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

Graefe's Archive for Clinical and Experimental Ophthalmology volume 256, pages 1179–1186 (2018)Cite this article

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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Fig. 1

References

  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

    Article  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 120:1268–1279

    Article  Google Scholar 

  9. Collaborative Normal-Tension Glaucoma Study Group (1998) The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 126:498–505

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 44:1573–1580

    Article  PubMed  Google Scholar 

  12. Grunwald JE, Piltz J, Hariprasad SM, DuPont J (1998) Optic nerve and choroidal circulation in glaucoma. Invest Ophthalmol Vis Sci 39:2329–2336

    PubMed  CAS  Google Scholar 

  13. Flammer J, Orgül S (1998) Optic nerve blood-flow abnormalities in glaucoma. Prog Retin Eye Res 17:267–289

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 123:320–327

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 111:585–588

    Article  PubMed  CAS  Google Scholar 

  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 18:201–204

    CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 105:35–39

    Article  PubMed  CAS  Google Scholar 

  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 78:449–453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 19:580–587

    Article  PubMed  Google Scholar 

  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 79:732–734

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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 132:63–69

    Article  PubMed  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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 40:1934–1943

    Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  37. Jonas JB, Fernández MC, Stürmer J (1993) Pattern of glaucomatous neuroretinal rim loss. Ophthalmology 100:63–68

    Article  PubMed  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Hayreh SS (2001) The blood supply of the optic nerve head and the evaluation of it - myth and reality. Prog Retin Eye Res 20:563–593

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

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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).

Author information

Author notes

  1. Huan Xu and Ruyi Zhai contributed equally to this study and share first authorship.

Affiliations

  1. Department of Ophthalmology and Visual Science, Eye, Ear, Nose, and Throat Hospital, Shanghai Medical College, Fudan University, 83 Fenyang Rd., Shanghai, 200031, People’s Republic of China

    Huan Xu, Ruyi Zhai, Yuan Zong, Xiangmei Kong, Chunhui Jiang & Xinghuai Sun

  2. Key Laboratory of Myopia, Ministry of Health (Fudan University), Shanghai, China

    Huan Xu, Ruyi Zhai, Yuan Zong, Xiangmei Kong, Chunhui Jiang & Xinghuai Sun

  3. Shanghai Key Laboratory of Visual Impairment and Restoration (Fudan University), Shanghai, China

    Huan Xu, Ruyi Zhai, Yuan Zong, Xiangmei Kong, Chunhui Jiang & Xinghuai Sun

  4. State Key Laboratory of Medical Neurobiology, Institutes of Brain Science, Fudan University, Shanghai, China

    Xinghuai Sun

  5. The Key Laboratory on Adaptive Optics, Chinese Academy of Sciences, Chengdu, 610209, China

    Yi He & Xiqi Li

  6. The Laboratory on Adaptive Optics, Institute of Optics and Electronics, Chinese Academy of Sciences, Chengdu, 610209, China

    Yi He & Xiqi Li

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  1. Huan Xu
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Correspondence to Xiangmei Kong.

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Cite this article

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

Keywords

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