Skip to main content

Advertisement

Log in

Optical coherence tomography angiography vessel density mapping at various retinal layers in healthy and normal tension glaucoma eyes

  • Glaucoma
  • Published:
Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To investigate peripapillary vessel density at various spatial locations and layers in healthy and normal tension glaucoma eyes using optical coherence tomography angiography (OCTA).

Methods

A commercial OCTA device (AngioPlex; Carl Zeiss Meditec) was used to image microvasculature in a 6 × 6-mm optic disc region. Vessel densities of superficial and deep retinal layers were calculated using an automatic thresholding algorithm. Vessel density maps were plotted by averaging individual angiogram images. The spatial characteristics of vessel densities were analyzed at clock-hour sectors and in five 0.7-mm-thick concentric circles from a diameter of 2.0 to 5.5 mm. Areas under the receiver operating characteristics curves (AUCs) assessed the glaucoma diagnostic ability.

Results

Vessel density maps of superficial and deep retinal layers were significantly reduced at the 7 and 11 o’clock positions in glaucomatous eyes. In superficial layer, vessel density significantly decreased as the distance from the optic disc margin increased, except in the innermost circle (2.0–2.7-mm). There were significant differences in AUCs of superficial vessel density between innermost circle and the other outer circles. In the deep layer, the innermost circle showed significantly higher vessel density than the outer circles. Vessel density at 7 o’clock showed the best diagnostic performance (AUCs, 0.898 and 0.789) both in the superficial and deep layers. The innermost circle showed eccentric feature compared to the outer circles in terms of spatial characteristics and diagnostic ability.

Conclusions

Understanding of the spatial characteristics of peripapillary vasculature may be helpful in clinical practice and determining the optimal measurement area of vessel density.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Flammer J, Orgul S, Costa VP, Orzalesi N, Krieglstein GK, Serra LM, Renard JP, Stefansson E (2002) The impact of ocular blood flow in glaucoma. Prog Retin Eye Res 21:359–393

    Article  PubMed  Google Scholar 

  2. Chung HS, Harris A, Kagemann L, Martin B (1999) Peripapillary retinal blood flow in normal tension glaucoma. Br J Ophthalmol 83:466–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Harris A, Sergott RC, Spaeth GL, Katz JL, Shoemaker JA, Martin BJ (1994) Color Doppler analysis of ocular vessel blood velocity in normal-tension glaucoma. Am J Ophthalmol 118:642–649

    Article  CAS  PubMed  Google Scholar 

  4. Mitchell P, Leung H, Wang JJ, Rochtchina E, Lee AJ, Wong TY, Klein R (2005) Retinal vessel diameter and open-angle glaucoma: the Blue Mountains eye study. Ophthalmology 112:245–250

    Article  PubMed  Google Scholar 

  5. Wang S, Xu L, Wang Y, Wang Y, Jonas JB (2007) Retinal vessel diameter in normal and glaucomatous eyes: the Beijing eye study. Clin Experiment Ophthalmol 35:800–807

    Article  PubMed  Google Scholar 

  6. Yu DY, Cringle SJ, Balaratnasingam C, Morgan WH, Yu PK, Su EN (2013) Retinal ganglion cells: energetics, compartmentation, axonal transport, cytoskeletons and vulnerability. Prog Retin Eye Res 36:217–246

    Article  CAS  PubMed  Google Scholar 

  7. Zhang HR (1994) Scanning electron-microscopic study of corrosion casts on retinal and choroidal angioarchitecture in man and animals. Prog Retin Eye Res 13:243–270

    Article  Google Scholar 

  8. Alterman M, Henkind P (1968) Radial peripapillary capillaries of the retina. II. Possible role in Bjerrum scotoma. Br J Ophthalmol 52:26–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kornzweig AL, Eliasoph I, Feldstein M (1968) Selective atrophy of the radial peripapillary capillaries in chronic glaucoma. Arch Ophthalmol 80:696–702

    Article  CAS  PubMed  Google Scholar 

  10. Spaide RF, Klancnik JM Jr, Cooney MJ (2015) Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 133:45–50

    Article  PubMed  Google Scholar 

  11. Mendis KR, Balaratnasingam C, Yu P, Barry CJ, McAllister IL, Cringle SJ, Yu DY (2010) Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying retinal capillary detail. Invest Ophthalmol Vis Sci 51:5864–5869

    Article  PubMed  Google Scholar 

  12. Akagi T, Iida Y, Nakanishi H, Terada N, Morooka S, Yamada H, Hasegawa T, Yokota S, Yoshikawa M, Yoshimura N (2016) Microvascular density in glaucomatous eyes with Hemifield visual field defects: an optical coherence tomography angiography study. Am J Ophthalmol 168:237–249

