Research progress of foveal avascular zone in retinal vascular disease_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhao Liyu ¹ , Yang Fang ¹ , Wu Changfan ² , Zhang Pengfei ² ,  Jiang Maohua ¹

1. Department of Ophthalmology, Wuhu Second People's Hospital, Wuhu 241000, China;
2. Department of Ophthalmology, The First Affiliated Hospital of Wannan Medical College, Wuhu 241000, China;

Corresponding author：

Jiang Maohua, Email: 815989834@qq.com

Keywords：

Diabetic retinopathy; Retinal vein occlusion; Tomography, optical coherence; Review; Foveal avascular zone

DOI：

10.3760/cma.j.cn511434-20200211-00050

Video：

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The fovea avascular area (FAZ) is an area of the retina surrounded by a continuous capillary plexus that does not have any capillary structure of its own. FAZ is an important region for the formation of fine vision function. The changes of its morphology and surrounding capillary density reflect the degree of macular ischemia, and are closely related to retinal vascular diseases such as diabetic retinopathy, retinal vein occlusion, Coats disease, idiopathic macular telangiectasia, and retinopathy of prematurity. Early observation of FAZ region changes in patients with retinal vascular disease by optical coherence tomography angiography (OCTA) can evaluate the severity and prognosis of the disease. However, the measurement error of FAZ-related data is still a problem that cannot be ignored. At present, OCTA devices of various manufacturers have different methods and algorithms for measuring and analyzing FAZ, which makes it impossible to compare the measured data between different devices. It is believed that with the continuous progress of OCTA related technology, more accurate data of FAZ regional changes can be obtained, which will bring more help to clinical work.

Citation： Zhao Liyu, Yang Fang, Wu Changfan, Zhang Pengfei, Jiang Maohua. Research progress of foveal avascular zone in retinal vascular disease. Chinese Journal of Ocular Fundus Diseases, 2021, 37(2): 158-162. doi: 10.3760/cma.j.cn511434-20200211-00050 Copy

