Visual Acuity Is Correlated with the Area of the Foveal Avascular Zone in Diabetic Retinopathy and Retinal Vein Occlusion

Ophthalmology

Volumn 123, Issue 11, 2016, Pages 2352-2367

  Balaratnasingam, Chandrakumar ^a,b,c,d   Inoue, Maiko ^a,b   Ahn, Seungjun ^e   McCann, Jesse ^a,b,c   Dhrami Gavazi, Elona ^a,b,c   Yannuzzi, Lawrence A ^a,b   Freund, K Bailey ^a,b,c  

^a EAR AND THROAT HOSPITAL   (United States)

^b VITREOUS RETINA MACULA CONSULTANTS OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANATOMICAL CONCEPTS; ANGIOGRAPHY; ANGIOGRAPHY DEVICE; ARTICLE; BRANCH RETINAL VEIN OCCLUSION; CENTRAL RETINA VEIN OCCLUSION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIABETIC RETINOPATHY; FEMALE; FOVEAL AVASCULAR ZONE; HUMAN; LENS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; OPTICAL COHERENCE TOMOGRAPHY; OPTICAL COHERENCE TOMOGRAPHY DEVICE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RETINA FOVEA; RETINA VEIN OCCLUSION; RETINAL INNER NUCLEAR LAYER; RETINAL INNER PLEXIFORM LAYER; RETINAL THICKNESS; VISION; VISUAL ACUITY; EYE FUNDUS; FLUORESCENCE ANGIOGRAPHY; FOLLOW UP; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; RETINA BLOOD VESSEL; RETINAL VEIN OCCLUSION; RETROSPECTIVE STUDY; SEVERITY OF ILLNESS INDEX;

CROSS-SECTIONAL STUDIES; DIABETIC RETINOPATHY; FEMALE; FLUORESCEIN ANGIOGRAPHY; FOLLOW-UP STUDIES; FOVEA CENTRALIS; FUNDUS OCULI; HUMANS; MALE; MIDDLE AGED; RETINAL VEIN OCCLUSION; RETINAL VESSELS; RETROSPECTIVE STUDIES; SEVERITY OF ILLNESS INDEX; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL ACUITY;

EID: 84981731318     PISSN: 01616420     EISSN: 15494713     Source Type: Journal    
DOI: 10.1016/j.ophtha.2016.07.008     Document Type: Article

References (74)