    Article  PubMed  Google Scholar 

  13. Liu L, Jia Y, Takusagawa HL, Pechauer AD, Edmunds B, Lombardi L, Davis E, Morrison JC, Huang D (2015) Optical coherence tomography angiography of the Peripapillary retina in glaucoma. JAMA Ophthalmol 133:1045–1052

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bojikian KD, Chen CL, Wen JC, Zhang Q, Xin C, Gupta D, Mudumbai RC, Johnstone MA, Wang RK, Chen PP (2016) Optic disc perfusion in primary open angle and normal tension glaucoma eyes using optical coherence tomography-based Microangiography. PLoS One 11:e0154691

    Article  PubMed  PubMed Central  Google Scholar 

  15. Yarmohammadi A, Zangwill LM, Diniz-Filho A, Suh MH, Manalastas PI, Fatehee N, Yousefi S, Belghith A, Saunders LJ, Medeiros FA, Huang D, Weinreb RN (2016) Optical coherence tomography angiography vessel density in healthy, glaucoma suspect, and glaucoma eyes. Invest Ophthalmol Vis Sci 57:451–459

    Article  Google Scholar 

  16. Hollo G (2016) Vessel density calculated from OCT angiography in 3 peripapillary sectors in normal, ocular hypertensive, and glaucoma eyes. Eur J Ophthalmol 26:e42–e45

    PubMed  Google Scholar 

  17. Yu PK, Cringle SJ, Yu DY (2014) Correlation between the radial peripapillary capillaries and the retinal nerve fibre layer in the normal human retina. Exp Eye Res 129:83–92

    Article  CAS  PubMed  Google Scholar 

  18. An L, Johnstone M, Wang RK (2012) Optical microangiography provides correlation between microstructure and microvasculature of optic nerve head in human subjects. J Biomed Opt 17:116018

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhang A, Zhang Q, Chen CL, Wang RK (2015) Methods and algorithms for optical coherence tomography-based angiography: a review and comparison. J Biomed Opt 20:100901

    Article  PubMed  PubMed Central  Google Scholar 

  20. Shahlaee A, Samara WA, Hsu J, Say EA, Khan MA, Sridhar J, Hong BK, Shields CL, Ho AC (2016) In vivo assessment of macular vascular density in healthy human eyes using optical coherence tomography angiography. Am J Ophthalmol 165:39–46

    Article  PubMed  Google Scholar 

  21. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845

    Article  CAS  PubMed  Google Scholar 

  22. Wang Q, Chan S, Yang JY, You B, Wang YX, Jonas JB, Wei WB (2016) Vascular density in retina and choriocapillaris as measured by optical coherence tomography angiography. Am J Ophthalmol

  23. Jia Y, Wei E, Wang X, Zhang X, Morrison JC, Parikh M, Lombardi LH, Gattey DM, Armour RL, Edmunds B, Kraus MF, Fujimoto JG, Huang D (2014) Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology 121:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wang X, Jiang C, Ko T, Kong X, Yu X, Min W, Shi G, Sun X (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 253:1557–1564

    Article  PubMed  Google Scholar 

  25. Henkind P (1967) Radial peripapillary capillaries of the retina. I. Anatomy: human and comparative. Br J Ophthalmol 51:115–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Scoles D, Gray DC, Hunter JJ, Wolfe R, Gee BP, Geng Y, Masella BD, Libby RT, Russell S, Williams DR, Merigan WH (2009) In-vivo imaging of retinal nerve fiber layer vasculature: imaging histology comparison. BMC Ophthalmol 9:9

    Article  PubMed  PubMed Central  Google Scholar 

  27. Garcia-Valenzuela E, Mori M, Edward DP, Shahidi M (2000) Thickness of the peripapillary retina in healthy subjects with different degrees of ametropia. Ophthalmology 107:1321–1327

    Article  CAS  PubMed  Google Scholar 

  28. Budenz DL, Anderson DR, Varma R, Schuman J, Cantor L, Savell J, Greenfield DS, Patella VM, Quigley HA, Tielsch J (2007) Determinants of normal retinal nerve fiber layer thickness measured by stratus OCT. Ophthalmology 114:1046–1052

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hayreh SS (2004) Posterior ciliary artery circulation in health and disease: the Weisenfeld lecture. Invest Ophthalmol Vis Sci 45:749–757 748

    Article  PubMed  Google Scholar 

  30. Hayreh SS (1990) In vivo choroidal circulation and its watershed zones. Eye (Lond) 4(Pt 2):273–289

    Article  Google Scholar 

  31. Ross RD, Barofsky JM, Cohen G, Baber WB, Palao SW, Gitter KA (1998) Presumed macular choroidal watershed vascular filling, choroidal neovascularization, and systemic vascular disease in patients with age-related macular degeneration. Am J Ophthalmol 125:71–80

