Abstract

Diabetic retinopathy (DR) is the leading cause of visual loss in working-age adults worldwide. Previous studies have found hemodynamic changes in the diabetic eyes, which precede clinically evident pathological alterations of the retinal microvasculature. There is a pressing need for new methods to allow greater understanding of these early hemodynamic changes that occur in DR. In this study, we propose a noninvasive method for the assessment of hemodynamics around the fovea (a region of the eye of paramount importance for vision). The proposed methodology combines adaptive optics scanning laser ophthalmoscopy and computational fluid dynamics modeling. We compare results obtained with this technique with in vivo measurements of blood flow based on blood cell aggregation tracking. Our results suggest that parafoveal hemodynamics, such as capillary velocity, wall shear stress, and capillary perfusion pressure can be noninvasively and reliably characterized with this method in both healthy and diabetic retinopathy patients.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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2016 (2)

A. de Castro, G. Huang, L. Sawides, T. Luo, and S. A. Burns, “Rapid high resolution imaging with a dual-channel scanning technique,” Opt. Lett. 41(8), 1881–1884 (2016).
[Crossref] [PubMed]

T. S. Hwang, S. S. Gao, L. Liu, A. K. Lauer, S. T. Bailey, C. J. Flaxel, D. J. Wilson, D. Huang, and Y. Jia, “Automated Quantification of Capillary Nonperfusion Using Optical Coherence Tomography Angiography in Diabetic Retinopathy,” JAMA Ophthalmol. 134(4), 367–373 (2016).
[Crossref] [PubMed]

2015 (1)

2014 (7)

J. B. Freund and J. Vermot, “The wall-stress footprint of blood cells flowing in microvessels,” Biophys. J. 106(3), 752–762 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

R. W. Nash, H. B. Carver, M. O. Bernabeu, J. Hetherington, D. Groen, T. Krüger, and P. V. Coveney, “Choice of boundary condition for lattice-Boltzmann simulation of moderate-Reynolds-number flow in complex domains,” Phys. Rev. E. 89(2), 1–13 (2014).

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
[Crossref] [PubMed]

2013 (1)

2012 (3)

2011 (2)

M. Potente, H. Gerhardt, and P. Carmeliet, “Basic and therapeutic aspects of angiogenesis,” Cell 146(6), 873–887 (2011).
[Crossref] [PubMed]

J. Tam and A. Roorda, “Speed quantification and tracking of moving objects in adaptive optics scanning laser ophthalmoscopy,” J. Biomed. Opt. 16(3), 036002 (2011).
[Crossref] [PubMed]

2010 (4)

Z. Burgansky-Eliash, D. A. Nelson, O. P. Bar-Tal, A. Lowenstein, A. Grinvald, and A. Barak, “Reduced retinal blood flow velocity in diabetic retinopathy,” Retina 30(5), 765–773 (2010).
[Crossref] [PubMed]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

N. Cheung, P. Mitchell, and T. Y. Wong, “Diabetic retinopathy,” Lancet 376(9735), 124–136 (2010).
[Crossref] [PubMed]

P. K. Yu, C. Balaratnasingam, W. H. Morgan, S. J. Cringle, I. L. McAllister, and D. Y. Yu, “The structural relationship between the microvasculature, neurons, and glia in the human retina,” Invest. Ophthalmol. Vis. Sci. 51(1), 447–458 (2010).
[Crossref] [PubMed]

2009 (4)

C. Hahn and M. A. Schwartz, “Mechanotransduction in vascular physiology and atherogenesis,” Nat. Rev. Mol. Cell Biol. 10(1), 53–62 (2009).
[Crossref] [PubMed]

T. M. Curtis, T. A. Gardiner, and A. W. Stitt, “Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis?” Eye (Lond.) 23(7), 1496–1508 (2009).
[Crossref] [PubMed]

J. Zhang, P. C. Johnson, and A. S. Popel, “Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows,” Microvasc. Res. 77(3), 265–272 (2009).
[Crossref] [PubMed]

