Classification of human retinal microaneurysms using adaptive optics scanning light ophthalmoscope fluorescein angiography

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 3, 2014, Pages 1299-1309

  Dubow, Michael ^a,b   Pinhas, Alexander ^a,b   Shah, Nishit ^a   Cooper, Robert F ^c   Gan, Alexander ^a   Gentile, Ronald C ^a,b,d   Hendrix, Vernon ^a   Sulai, Yusufu N ^e   Carroll, Joseph ^c,f   Chui, Toco Y P ^a   Walsh, Joseph B ^a   Weitz, Rishard ^a   Dubra, Alfredo ^c,f   Rosen, Richard B ^a,b  

^a NEW YORK EYE AND EAR INFIRMARY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c Medical College of Wisconsin and Marquette University   (United States)

^d WINTHROP UNIVERSITY HOSPITAL   (United States)

^e UNIVERSITY OF ROCHESTER   (United States)

^f MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

AOSLO; Fluorescein angiography; Microaneurysm

Indexed keywords

ACCOMMODATION PARALYSIS; ADULT; AGED; ARTICLE; CLINICAL ARTICLE; EYE AXIS LENGTH; FEMALE; HISTOLOGY; HUMAN; MALE; MIDDLE AGED; MYDRIASIS; OBSERVER VARIATION; PRIORITY JOURNAL; RELIABILITY; RETINA DISEASE; RETINA FLUORESCEIN ANGIOGRAPHY; RETINA MICROANEURYSM; SCANNING LASER OPHTHALMOSCOPY; TREATMENT RESPONSE;

AOSLO; FLUORESCEIN ANGIOGRAPHY; MICROANEURYSM;

ADULT; AGED; AGED, 80 AND OVER; ANEURYSM; EQUIPMENT DESIGN; FEMALE; FLUORESCEIN ANGIOGRAPHY; FUNDUS OCULI; HUMANS; MALE; MIDDLE AGED; OPHTHALMOSCOPES; RETINAL ARTERY; RETINAL DISEASES; SEVERITY OF ILLNESS INDEX;

EID: 84895766622     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13122     Document Type: Article

References (73)