    Article  CAS  PubMed  Google Scholar 

  32. Takahashi K, Muraoka K, Kishi S, Shimizu K (1996) Watershed zone in the human peripheral choroid. Ophthalmology 103:336–342

    Article  CAS  PubMed  Google Scholar 

  33. Mammo Z, Heisler M, Balaratnasingam C, Lee S, Yu DY, Mackenzie P, Schendel S, Merkur A, Kirker A, Albiani D, Navajas E, Beg MF, Morgan W, Sarunic MV (2016) Quantitative optical coherence tomography angiography of radial Peripapillary capillaries in glaucoma, glaucoma suspect, and normal eyes. Am J Ophthalmol 170:41–49

    Article  PubMed  Google Scholar 

  34. Zhang M, Hwang TS, Campbell JP, Bailey ST, Wilson DJ, Huang D, Jia Y (2016) Projection-resolved optical coherence tomographic angiography. Biomed Opt Express 7:816–828

    Article  PubMed  PubMed Central  Google Scholar 

  35. Zhang A, Zhang Q, Wang RK (2015) Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography. Biomed Opt Express 6:4130–4143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mitchell P, Hourihan F, Sandbach J, Wang JJ (1999) The relationship between glaucoma and myopia: the Blue Mountains eye study. Ophthalmology 106:2010–2015

    Article  CAS  PubMed  Google Scholar 

  37. Perera SA, Wong TY, Tay WT, Foster PJ, Saw SM, Aung T (2010) Refractive error, axial dimensions, and primary open-angle glaucoma: the Singapore Malay eye study. Arch Ophthalmol 128:900–905

    Article  PubMed  Google Scholar 

  38. Sommer A, Tielsch JM (1996) Risk factors for open-angle glaucoma: the Barbados eye study. Arch Ophthalmol 114:235

    Article  CAS  PubMed  Google Scholar 

  39. Wong TY, Klein BE, Klein R, Knudtson M, Lee KE (2003) Refractive errors, intraocular pressure, and glaucoma in a white population. Ophthalmology 110:211–217

    Article  PubMed  Google Scholar 

  40. Xu L, Wang Y, Wang S, Wang Y, Jonas JB (2007) High myopia and glaucoma susceptibility the Beijing eye study. Ophthalmology 114:216–220

    Article  PubMed  Google Scholar 

  41. Shin JW, Shin YU, Lee BR (2012) Choroidal thickness and volume mapping by a six radial scan protocol on spectral-domain optical coherence tomography. Ophthalmology 119:1017–1023

    Article  PubMed  Google Scholar 

  42. Ho M, Liu DT, Chan VC, Lam DS (2013) Choroidal thickness measurement in myopic eyes by enhanced depth optical coherence tomography. Ophthalmology 120:1909–1914

    Article  PubMed  Google Scholar 

  43. Bussel II, Wollstein G, Schuman JS (2014) OCT for glaucoma diagnosis, screening and detection of glaucoma progression. Br J Ophthalmol 98(Suppl 2):ii15-19

    Article  Google Scholar 

  44. Mwanza JC, Oakley JD, Budenz DL, Anderson DR (2011) Ability of cirrus HD-OCT optic nerve head parameters to discriminate normal from glaucomatous eyes. Ophthalmology 118(241–248):e241

    Article  Google Scholar 

  45. Bengtsson B, Andersson S, Heijl A (2012) Performance of time-domain and spectral-domain optical coherence tomography for glaucoma screening. Acta Ophthalmol 90:310–315

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kim CS, Seong GJ, Lee NH, Song KC, Namil Study Group KGS (2011) Prevalence of primary open-angle glaucoma in central South Korea the Namil study. Ophthalmology 118:1024–1030

    Article  PubMed  Google Scholar 

  47. Suh W, Kee C, Namil Study G, Korean Glaucoma S (2012) The distribution of intraocular pressure in urban and in rural populations: the Namil study in South Korea. Am J Ophthalmol 154:99–106

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kyung Rim Sung.

Ethics declarations

Funding

No funding was received for this research.

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shin, J.W., Sung, K.R., Lee, J.Y. et al. Optical coherence tomography angiography vessel density mapping at various retinal layers in healthy and normal tension glaucoma eyes. Graefes Arch Clin Exp Ophthalmol 255, 1193–1202 (2017). https://doi.org/10.1007/s00417-017-3671-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-017-3671-4

Keywords

Navigation