1. 1 From the Centers for Disease Control and Prevention. Blindness caused by diabetes–Massachusetts, 1987-1994. JAMA 276 (1996), 1865–1866.
2. 2 Diabetic Retinopathy. Available at: https://nei.nih.gov/eyedata/diabetic. Accessed May 2, 2016.
3. 3 Rogers, S., McIntosh, R.L., Cheung, N., et al. The prevalence of retinal vein occlusion: pooled data from population studies from the United States, Europe, Asia, and Australia. Ophthalmology 117 (2010), 313–319 e1.
4. 4 Boyle, J.P., Honeycutt, A.A., Narayan, K.M., et al. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care 24 (2001), 1936–1940.
5. 5 Jonas, J.B., Schneider, U., Naumann, G.O., Count and density of human retinal photoreceptors. Graefes Arch Clin Exp Ophthalmol 230 (1992), 505–510.
6. 6 Yu, D.Y., Cringle, S.J., Su, E.N., Intraretinal oxygen distribution in the monkey retina and the response to systemic hyperoxia. Invest Ophthalmol Vis Sci 46 (2005), 4728–4733.
7. 7 Yu, P.K., Balaratnasingam, C., Cringle, S.J., et al. Microstructure and network organization of the microvasculature in the human macula. Invest Ophthalmol Vis Sci 51 (2010), 6735–6743.
8. 8 Yu, P.K., Balaratnasingam, C., Morgan, W.H., et al. The structural relationship between the microvasculature, neurons, and glia in the human retina. Invest Ophthalmol Vis Sci 51 (2010), 447–458.
9. 9 Mammo, Z., Balaratnasingam, C., Yu, P., et al. Quantitative noninvasive angiography of the fovea centralis using speckle variance optical coherence tomography. Invest Ophthalmol Vis Sci 56 (2015), 5074–5086.
10. 10 Kim, D.Y., Fingler, J., Zawadzki, R.J., et al. Noninvasive imaging of the foveal avascular zone with high-speed, phase-variance optical coherence tomography. Invest Ophthalmol Vis Sci 53 (2012), 85–92.
11. 11 Zheng, Y., Gandhi, J.S., Stangos, A.N., et al. Automated segmentation of foveal avascular zone in fundus fluorescein angiography. Invest Ophthalmol Vis Sci 51 (2010), 3653–3659.
12. 12 Popovic, Z., Knutsson, P., Thaung, J., et al. Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics. Invest Ophthalmol Vis Sci 52 (2011), 2649–2655.
13. 13 Chui, T.Y., VanNasdale, D.A., Elsner, A.E., Burns, S.A., The association between the foveal avascular zone and retinal thickness. Invest Ophthalmol Vis Sci 55 (2014), 6870–6877.
14. 14 Pinhas, A., Razeen, M., Dubow, M., et al. Assessment of perfused foveal microvascular density and identification of nonperfused capillaries in healthy and vasculopathic eyes. Invest Ophthalmol Vis Sci 55 (2014), 8056–8066.
15. 15 Schmoll, T., Singh, A.S., Blatter, C., et al. Imaging of the parafoveal capillary network and its integrity analysis using fractal dimension. Biomed Opt Express 2 (2011), 1159–1168.
16. 16 Kuehlewein, L., Tepelus, T.C., An, L., et al. Noninvasive visualization and analysis of the human parafoveal capillary network using swept source OCT optical microangiography. Invest Ophthalmol Vis Sci 56 (2015), 3984–3988.
17. 17 Samara, W.A., Say, E.A., Khoo, C.T., et al. Correlation of foveal avascular zone size with foveal morphology in normal eyes using optical coherence tomography angiography. Retina 35 (2015), 2188–2195.
18. 18 Dubis, A.M., Hansen, B.R., Cooper, R.F., et al. Relationship between the foveal avascular zone and foveal pit morphology. Invest Ophthalmol Vis Sci 53 (2012), 1628–1636.
19. 19 Tam, J., Martin, J.A., Roorda, A., Noninvasive visualization and analysis of parafoveal capillaries in humans. Invest Ophthalmol Vis Sci 51 (2010), 1691–1698.
20. 20 Laatikainen, L., Larinkari, J., Capillary-free area of the fovea with advancing age. Invest Ophthalmol Vis Sci 16 (1977), 1154–1157.
21. 21 Arend, O., Wolf, S., Harris, A., Reim, M., The relationship of macular microcirculation to visual acuity in diabetic patients. Arch Ophthalmol 113 (1995), 610–614.
22. 22 Remky, A., Wolf, S., Knabben, H., et al. Perifoveal capillary network in patients with acute central retinal vein occlusion. Ophthalmology 104 (1997), 33–37.
23. 23 Maheshwary, A.S., Oster, S.F., Yuson, R.M., et al. The association between percent disruption of the photoreceptor inner segment-outer segment junction and visual acuity in diabetic macular edema. Am J Ophthalmol 150 (2010), 63–67.e1.
24. 24 Schwartz, D.M., Fingler, J., Kim, D.Y., et al. Phase-variance optical coherence tomography: a technique for noninvasive angiography. Ophthalmology 121 (2014), 180–187.