1.	Mihailovic N, Eter N, Alnawaiseh M. Foveal avascular zone and OCT angiography. An overview of current knowledge[J]. Ophthalmologe, 2019, 116(7): 610-616. DOI: 10.1007/s00347-018-0838-2.
2.	Ciloglu E, Unal F, Sukgen EA, et al. Evaluation of foveal avascular zone and capillary plexuses in diabetic patients by optical coherence tomography angiography[J]. Korean J Ophthalmol, 2019, 33(4): 359-365. DOI: 10.3341/kjo.2018.0025.
3.	Jia Y, Bailey ST, Hwang TS, et al. Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye[J]. Proc Natl Acad Sci U S A, 2015, 112(18): E2395-E2402. DOI: 10.1073/pnas.1500185112.
4.	Iafe NA, Phasukkijwatana N, Chen X, et al. Retinal capillary density and foveal avascular zone area are age-dependent: quantitative analysis using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(13): 5780-5787. DOI: 10.1167/iovs.16-20045.
5.	Garrity ST, Iafe NA, Phasukkijwatana N, et al. Quantitative analysis of three distinct retinal capillary plexuses in healthy eyes using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(12): 5548-5555. DOI: 10.1167/iovs.17-22036.
6.	Magrath GN, Say EAT, Sioufi K, et al. Variability in foveal avascular zone and capillary density using optical coherence tomography angiography machines in healthy eyes[J]. Retina, 2017, 37(11): 2102-2111. DOI: 10.1097/IAE.0000000000001458.
7.	Corvi F, Pellegrini M, Erba S, et al. Reproducibility of vessel density, fractal dimension, and foveal avascular zone using 7 different optical coherence tomography angiography devices[J]. Am J Ophthalmol, 2018, 186: 25-31. DOI: 10.1016/j.ajo.2017.11.011.
8.	Rommel F, Siegfried F, Kurz M, et al. Impact of correct anatomical slab segmentation on foveal avascular zone measurements by optical coherence tomography angiography in healthy adults[J]. J Curr Ophthalmol, 2018, 30(2): 156-160. DOI: 10.1016/j.joco.2018.02.001.
9.	Shahlaee A, Pefkianaki M, Hsu J, et al. Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 161: 50-55. DOI: 10.1016/j.ajo.2015.09.026.
10.	Ghassemi F, Mirshahi R, Bazvand F, et al. The quantitative measurements of foveal avascular zone using optical coherence tomography angiography in normal volunteers[J]. J Curr Ophthalmol, 2017, 29(4): 293-299. DOI: 10.1016/j.joco.2017.06.004.
11.	Linderman R, Salmon AE, Strampe M, et al. Assessing the accuracy of foveal avascular zone measurements using optical coherence tomography angiography: segmentation and scaling[J/OL]. Transl Vis Sci Technol, 2017, 6(3): 16[2017-06-09].http://europepmc.org/article/MED/28616362. DOI: 10.1167/tvst.6.3.16..
12.	Cao D, Yang D, Huang Z, et al. Optical coherence tomography angiography discerns preclinical diabetic retinopathy in eyes of patients with type 2 diabetes without clinical diabetic retinopathy[J]. Acta Diabetol, 2018, 55(5): 469-477. DOI: 10.1007/s00592-018-1115-1.
13.	Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
14.	Tang FY, Ng DS, Lam A, et al. Author correction: determinants of quantitative optical coherence tomography angiography metrics in patients with diabetes[J/OL]. Sci Rep, 2018, 8(1): 7314[2018-05-04]. http://europepmc.org/article/MED/29728691. DOI: 10.1038/s41598-018-25619-x..
15.	Lu Y, Simonett JM, Wang J, et al. Evaluation of automatically quantified foveal avascular zone metrics for diagnosis of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2018, 59(6): 2212-2221. DOI: 10.1167/iovs.17-23498.
16.	Ghasemi Falavarjani K, Iafe NA, Hubschman JP, et al. Optical coherence tomography angiography analysis of the foveal avascular zone and macular vessel density after anti-vegf therapy in eyes with diabetic macular edema and retinal vein occlusion[J]. Invest Ophthalmol Vis Sci, 2017, 58(1): 30-34. DOI: 10.1167/iovs.16-20579.
17.	Dastiridou A, Karathanou K, Riga P, et al. OCT angiography study of the macula in patients with diabetic macular edema treated with intravitreal aflibercept[J/OL]. Ocul Immunol Inflamm, 2020, 2020: E1-6[2020-01-17]. https://www.tandfonline.com/doi/abs/10.1080/09273948.2019.1704028?journalCode=ioii20. DOI: 10.1080/09273948.2019.1704028. [published online ahead of print].
18.	Adhi M, Filho MA, Louzada RN, et al. Retinal capillary network and foveal avascular zone in eyes with vein occlusion and fellow eyes analyzed with optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): OCT486-OCT494. DOI: 10.1167/iovs.15-18907.
19.	Kang JW, Yoo R, Jo YH, et al. Correlation of microvascular structures on optical coherence tomography angiography with visual acuity in retinal vein occlusion[J]. Retina, 2017, 37(9): 1700-1709. DOI: 10.1097/IAE.0000000000001403.