J. L. McWhirter, H. Noguchi, and G. Gompper, “Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries,” Proc. Natl. Acad. Sci. U.S.A. 106(15), 6039–6043 (2009).
[Crossref] [PubMed]

2007 (4)

J. Boyd, J. M. Buick, and S. Green, “Analysis of the Casson and Carreau-Yasuda non-Newtonian blood models in steady and oscillatory flows using the lattice Boltzmann method,” Phys. Fluids 19(9), 093103 (2007).
[Crossref]

S. A. Burns, R. Tumbar, A. E. Elsner, D. Ferguson, and D. X. Hammer, “Large-Field-of-View, Modular, Stabilized, Adaptive-Optics-Based Scanning Laser Ophthalmoscope,” J. Opt. Soc. Am. A 24(5), 1313–1326 (2007).
[Crossref] [PubMed]

B. E. K. Klein, “Overview of epidemiologic studies of diabetic retinopathy,” Ophthalmic Epidemiol. 14(4), 179–183 (2007).
[Crossref] [PubMed]

R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

2006 (3)

A. S. Kwan, C. Barry, I. L. McAllister, and I. Constable, “Fluorescein angiography and adverse drug reactions revisited: the Lions Eye experience,” Clin. Experiment. Ophthalmol. 34(1), 33–38 (2006).
[Crossref] [PubMed]

T. Nagaoka and A. Yoshida, “Noninvasive evaluation of wall shear stress on retinal microcirculation in humans,” Invest. Ophthalmol. Vis. Sci. 47(3), 1113–1119 (2006).
[Crossref] [PubMed]

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

2005 (2)

A. R. Pries and T. W. Secomb, “Microvascular blood viscosity in vivo and the endothelial surface layer,” Am. J. Physiol. Heart Circ. Physiol. 289(6), H2657–H2664 (2005).
[Crossref] [PubMed]

J. A. Martin and A. Roorda, “Direct and noninvasive assessment of parafoveal capillary leukocyte velocity,” Ophthalmology 112(12), 2219–2224 (2005).
[Crossref] [PubMed]

2004 (2)

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
[Crossref] [PubMed]

R. H. Webb, M. J. Albanese, Y. Zhou, T. Bifano, and S. A. Burns, “Stroke amplifier for deformable mirrors,” Appl. Opt. 43(28), 5330–5333 (2004).
[Crossref] [PubMed]

1998 (1)

A. F. Frangi, “Multiscale vessel enhancement filtering,” Med. Image Comput. Comput. Assist. Interv. 1496, 130–137 (1998).

1997 (1)

A. Mendívil, V. Cuartero, and M. P. Mendívil, “Ocular blood flow velocities in patients with proliferative diabetic retinopathy after panretinal photocoagulation,” Surv. Ophthalmol. 42(13Suppl 1), S89–S95 (1997).
[Crossref] [PubMed]

1993 (1)

J. E. Grunwald, J. Piltz, N. Patel, S. Bose, and C. E. Riva, “Effect of aging on retinal macular microcirculation: a blue field simulation study,” Invest. Ophthalmol. Vis. Sci. 34(13), 3609–3613 (1993).
[PubMed]

1992 (1)

A. R. Pries, D. Neuhaus, and P. Gaehtgens, “Blood viscosity in tube flow: dependence on diameter and hematocrit,” Am. J. Physiol. 263(6 Pt 2), H1770–H1778 (1992).
[PubMed]

1961 (1)

H. R. Novotny and D. L. Alvis, “A Method of Photographing Fluorescence in Circulating Blood in the Human Retina,” Circulation 24(1), 82–86 (1961).
[Crossref] [PubMed]

Albanese, M. J.

Alvis, D. L.

H. R. Novotny and D. L. Alvis, “A Method of Photographing Fluorescence in Circulating Blood in the Human Retina,” Circulation 24(1), 82–86 (1961).
[Crossref] [PubMed]

Arichika, S.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
[Crossref] [PubMed]

Atasever, B.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Bailey, S. T.