1. Ashton N. Retinal micro-aneurysms in the non-diabetic subject. Br J Ophthalmol. 1951;35:189-212.
2. Ashton N. Studies of the retinal capillaries in relation to diabetic and other retinopathies. Br J Ophthalmol. 1963;47: 521-538.
3. Factor SM, Okun EM, Minase T. Capillary microaneurysms in the human diabetic heart. N Engl J Med. 1980;302:384-388.
4. Russell RW. How does blood-pressure cause stroke? Lancet. 1975;2:1283-1285.
5. Bloodworth JM Jr. A re-evaluation of diabetic glomerulosclerosis 50 years after the discovery of insulin. Hum Pathol. 1978;9:439-453.
6. Wong TY, Klein R, Sharrett AR, et al. Retinal microvascular abnormalities and cognitive impairment in middle-aged persons: the Atherosclerosis Risk in Communities Study. Stroke. 2002;33:1487-1492.
7. Wong TY, McIntosh R. Hypertensive retinopathy signs as risk indicators of cardiovascular morbidity and mortality. Br Med Bull. 2005;73-74:57-70.
8. Cooper LS, Wong TY, Klein R, et al. Retinal microvascular abnormalities and MRI-defined subclinical cerebral infarction: the Atherosclerosis Risk in Communities Study. Stroke. 2006; 37:82-86.
9. Baker ML, Hand PJ, Wang JJ, Wong TY. Retinal signs and stroke: revisiting the link between the eye and brain. Stroke. 2008;39: 1371-1379.
10. Wong TY, Klein R, Sharrett AR, et al. Cerebral white matter lesions, retinopathy, and incident clinical stroke. JAMA. 2002; 288:67-74.
11. Yu T, Mitchell P, Berry G, Li W, Wang JJ. Retinopathy in older persons without diabetes and its relationship to hypertension. Arch Ophthalmol. 1998;116:83-89.
12. Ishikawa K, Uyama M, Asayama K. Occlusive thromboaortopathy (Takayasu's disease): cervical arterial stenoses, retinal arterial pressure, retinal microaneurysms and prognosis. Stroke. 1983;14:730-735.
13. Wilkinson CP, Ferris FL III, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110: 1677-1682.
14. Hirai FE, Moss SE, Knudtson MD, Klein BE, Klein R. Retinopathy and survival in a population without diabetes: the Beaver Dam Eye Study. Am J Epidemiol. 2007;166:724-730.
15. 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. 1991;98:786-806.
16. Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98:823-833.
17. Klein R, Meuer SM, Moss SE, Klein BE. Retinal microaneurysm counts and 10-year progression of diabetic retinopathy. Arch Ophthalmol. 1995;113:1386-1391.
18. Sjolie AK, Klein R, Porta M, et al. Retinal microaneurysm count predicts progression and regression of diabetic retinopathy. Post-hoc results from the DIRECT Programme. Diabet Med. 2011;28:345-351.
19. Csaky KG, Richman EA, Ferris FL III. Report from the NEI/FDA Ophthalmic Clinical Trial Design and Endpoints Symposium. Invest Ophthalmol Vis Sci. 2008;49:479-489.
20. Klein R, Meuer SM, Moss SE, Klein BE. The relationship of retinal microaneurysm counts to the 4-year progression of diabetic retinopathy. Arch Ophthalmol. 1989;107:1780-1785.
21. Kohner EM, Sleightholm M. Does microaneurysm count reflect severity of early diabetic retinopathy? Ophthalmology. 1986;93:586-589.
22. Ribeiro ML, Nunes SG, Cunha-Vaz JG. Microaneurysm turnover at the macula predicts risk of development of clinically significant macular edema in persons with mild nonproliferative diabetic retinopathy. Diabetes Care. 2013;36:1254-1259.
23. Nunes S, Pires I, Rosa A, Duarte L, Bernardes R, Cunha-Vaz J. Microaneurysm turnover is a biomarker for diabetic retinopathy progression to clinically significant macular edema: findings for type 2 diabetics with nonproliferative retinopathy. Int J Ophthalmol. 2009;223:292-297.
24. Bernardes R, Nunes S, Pereira I, et al. Computer-assisted microaneurysm turnover in the early stages of diabetic retinopathy. Int J Ophthalmol. 2009;223:284-291.
25. Goatman KA, Cree MJ, Olson JA, Forrester JV, Sharp PF. Automated measurement of microaneurysm turnover. Invest Ophthalmol Vis Sci. 2003;44:5335-5341.