20.	Samara WA, Shahlaee A, Sridhar J, et al. Quantitative optical coherence tomography angiography features and visual function in eyes with branch retinal vein occlusion[J]. Am J Ophthalmol, 2016, 166: 76-83. DOI: 10.1016/j.ajo.2016.03.033.
21.	Wakabayashi T, Sato T, Hara-Ueno C, et al. Retinal microvasculature and visual acuity in eyes with branch retinal vein occlusion: imaging analysis by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2087-2094. DOI: 10.1167/iovs.16-21208.
22.	Scarinci F, Nesper PL, Fawzi AA. Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia[J]. Am J Ophthalmol, 2016, 168: 129-138. DOI: 10.1016/j.ajo.2016.05.002.
23.	Ogasawara Y, Iwase T, Yamamoto K, et al. Relationship between abnormalities of photoreceptor microstructures and microvascular structures determined by optical coherence tomography angiography in eyes with branch retinal vein occlusion[J]. Retina, 2020, 40(2): 350-358. DOI: 10.1097/IAE.0000000000002379.
24.	Deng Y, Zhong QW, Zhang AQ, et al. Microvascular changes after conbercept therapy in central retinal vein occlusion analyzed by optical coherence tomography angiography[J]. Int J Ophthalmol, 2019, 12(5): 802-808. DOI: 10.18240/ijo.2019.05.16.
25.	Winegarner A, Wakabayashi T, Fukushima Y, et al. Changes in retinal microvasculature and visual acuity after antivascular endothelial growth factor therapy in retinal vein occlusion[J]. Invest Ophthalmol Vis Sci, 2018, 59(7): 2708-2716. DOI: 10.1167/iovs.17-23437.
26.	Schwartz R, Sivaprasad S, Macphee R, et al. Subclinical macular changes and disease laterality in pediatric coats disease determined by quantitative optical coherence tomography angiography[J]. Retina, 2019, 39(12): 2392-2398. DOI: 10.1097/IAE.0000000000002322.
27.	Gass JD, Blodi BA. Idiopathic juxtafoveolar retinal telangiectasis: update of classification and follow-up study[J]. Ophthalmology, 1993, 100(10): 1536-1546. DOI: 10.1016/S0161-6420(93)31447-8.
28.	Zhao M, Andrieu-Soler C, Kowalczuk L, et al. A new CRB1 rat mutation links Müller glial cells to retinal telangiectasia[J]. J Neurosci, 2015, 35(15): 6093-6106. DOI: 10.1523/JNEUROSCI.3412-14.2015.
29.	Guo J, Tang W, Ye X, et al. Predictive multi-imaging biomarkers relevant for visual acuity in idiopathic macular telangiectasis type 1[J/OL]. BMC Ophthalmol, 2018, 18(1): 69[2018-03-05]. https://bmcophthalmol.biomedcentral.com/articles/10.1186/s12886-018-0737-y. DOI: 10.1186/s12886-018-0737-y.
30.	Chidambara L, Gadde SG, Yadav NK, et al. Characteristics and quantification of vascular changes in macular telangiectasia type 2 on optical coherence tomography angiography[J]. Br J Ophthalmol, 2016, 100(11): 1482-1488. DOI: 10.1136/bjophthalmol-2015-307941.
31.	Hammer DX, Iftimia NV, Ferguson RD, et al. Foveal fine structure in retinopathy of prematurity: an adaptive optics fourier domain optical coherence tomography study[J]. Invest Ophthalmol Vis Sci, 2008, 49(5): 2061-2070. DOI: 10.1167/iovs.07-1228.
32.	Chen YC, Chen YT, Chen SN. Foveal microvascular anomalies on optical coherence tomography angiography and the correlation with foveal thickness and visual acuity in retinopathy of prematurity[J]. Graefe’s Arch Clin Exp Ophthalmol, 2019, 257(1): 23-30. DOI: 10.1007/s00417-018-4162-y.
33.	Falavarjani KG, Iafe NA, Velez FG, et al. Optical coherence tomography angiography of the fovea in children born preterm[J]. Retina, 2017, 37(12): 2289-2294. DOI: 10.1097/IAE.0000000000001471.
34.	Akula JD, Hansen RM, Martinez-Perez ME, et al. Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity[J]. Invest Ophthalmol Vis Sci, 2007, 48(9): 4351-4359. DOI: 10.1167/iovs.07-0204.
35.	Chen YC, Chen SN. Foveal microvasculature, refractive errors, optical biometry and their correlations in school-aged children with retinopathy of prematurity after intravitreal antivascular endothelial growth factors or laser photocoagulation[J]. Br J Ophthalmol, 2020, 104(5): 691-696. DOI: 10.1136/bjophthalmol-2019-314610.
36.	Ku JH, Ali A, Suhler EB, et al. Characteristics and visual outcome of patients with retinal vasculitis[J]. Arch Ophthalmol, 2012, 130(10): 1261-1266. DOI: 10.1001/archophthalmol.2012.1596.
37.	Tian M, Tappeiner C, Zinkernagel MS, et al. Swept-source optical coherence tomography angiography reveals vascular changes in intermediate uveitis[J]. Acta Ophthalmol, 2019, 97(5): e785-e791. DOI: 10.1111/aos.14024.