25. 25 Fingler, J., Readhead, C., Schwartz, D.M., Fraser, S.E., Phase-contrast OCT imaging of transverse flows in the mouse retina and choroid. Invest Ophthalmol Vis Sci 49 (2008), 5055–5059.
26. 26 Makita, S., Jaillon, F., Yamanari, M., et al. Comprehensive in vivo micro-vascular imaging of the human eye by dual-beam-scan Doppler optical coherence angiography. Opt Express 19 (2011), 1271–1283.
27. 27 Jia, Y., Bailey, S.T., Hwang, T.S., et al. Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye. Proc Natl Acad Sci U S A 112 (2015), E2395–E2402.
28. 28 Xu, J., Han, S., Balaratnasingam, C., et al. Retinal angiography with real-time speckle variance optical coherence tomography. Br J Ophthalmol 99 (2015), 1315–1319.
29. 29 An, L., Wang, R.K., In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography. Opt Express 16 (2008), 11438–11452.
30. 30 Carpineto, P., Mastropasqua, R., Marchini, G., et al. Reproducibility and repeatability of foveal avascular zone measurements in healthy subjects by optical coherence tomography angiography. Br J Ophthalmol 100 (2016), 671–676.
31. 31 Grading diabetic retinopathy from stereoscopic color fundus photographs–an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 98:5 Suppl (1991), 786–806.
32. 32 Trichonas, G., Kaiser, P.K., Optical coherence tomography imaging of macular oedema. Br J Ophthalmol 98:Suppl 2 (2014), ii24–ii29.
33. 33 Sim, D.A., Keane, P.A., Fung, S., et al. Quantitative analysis of diabetic macular ischemia using optical coherence tomography. Invest Ophthalmol Vis Sci 55 (2014), 417–423.
34. 34 Radwan, S.H., Soliman, A.Z., Tokarev, J., et al. Association of disorganization of retinal inner layers with vision after resolution of center-involved diabetic macular edema. JAMA Ophthalmol 133 (2015), 820–825.
35. 35 Sun, J.K., Lin, M.M., Lammer, J., et al. Disorganization of the retinal inner layers as a predictor of visual acuity in eyes with center-involved diabetic macular edema. JAMA Ophthalmol 132 (2014), 1309–1316.
36. 36 Prakash, Y.S., Smithson, K.G., Sieck, G.C., Application of the Cavalieri principle in volume estimation using laser confocal microscopy. Neuroimage 1 (1994), 325–333.
37. 37 Balaratnasingam, C., Chae, B., Remmer, M.H., et al. The spatial profile of macular pigments is related to the topological characteristics of the foveal avascular zone. Invest Ophthalmol Vis Sci 56 (2015), 7859–7865.
38. 38 Cohen, J., Cohen, P., West, S.G., Aiken, L.S., Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences. 3rd ed., 2003, Lawrence Erlbaum Associates, Mahwah, New Jersey.
39. 39 Roach, E.S., Bettermann, K., Biller, J., Toole's Cerebrovascular Disorders. 6th ed., 2010, Cambridge University Press, New York, 33.
40. 40 Yu, D.Y., Cringle, S.J., Yu, P.K., Su, E.N., Intraretinal oxygen distribution and consumption during retinal artery occlusion and graded hyperoxic ventilation in the rat. Invest Ophthalmol Vis Sci 48 (2007), 2290–2296.
41. 41 Parodi, M.B., Visintin, F., Della Rupe, P., Ravalico, G., Foveal avascular zone in macular branch retinal vein occlusion. Int Ophthalmol 19 (1995), 25–28.
42. 42 Simader, C., Ritter, M., Bolz, M., et al. Morphologic parameters relevant for visual outcome during anti-angiogenic therapy of neovascular age-related macular degeneration. Ophthalmology 121 (2014), 1237–1245.
43. 43 Mariampillai, A., Standish, B.A., Moriyama, E.H., et al. Speckle variance detection of microvasculature using swept-source optical coherence tomography. Opt Lett 33 (2008), 1530–1532.
44. 44 de Carlo, T.E., Chin, A.T., Bonini Filho, M.A., et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 35 (2015), 2364–2370.
45. 45 Coscas, F., Glacet-Bernard, A., Miere, A., et al. Optical coherence tomography angiography in retinal vein occlusion: evaluation of superficial and deep capillary plexa. Am J Ophthalmol 161 (2016), 160–171 e1–2.
46. 46 Agemy, S.A., Scripsema, N.K., Shah, C.M., et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina 35 (2015), 2353–2363.
47. 47 Kashani, A.H., Lee, S.Y., Moshfeghi, A., et al. Optical coherence tomography angiography of retinal venous occlusion. Retina 35 (2015), 2323–2331.
48. 48 Salz, D.A., de Carlo, T.E., Adhi, M., et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol 134 (2016), 644–650.