T. S. Hwang, S. S. Gao, L. Liu, A. K. Lauer, S. T. Bailey, C. J. Flaxel, D. J. Wilson, D. Huang, and Y. Jia, “Automated Quantification of Capillary Nonperfusion Using Optical Coherence Tomography Angiography in Diabetic Retinopathy,” JAMA Ophthalmol. 134(4), 367–373 (2016).
[Crossref] [PubMed]

M. Zhang, J. Wang, A. D. Pechauer, T. S. Hwang, S. S. Gao, L. Liu, L. Liu, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Advanced image processing for optical coherence tomographic angiography of macular diseases,” Biomed. Opt. Express 6(12), 4661–4675 (2015).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

Balaratnasingam, C.

P. K. Yu, C. Balaratnasingam, W. H. Morgan, S. J. Cringle, I. L. McAllister, and D. Y. Yu, “The structural relationship between the microvasculature, neurons, and glia in the human retina,” Invest. Ophthalmol. Vis. Sci. 51(1), 447–458 (2010).
[Crossref] [PubMed]

Barak, A.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Z. Burgansky-Eliash, D. A. Nelson, O. P. Bar-Tal, A. Lowenstein, A. Grinvald, and A. Barak, “Reduced retinal blood flow velocity in diabetic retinopathy,” Retina 30(5), 765–773 (2010).
[Crossref] [PubMed]

Barash, H.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Barry, C.

A. S. Kwan, C. Barry, I. L. McAllister, and I. Constable, “Fluorescein angiography and adverse drug reactions revisited: the Lions Eye experience,” Clin. Experiment. Ophthalmol. 34(1), 33–38 (2006).
[Crossref] [PubMed]

Bar-Tal, O. P.

Z. Burgansky-Eliash, D. A. Nelson, O. P. Bar-Tal, A. Lowenstein, A. Grinvald, and A. Barak, “Reduced retinal blood flow velocity in diabetic retinopathy,” Retina 30(5), 765–773 (2010).
[Crossref] [PubMed]

Bernabeu, M. O.

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Johnson, P. C.

J. Zhang, P. C. Johnson, and A. S. Popel, “Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows,” Microvasc. Res. 77(3), 265–272 (2009).
[Crossref] [PubMed]

Jones, M. L.

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

Kastelein, J. J.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
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Kempen, J. H.

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
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Klein, B. E. K.

B. E. K. Klein, “Overview of epidemiologic studies of diabetic retinopathy,” Ophthalmic Epidemiol. 14(4), 179–183 (2007).
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Klein, M. L.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
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Klein, R.

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
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Kraus, M. F.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
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Kroon, J.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Krüger, T.

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

R. W. Nash, H. B. Carver, M. O. Bernabeu, J. Hetherington, D. Groen, T. Krüger, and P. V. Coveney, “Choice of boundary condition for lattice-Boltzmann simulation of moderate-Reynolds-number flow in complex domains,” Phys. Rev. E. 89(2), 1–13 (2014).

Kwan, A. S.

A. S. Kwan, C. Barry, I. L. McAllister, and I. Constable, “Fluorescein angiography and adverse drug reactions revisited: the Lions Eye experience,” Clin. Experiment. Ophthalmol. 34(1), 33–38 (2006).
[Crossref] [PubMed]

Lauer, A. K.

T. S. Hwang, S. S. Gao, L. Liu, A. K. Lauer, S. T. Bailey, C. J. Flaxel, D. J. Wilson, D. Huang, and Y. Jia, “Automated Quantification of Capillary Nonperfusion Using Optical Coherence Tomography Angiography in Diabetic Retinopathy,” JAMA Ophthalmol. 134(4), 367–373 (2016).
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Leske, M. C.

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
[Crossref] [PubMed]

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R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

Liu, J. J.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

Liu, L.