1. Mihailovic N, Eter N, Alnawaiseh M. Foveal avascular zone and OCT angiography. An overview of current knowledge[J]. Ophthalmologe, 2019, 116(7): 610-616. DOI: 10.1007/s00347-018-0838-2.
2. Ciloglu E, Unal F, Sukgen EA, et al. Evaluation of foveal avascular zone and capillary plexuses in diabetic patients by optical coherence tomography angiography[J]. Korean J Ophthalmol, 2019, 33(4): 359-365. DOI: 10.3341/kjo.2018.0025.
3. Jia Y, Bailey ST, Hwang TS, et al. Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye[J]. Proc Natl Acad Sci U S A, 2015, 112(18): E2395-E2402. DOI: 10.1073/pnas.1500185112.
4. Iafe NA, Phasukkijwatana N, Chen X, et al. Retinal capillary density and foveal avascular zone area are age-dependent: quantitative analysis using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(13): 5780-5787. DOI: 10.1167/iovs.16-20045.
5. Garrity ST, Iafe NA, Phasukkijwatana N, et al. Quantitative analysis of three distinct retinal capillary plexuses in healthy eyes using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(12): 5548-5555. DOI: 10.1167/iovs.17-22036.
6. Magrath GN, Say EAT, Sioufi K, et al. Variability in foveal avascular zone and capillary density using optical coherence tomography angiography machines in healthy eyes[J]. Retina, 2017, 37(11): 2102-2111. DOI: 10.1097/IAE.0000000000001458.
7. Corvi F, Pellegrini M, Erba S, et al. Reproducibility of vessel density, fractal dimension, and foveal avascular zone using 7 different optical coherence tomography angiography devices[J]. Am J Ophthalmol, 2018, 186: 25-31. DOI: 10.1016/j.ajo.2017.11.011.
8. Rommel F, Siegfried F, Kurz M, et al. Impact of correct anatomical slab segmentation on foveal avascular zone measurements by optical coherence tomography angiography in healthy adults[J]. J Curr Ophthalmol, 2018, 30(2): 156-160. DOI: 10.1016/j.joco.2018.02.001.
9. Shahlaee A, Pefkianaki M, Hsu J, et al. Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography[J]. Am J Ophthalmol, 2016, 161: 50-55. DOI: 10.1016/j.ajo.2015.09.026.
10. Ghassemi F, Mirshahi R, Bazvand F, et al. The quantitative measurements of foveal avascular zone using optical coherence tomography angiography in normal volunteers[J]. J Curr Ophthalmol, 2017, 29(4): 293-299. DOI: 10.1016/j.joco.2017.06.004.
11. Linderman R, Salmon AE, Strampe M, et al. Assessing the accuracy of foveal avascular zone measurements using optical coherence tomography angiography: segmentation and scaling[J/OL]. Transl Vis Sci Technol, 2017, 6(3): 16[2017-06-09].http://europepmc.org/article/MED/28616362. DOI: 10.1167/tvst.6.3.16..
12. Cao D, Yang D, Huang Z, et al. Optical coherence tomography angiography discerns preclinical diabetic retinopathy in eyes of patients with type 2 diabetes without clinical diabetic retinopathy[J]. Acta Diabetol, 2018, 55(5): 469-477. DOI: 10.1007/s00592-018-1115-1.
13. Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
14. Tang FY, Ng DS, Lam A, et al. Author correction: determinants of quantitative optical coherence tomography angiography metrics in patients with diabetes[J/OL]. Sci Rep, 2018, 8(1): 7314[2018-05-04]. http://europepmc.org/article/MED/29728691. DOI: 10.1038/s41598-018-25619-x..
15. Lu Y, Simonett JM, Wang J, et al. Evaluation of automatically quantified foveal avascular zone metrics for diagnosis of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2018, 59(6): 2212-2221. DOI: 10.1167/iovs.17-23498.
16. Ghasemi Falavarjani K, Iafe NA, Hubschman JP, et al. Optical coherence tomography angiography analysis of the foveal avascular zone and macular vessel density after anti-vegf therapy in eyes with diabetic macular edema and retinal vein occlusion[J]. Invest Ophthalmol Vis Sci, 2017, 58(1): 30-34. DOI: 10.1167/iovs.16-20579.
17. Dastiridou A, Karathanou K, Riga P, et al. OCT angiography study of the macula in patients with diabetic macular edema treated with intravitreal aflibercept[J/OL]. Ocul Immunol Inflamm, 2020, 2020: E1-6[2020-01-17]. https://www.tandfonline.com/doi/abs/10.1080/09273948.2019.1704028?journalCode=ioii20. DOI: 10.1080/09273948.2019.1704028. [published online ahead of print].
18. Adhi M, Filho MA, Louzada RN, et al. Retinal capillary network and foveal avascular zone in eyes with vein occlusion and fellow eyes analyzed with optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): OCT486-OCT494. DOI: 10.1167/iovs.15-18907.
19. Kang JW, Yoo R, Jo YH, et al. Correlation of microvascular structures on optical coherence tomography angiography with visual acuity in retinal vein occlusion[J]. Retina, 2017, 37(9): 1700-1709. DOI: 10.1097/IAE.0000000000001403.