26. Kohner EM, Stratton IM, Aldington SJ, Turner RC, Matthews DR. Microaneurysms in the development of diabetic retinopathy (UKPDS 42). UK Prospective Diabetes Study Group. Diabetologia. 1999;42:1107-1112.
27. Murakami T, Nishijima K, Sakamoto A, Ota M, Horii T, Yoshimura N. Foveal cystoid spaces are associated with enlarged foveal avascular zone and microaneurysms in diabetic macular edema. Ophthalmology. 2011;118:359-367.
28. Cogan DG, Toussaint D, Kuwabara T. Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol. 1961;66:366-378.
29. de Oliveira F. Pericytes in diabetic retinopathy. Br J Ophthalmol. 1966;50:134-143.
30. Ashton N. Vascular basement membrane changes in diabetic retinopathy. Montgomery lecture, 1973. Br J Ophthalmol. 1974;58:344-366.
31. Wise G. Retinal microaneurysms. Arch Ophthalmol. 1957; 151-156.
32. Yanoff M, Fine BS. Ocular Pathology: A Text and Atlas. Hagerstown: Harper & Row; 1975.
33. Bresnick GH, Davis MD, Myers FL, de Venecia G. Clinicopathologic correlations in diabetic retinopathy. II. Clinical and histologic appearances of retinal capillary microaneurysms. Arch Ophthalmol. 1977;95:1215-1220.
34. Stitt AW, Gardiner TA, Archer DB. Histological and ultrastructural investigation of retinal microaneurysm development in diabetic patients. Br J Ophthalmol. 1995;79:362-367.
35. Moore J, Bagley S, Ireland G, McLeod D, Boulton ME. Three dimensional analysis of microaneurysms in the human diabetic retina. J Anat. 1999;194(pt 1):89-100.
36. Ezra E, Keinan E, Mandel Y, Boulton ME, Nahmias Y. Nondimensional analysis of retinal microaneurysms: critical threshold for treatment. Integr Biol. 2013;5:474-480.
37. Kozak I, Oster SF, Cortes MA, et al. Clinical evaluation and treatment accuracy in diabetic macular edema using navigated laser photocoagulator NAVILAS. Ophthalmology. 2011;118: 1119-1124.
38. Burgansky-Eliash Z, Barak A, Barash H, et al. Increased retinal blood flow velocity in patients with early diabetes mellitus. Retina. 2012;32:112-119.
39. Burgansky-Eliash Z, Nelson DA, Bar-Tal OP, Lowenstein A, Grinvald A, Barak A. Reduced retinal blood flow velocity in diabetic retinopathy. Retina. 2010;30:765-773.
40. Nelson DA, Burgansky-Eliash Z, Barash H, et al. High-resolution wide-field imaging of perfused capillaries without the use of contrast agent. Clin Ophthalmol. 2011;5:1095-1106.
41. Srinivasan VJ, Adler DC, Chen Y, et al. Ultrahigh-speed optical coherence tomography for three-dimensional and en face imaging of the retina and optic nerve head. Invest Ophthalmol Vis Sci. 2008;49:5103-5110.
42. Schmoll T, Singh ASG, Blatter C, et al. Imaging of the parafoveal capillary network and its integrity analysis using fractal dimension. Biomed Opt Express. 2011;2:1159-1168.
43. Zhi Z, Yin X, Dziennis S, et al. Optical microangiography of retina and choroid and measurement of total retinal blood flow in mice. Biomed Opt Express. 2012;3:2976-2986.
44. Kim DY, Fingler J, Werner JS, Schwartz DM, Fraser SE, Zawadzki RJ. In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography. Biomed Opt Express. 2011;2:1504-1513.
45. Kim DY, Fingler J, Zawadzki RJ, et al. Noninvasive imaging of the foveal avascular zone with high-speed, phase-variance optical coherence tomography. Invest Ophthalmol Vis Sci. 2012;53:85-92.
46. Zotter S, Pircher M, Torzicky T, et al. Visualization of microvasculature by dual-beam phase-resolved Doppler optical coherence tomography. Opt Express. 2011;19:1217-1227.
47. Bradley A, Zhang H, Applegate RA, Thibos LN, Elsner AE. Entoptic image quality of the retinal vasculature. Vision Res. 1998;38:2685-2696.
48. Yap M, Gilchrist J, Weatherill J. Psychophysical measurement of the foveal avascular zone. Ophthalmic Physiol Opt. 1987;7: 405-410.
49. Bird AC, Weale RA. On the retinal vasculature of the human fovea. Exp Eye Res. 1974;19:409-417.
