Advertisement

Comparison of retinal microvascular changes in eyes with high-tension glaucoma or normal-tension glaucoma: a quantitative optic coherence tomography angiographic study

  • Huan Xu
  • Ruyi Zhai
  • Yuan Zong
  • Xiangmei Kong
  • Chunhui Jiang
  • Xinghuai Sun
  • Yi He
  • Xiqi Li
Glaucoma

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.

Keywords

High-tension glaucoma Normal-tension glaucoma Retinal vessel density OCT angiography 

Notes

Acknowledgements

The authors would like to thank Jianfeng Luo of Fudan University, Shanghai, China, for assistance with the statistical analyses in this study.

Funding information

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

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.

Supplementary material

417_2018_3930_MOESM1_ESM.docx (60 kb)
ESM 1 (DOCX 60.2 kb)
417_2018_3930_MOESM2_ESM.docx (47 kb)
ESM 2 (DOCX 46.9 kb)
417_2018_3930_MOESM3_ESM.docx (58 kb)
ESM 3 (DOCX 57.6 kb)
417_2018_3930_MOESM4_ESM.docx (52 kb)
ESM 4 (DOCX 51.9 kb)
417_2018_3930_MOESM5_ESM.docx (48 kb)
ESM 5 (DOCX 48.3 kb)
417_2018_3930_MOESM6_ESM.docx (508 kb)
ESM 6 (DOCX 507 kb)
417_2018_3930_MOESM7_ESM.docx (567 kb)
ESM 7 (DOCX 566 kb)

References

  1. 1.
    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 CrossRefPubMedGoogle Scholar
  2. 2.
    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 CrossRefGoogle Scholar
  3. 3.
    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 CrossRefPubMedGoogle Scholar
  4. 4.
    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 CrossRefPubMedGoogle Scholar
  5. 5.
    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 CrossRefPubMedGoogle Scholar
  6. 6.
    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 CrossRefPubMedGoogle Scholar
  7. 7.
    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 CrossRefPubMedGoogle Scholar
  8. 8.
    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 120:1268–1279CrossRefGoogle Scholar
  9. 9.
    Collaborative Normal-Tension Glaucoma Study Group (1998) The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 126:498–505CrossRefGoogle Scholar
  10. 10.
    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 CrossRefPubMedGoogle Scholar
  11. 11.
    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 44:1573–1580CrossRefPubMedGoogle Scholar
  12. 12.
    Grunwald JE, Piltz J, Hariprasad SM, DuPont J (1998) Optic nerve and choroidal circulation in glaucoma. Invest Ophthalmol Vis Sci 39:2329–2336PubMedGoogle Scholar
  13. 13.
    Flammer J, Orgül S (1998) Optic nerve blood-flow abnormalities in glaucoma. Prog Retin Eye Res 17:267–289CrossRefPubMedGoogle Scholar
  14. 14.
    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 CrossRefPubMedGoogle Scholar
  15. 15.
    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 123:320–327CrossRefPubMedGoogle Scholar
  16. 16.
    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 CrossRefPubMedGoogle Scholar
  17. 17.
    Gasser P, Flammer J (1991) Blood-cell velocity in the nailfold capillaries of patients with normal-tension and high-tension glaucoma. Am J Ophthalmol 111:585–588CrossRefPubMedGoogle Scholar
  18. 18.
    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 18:201–204Google Scholar
  19. 19.
    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 CrossRefPubMedGoogle Scholar
  20. 20.
    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 105:35–39CrossRefPubMedGoogle Scholar
  21. 21.
    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 78:449–453CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Stalmans I, Harris A, Fieuws S et al (2009) Color Doppler imaging and ocular pulse amplitude in glaucomatous and healthy eyes. Eur J Ophthalmol 19:580–587CrossRefPubMedGoogle Scholar
  23. 23.
    Yamazaki Y, Hayamizu F (1995) Comparison of flow velocity of ophthalmic artery between primary open angle glaucoma and normal tension glaucoma. Br J Ophthalmol 79:732–734CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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 132:63–69CrossRefPubMedGoogle Scholar
  26. 26.
    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 CrossRefGoogle Scholar
  27. 27.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    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 CrossRefPubMedGoogle Scholar
  30. 30.
    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 CrossRefPubMedGoogle Scholar
  31. 31.
    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 40:1934–1943Google Scholar
  32. 32.
    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 CrossRefPubMedGoogle Scholar
  33. 33.
    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 CrossRefPubMedGoogle Scholar
  34. 34.
    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 CrossRefPubMedGoogle Scholar
  35. 35.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    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 CrossRefPubMedGoogle Scholar
  37. 37.
    Jonas JB, Fernández MC, Stürmer J (1993) Pattern of glaucomatous neuroretinal rim loss. Ophthalmology 100:63–68CrossRefPubMedGoogle Scholar
  38. 38.
    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 CrossRefGoogle Scholar
  39. 39.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Hayreh SS (2001) The blood supply of the optic nerve head and the evaluation of it - myth and reality. Prog Retin Eye Res 20:563–593CrossRefPubMedGoogle Scholar
  41. 41.
    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 CrossRefPubMedGoogle Scholar
  42. 42.
    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 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Huan Xu
    • 1
    • 2
    • 3
  • Ruyi Zhai
    • 1
    • 2
    • 3
  • Yuan Zong
    • 1
    • 2
    • 3
  • Xiangmei Kong
    • 1
    • 2
    • 3
  • Chunhui Jiang
    • 1
    • 2
    • 3
  • Xinghuai Sun
    • 1
    • 2
    • 3
    • 4
  • Yi He
    • 5
    • 6
  • Xiqi Li
    • 5
    • 6
  1. 1.Department of Ophthalmology and Visual Science, Eye, Ear, Nose, and Throat Hospital, Shanghai Medical CollegeFudan UniversityShanghaiPeople’s Republic of China
  2. 2.Key Laboratory of MyopiaMinistry of Health (Fudan University)ShanghaiChina
  3. 3.Shanghai Key Laboratory of Visual Impairment and Restoration (Fudan University)ShanghaiChina
  4. 4.State Key Laboratory of Medical Neurobiology, Institutes of Brain ScienceFudan UniversityShanghaiChina
  5. 5.The Key Laboratory on Adaptive OpticsChinese Academy of SciencesChengduChina
  6. 6.The Laboratory on Adaptive Optics, Institute of Optics and ElectronicsChinese Academy of SciencesChengduChina

Personalised recommendations