49. 49 Takase, N., Nozaki, M., Kato, A., et al. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina 35 (2015), 2377–2383.
50. 50 Samara, W.A., Shahlaee, A., Sridhar, J., et al. Quantitative optical coherence tomography angiography features and visual function in eyes with branch retinal vein occlusion. Am J Ophthalmol 166 (2016), 76–83.
51. 51 Hwang, T.S., Gao, S.S., Liu, L., et al. Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol 134 (2016), 367–373.
52. 52 Shahlaee, A., Pefkianaki, M., Hsu, J., Ho, A.C., Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography. Am J Ophthalmol 165 (2016), 201–202.
53. 53 Bringmann, A., Pannicke, T., Grosche, J., et al. Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25 (2006), 397–424.
54. 54 Distler, C., Weigel, H., Hoffmann, K.P., Glia cells of the monkey retina. I. Astrocytes. J Comp Neurol 333 (1993), 134–147.
55. 55 Gariano, R.F., Sage, E.H., Kaplan, H.J., Hendrickson, A.E., Development of astrocytes and their relation to blood vessels in fetal monkey retina. Invest Ophthalmol Vis Sci 37 (1996), 2367–2375.
56. 56 Cai, J., Boulton, M., The pathogenesis of diabetic retinopathy: old concepts and new questions. Eye 16 (2002), 242–260.
57. 57 Gittings, N.S., Fozard, J.L., Age related changes in visual acuity. Exp Gerontol 21 (1986), 423–433.
58. 58 Mizutani, M., Gerhardinger, C., Lorenzi, M., Muller cell changes in human diabetic retinopathy. Diabetes 47 (1998), 445–449.
59. 59 Ly, A., Yee, P., Vessey, K.A., et al. Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest Ophthalmol Vis Sci 52 (2011), 9316–9326.
60. 60 Yu, D.Y., Yu, P.K., Cringle, S.J., et al. Functional and morphological characteristics of the retinal and choroidal vasculature. Prog Retin Eye Res 40 (2014), 53–93.
61. 61 Yu, D.Y., Cringle, S.J., Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res 20 (2001), 175–208.
62. 62 Springer, A.D., Hendrickson, A.E., Development of the primate area of high acuity, 3: temporal relationships between pit formation, retinal elongation and cone packing. Vis Neurosci 22 (2005), 171–185.
63. 63 Provis, J.M., Sandercoe, T., Hendrickson, A.E., Astrocytes and blood vessels define the foveal rim during primate retinal development. Invest Ophthalmol Vis Sci 41 (2000), 2827–2836.
64. 64 Dong, L.M., Marsh, M.J., Hawkins, B.S., Measurement and analysis of visual acuity in multicenter randomized clinical trials in the United States: findings from a survey. Ophthalmic Epidemiol 10 (2003), 149–165.
65. 65 Spaide, R.F., Fujimoto, J.G., Waheed, N.K., Image artifacts in optical coherence tomography angiography. Retina 35 (2015), 2163–2180.
66. 66 Leese, G., Longitudinal study examining the risk factors for proliferative retinopathy and maculopathy in type-I diabetes: The Royal College of Physicians of Edinburgh Diabetes Register Group. Eye 18 (2004), 814–820.
67. 67 Yau, J.W., Rogers, S.L., Kawasaki, R., et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35 (2012), 556–564.
68. 68 Moss, S.E., Klein, R., Klein, B.E., Ten-year incidence of visual loss in a diabetic population. Ophthalmology 101 (1994), 1061–1070.
69. 69 Banerjee, D., Chung, S., Wong, E.C., et al. Underdiagnosis of hypertension using electronic health records. Am J Hypertens 25 (2012), 97–102.
70. 70 Staff, M., Roberts, C., March, L., The completeness of electronic medical record data for patients with Type 2 Diabetes in primary care and its implications for computer modelling of predicted clinical outcomes. Prim Care Diabetes 10 (2016), 352–359.
71. 71 Lachin, J.M., Genuth, S., Nathan, D.M., et al. Effect of glycemic exposure on the risk of microvascular complications in the diabetes control and complications trial−revisited. Diabetes 57 (2008), 995–1001.
72. 72 Hirsch, I.B., Brownlee, M., Beyond hemoglobin A1c−need for additional markers of risk for diabetic microvascular complications. JAMA 303 (2010), 2291–2292.
73. 73 Miri, S., Shrier, E.M., Glazman, S., et al. The avascular zone and neuronal remodeling of the fovea in Parkinson disease. Ann Clin Transl Neurol 2 (2015), 196–201.
74. 74 Sim, D.A., Keane, P.A., Zarranz-Ventura, J., et al. Predictive factors for the progression of diabetic macular ischemia. Am J Ophthalmol 156 (2013), 684–692.