20. Samara WA, Shahlaee A, Sridhar J, et al. Quantitative optical coherence tomography angiography features and visual function in eyes with branch retinal vein occlusion[J]. Am J Ophthalmol, 2016, 166: 76-83. DOI: 10.1016/j.ajo.2016.03.033.
21. Wakabayashi T, Sato T, Hara-Ueno C, et al. Retinal microvasculature and visual acuity in eyes with branch retinal vein occlusion: imaging analysis by optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2087-2094. DOI: 10.1167/iovs.16-21208.
22. Scarinci F, Nesper PL, Fawzi AA. Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia[J]. Am J Ophthalmol, 2016, 168: 129-138. DOI: 10.1016/j.ajo.2016.05.002.
23. Ogasawara Y, Iwase T, Yamamoto K, et al. Relationship between abnormalities of photoreceptor microstructures and microvascular structures determined by optical coherence tomography angiography in eyes with branch retinal vein occlusion[J]. Retina, 2020, 40(2): 350-358. DOI: 10.1097/IAE.0000000000002379.
24. Deng Y, Zhong QW, Zhang AQ, et al. Microvascular changes after conbercept therapy in central retinal vein occlusion analyzed by optical coherence tomography angiography[J]. Int J Ophthalmol, 2019, 12(5): 802-808. DOI: 10.18240/ijo.2019.05.16.
25. Winegarner A, Wakabayashi T, Fukushima Y, et al. Changes in retinal microvasculature and visual acuity after antivascular endothelial growth factor therapy in retinal vein occlusion[J]. Invest Ophthalmol Vis Sci, 2018, 59(7): 2708-2716. DOI: 10.1167/iovs.17-23437.
26. Schwartz R, Sivaprasad S, Macphee R, et al. Subclinical macular changes and disease laterality in pediatric coats disease determined by quantitative optical coherence tomography angiography[J]. Retina, 2019, 39(12): 2392-2398. DOI: 10.1097/IAE.0000000000002322.
27. Gass JD, Blodi BA. Idiopathic juxtafoveolar retinal telangiectasis: update of classification and follow-up study[J]. Ophthalmology, 1993, 100(10): 1536-1546. DOI: 10.1016/S0161-6420(93)31447-8.
28. Zhao M, Andrieu-Soler C, Kowalczuk L, et al. A new CRB1 rat mutation links Müller glial cells to retinal telangiectasia[J]. J Neurosci, 2015, 35(15): 6093-6106. DOI: 10.1523/JNEUROSCI.3412-14.2015.
29. Guo J, Tang W, Ye X, et al. Predictive multi-imaging biomarkers relevant for visual acuity in idiopathic macular telangiectasis type 1[J/OL]. BMC Ophthalmol, 2018, 18(1): 69[2018-03-05]. https://bmcophthalmol.biomedcentral.com/articles/10.1186/s12886-018-0737-y. DOI: 10.1186/s12886-018-0737-y.
30. Chidambara L, Gadde SG, Yadav NK, et al. Characteristics and quantification of vascular changes in macular telangiectasia type 2 on optical coherence tomography angiography[J]. Br J Ophthalmol, 2016, 100(11): 1482-1488. DOI: 10.1136/bjophthalmol-2015-307941.
31. Hammer DX, Iftimia NV, Ferguson RD, et al. Foveal fine structure in retinopathy of prematurity: an adaptive optics fourier domain optical coherence tomography study[J]. Invest Ophthalmol Vis Sci, 2008, 49(5): 2061-2070. DOI: 10.1167/iovs.07-1228.
32. Chen YC, Chen YT, Chen SN. Foveal microvascular anomalies on optical coherence tomography angiography and the correlation with foveal thickness and visual acuity in retinopathy of prematurity[J]. Graefe’s Arch Clin Exp Ophthalmol, 2019, 257(1): 23-30. DOI: 10.1007/s00417-018-4162-y.
33. Falavarjani KG, Iafe NA, Velez FG, et al. Optical coherence tomography angiography of the fovea in children born preterm[J]. Retina, 2017, 37(12): 2289-2294. DOI: 10.1097/IAE.0000000000001471.
34. Akula JD, Hansen RM, Martinez-Perez ME, et al. Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity[J]. Invest Ophthalmol Vis Sci, 2007, 48(9): 4351-4359. DOI: 10.1167/iovs.07-0204.
35. Chen YC, Chen SN. Foveal microvasculature, refractive errors, optical biometry and their correlations in school-aged children with retinopathy of prematurity after intravitreal antivascular endothelial growth factors or laser photocoagulation[J]. Br J Ophthalmol, 2020, 104(5): 691-696. DOI: 10.1136/bjophthalmol-2019-314610.
36. Ku JH, Ali A, Suhler EB, et al. Characteristics and visual outcome of patients with retinal vasculitis[J]. Arch Ophthalmol, 2012, 130(10): 1261-1266. DOI: 10.1001/archophthalmol.2012.1596.
37. Tian M, Tappeiner C, Zinkernagel MS, et al. Swept-source optical coherence tomography angiography reveals vascular changes in intermediate uveitis[J]. Acta Ophthalmol, 2019, 97(5): e785-e791. DOI: 10.1111/aos.14024.

Chinese Journal of Ocular Fundus Diseases

Research progress of foveal avascular zone in retinal vascular disease

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