal-tension glaucoma. Invest Ophthalmol Vis Sci 57:OCT611–OCT620. https://doi.org/10.1167/iovs.15-18945
Li X, Wong WL, Cheung CY et al (2013) Racial differences in retinal vessel geometric characteristics: a multiethnic study in healthy Asians. Invest Ophthalmol Vis Sci 54:3650–3656. https://doi.org/10.1167/iovs.12-11126
Wong TY, Islam FMA, Klein R et al (2006) Retinal vascular caliber, cardiovascular risk factors, and inflammation: the multi-ethnic study of atherosclerosis (MESA). Invest Ophthalmol Vis Sci 47:2341–2350. https://doi.org/10.1167/iovs.05-1539
Oddone F, Centofanti M, Iester M et al (2009) Sector-based analysis with the Heidelberg retinal Tomograph 3 across disc sizes and glaucoma stages: a multicenter study. Ophthalmology 116:1106–1111–3. https://doi.org/10.1016/j.ophtha.2009.01.020
Jonas JB, Fernández MC, Stürmer J (1993) Pattern of glaucomatous neuroretinal rim loss. Ophthalmology 100:63–68
Wang X, Jiang C, Ko T et al (2015) Correlation between optic disc perfusion and glaucomatous severity in patients with open-angle glaucoma: an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmol Albrecht Von Graefes Arch Für Klin Exp Ophthalmol 253:1557–1564. https://doi.org/10.1007/s00417-015-3095-y
Kur J, Newman EA, Chan-Ling T (2012) Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease. Prog Retin Eye Res 31:377–406. https://doi.org/10.1016/j.preteyeres.2012.04.004
Hayreh SS (2001) The blood supply of the optic nerve head and the evaluation of it - myth and reality. Prog Retin Eye Res 20:563–593
Mohammad Salih PA-K (2012) Evaluation of peripapillary retinal nerve fiber layer thickness in myopic eyes by spectral-domain optical coherence tomography. J Glaucoma 21:41–44. https://doi.org/10.1097/IJG.0b013e3181fc8053
Wang X, Kong X, Jiang C et al (2016) Is the peripapillary retinal perfusion related to myopia in healthy eyes? A prospective comparative study. BMJ Open 6:e010791. https://doi.org/10.1136/bmjopen-2015-010791
Acknowledgements
The authors would like to thank Jianfeng Luo of Fudan University, Shanghai, China, for assistance with the statistical analyses in this study.
Funding
This study was supported in part by research grants from the Surface Project of National Natural Science Foundation of China (Grant No. 81770922, China), the project of Shanghai Municipal Commission of Health and Family Planning (Grant No. 201740204, China), the clinical science and technology innovation project of Shanghai Shenkang Hospital Development Center (SHDC12017X18), the National Major Scientific Equipment Program (2012YQ12008003), the Shanghai Nature Science Foundation (14ZR1405400) and the International Science and Technology Cooperation Program of China (2015DFA31340).
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
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Xu, H., Zhai, R., Zong, Y. et al. Comparison of retinal microvascular changes in eyes with high-tension glaucoma or normal-tension glaucoma: a quantitative optic coherence tomography angiographic study. Graefes Arch Clin Exp Ophthalmol 256, 1179–1186 (2018). https://doi.org/10.1007/s00417-018-3930-z
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DOI: https://doi.org/10.1007/s00417-018-3930-z