50. Wang H, Chhablani J, Freeman WR, et al. Characterization of diabetic microaneurysms by simultaneous fluorescein angiography and spectral-domain optical coherence tomography. Am J Ophthalmol. 2012;153:861-867.
51. Rha J, Jonnal RS, Thorn KE, Qu J, Zhang Y, Miller DT. Adaptive optics flood-illumination camera for high speed retinal imaging. Opt Express. 2006;14:4552-4569.
52. Lombardo M, Parravano M, Serrao S, Ducoli P, Stirpe M, Lombardo G. Analysis of retinal capillaries in patients with type 1 diabetes and nonproliferative diabetic retinopathy using adaptive optics imaging. Retina. 2013;33:1630-1639.
53. Chui TY, Vannasdale DA, Burns SA. The use of forward scatter to improve retinal vascular imaging with an adaptive optics scanning laser ophthalmoscope. Biomed Opt Express. 2012;3: 2537-2549.
54. Chui TY, Zhong Z, Song H, Burns SA. Foveal avascular zone and its relationship to foveal pit shape. Optom Vis Sci. 2012; 89:602-610.
55. Tam J, Martin JA, Roorda A. Noninvasive visualization and analysis of parafoveal capillaries in humans. Invest Ophthalmol Vis Sci. 2010;51:1691-1698.
56. Tam J, Dhamdhere KP, Tiruveedhula P, et al. Disruption of the retinal parafoveal capillary network in type 2 diabetes before the onset of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2011;52:9257-9266.
57. Chui TY, Gast TJ, Burns SA. Imaging of vascular wall fine structure in human retina using adaptive optics scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci. 2013;54:7115-7124.
58. Miller DT, Kocaoglu OP, Wang Q, Lee S. Adaptive optics and the eye (super resolution OCT). Eye. 2011;25:321-330.
59. Wang Q, Kocaoglu OP, Cense B, et al. Imaging retinal capillaries using ultrahigh-resolution optical coherence tomography and adaptive optics. Invest Ophthalmol Vis Sci. 2011;52:6292-6299.
60. Pinhas A, Dubow M, Shah N, et al. In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography. Biomed Opt Express. 2013;4:1305-1317.
61. Smith G, Atchison DA. The Eye and Visual Optical Instruments. 1st ed. Cambridge: Cambridge University Press; 1997.
62. Dubra A, Sulai Y. Reflective afocal broadband adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011;2: 1757-1768.
63. Delori FC, Webb RH, Sliney DH. American National Standards I. Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices. J Opt Soc Am A. 2007;24:1250-1265.
64. Dubra A, Harvey Z. Registration of 2D Images from Fast Scanning Ophthalmic Instruments The 4th International Workshop on Biomedical Image Registration. Lübeck; Springer Berlin Heidelberg; 2010.
65. Fleiss JL, Levin B, Paik MC. Statistical Methods for Rates and Proportions. 3rd ed. New York: John Wiley & Sons; 2003.
66. Tam J, Dhamdhere KP, Tiruveedhula P, et al. Subclinical capillary changes in non-proliferative diabetic retinopathy. Optom Vis Sci. 2012;89:E692-E703.
67. Srinivasan VJ, Radhakrishnan H, Lo EH, et al. OCT methods for capillary velocimetry. Biomed Opt Express. 2012;3:612-629.
68. Braaf B, Vienola KV, Sheehy CK, et al. Real-time eye motion correction in phase-resolved OCT angiography with tracking SLO. Biomed Opt Express. 2013;4:51-65.
69. Jia Y, Morrison JC, Tokayer J, et al. Quantitative OCT angiography of optic nerve head blood flow. Biomed Opt Express. 2012;3:3127-3137.
70. Asari S, Ohmoto T. Natural history and risk factors of unruptured cerebral aneurysms. Clin Neurol Neurosurg. 1993;95:205-214.
71. Wiebers DO, Whisnant JP, O'Fallon WM. The natural history of unruptured intracranial aneurysms. N Engl J Med. 1981;304: 696-698.
72. Sampei T, Mizuno M, Nakajima S, et al. Clinical study of growing up aneurysms: report of 25 cases. Neurol Med Chir. 1991;19:825-830.
73. Hademenos GJ, Massoud TF, Turjman F, Sayre JW. Anatomical and morphological factors correlating with rupture of intracranial aneurysms in patients referred for endovascular treatment. Neuroradiology. 1998;40:755-760.