Lowenstein, A.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Z. Burgansky-Eliash, D. A. Nelson, O. P. Bar-Tal, A. Lowenstein, A. Grinvald, and A. Barak, “Reduced retinal blood flow velocity in diabetic retinopathy,” Retina 30(5), 765–773 (2010).
[Crossref] [PubMed]

Lu, C. D.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

Luo, T.

Marques, M. V. R. B.

R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

Martin, J. A.

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

J. A. Martin and A. Roorda, “Direct and noninvasive assessment of parafoveal capillary leukocyte velocity,” Ophthalmology 112(12), 2219–2224 (2005).
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McAllister, I. L.

P. K. Yu, C. Balaratnasingam, W. H. Morgan, S. J. Cringle, I. L. McAllister, and D. Y. Yu, “The structural relationship between the microvasculature, neurons, and glia in the human retina,” Invest. Ophthalmol. Vis. Sci. 51(1), 447–458 (2010).
[Crossref] [PubMed]

A. S. Kwan, C. Barry, I. L. McAllister, and I. Constable, “Fluorescein angiography and adverse drug reactions revisited: the Lions Eye experience,” Clin. Experiment. Ophthalmol. 34(1), 33–38 (2006).
[Crossref] [PubMed]

McWhirter, J. L.

J. L. McWhirter, H. Noguchi, and G. Gompper, “Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries,” Proc. Natl. Acad. Sci. U.S.A. 106(15), 6039–6043 (2009).
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Mehta, M.

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
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A. Mendívil, V. Cuartero, and M. P. Mendívil, “Ocular blood flow velocities in patients with proliferative diabetic retinopathy after panretinal photocoagulation,” Surv. Ophthalmol. 42(13Suppl 1), S89–S95 (1997).
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Mendívil, M. P.

A. Mendívil, V. Cuartero, and M. P. Mendívil, “Ocular blood flow velocities in patients with proliferative diabetic retinopathy after panretinal photocoagulation,” Surv. Ophthalmol. 42(13Suppl 1), S89–S95 (1997).
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Mitchell, P.

N. Cheung, P. Mitchell, and T. Y. Wong, “Diabetic retinopathy,” Lancet 376(9735), 124–136 (2010).
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Miyamoto, K.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
[Crossref] [PubMed]

Mooij, H. L.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Morgan, W. H.

P. K. Yu, C. Balaratnasingam, W. H. Morgan, S. J. Cringle, I. L. McAllister, and D. Y. Yu, “The structural relationship between the microvasculature, neurons, and glia in the human retina,” Invest. Ophthalmol. Vis. Sci. 51(1), 447–458 (2010).
[Crossref] [PubMed]

Moss, S. E.

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
[Crossref] [PubMed]

Murakami, T.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
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Nagaoka, T.

T. Nagaoka and A. Yoshida, “Noninvasive evaluation of wall shear stress on retinal microcirculation in humans,” Invest. Ophthalmol. Vis. Sci. 47(3), 1113–1119 (2006).
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Nash, R. W.

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

R. W. Nash, H. B. Carver, M. O. Bernabeu, J. Hetherington, D. Groen, T. Krüger, and P. V. Coveney, “Choice of boundary condition for lattice-Boltzmann simulation of moderate-Reynolds-number flow in complex domains,” Phys. Rev. E. 89(2), 1–13 (2014).

Nelson, D. A.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Z. Burgansky-Eliash, D. A. Nelson, O. P. Bar-Tal, A. Lowenstein, A. Grinvald, and A. Barak, “Reduced retinal blood flow velocity in diabetic retinopathy,” Retina 30(5), 765–773 (2010).
[Crossref] [PubMed]

Neuhaus, D.

A. R. Pries, D. Neuhaus, and P. Gaehtgens, “Blood viscosity in tube flow: dependence on diameter and hematocrit,” Am. J. Physiol. 263(6 Pt 2), H1770–H1778 (1992).
[PubMed]

Nielsen, J. H.

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

Nieuwdorp, M.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Noguchi, H.

J. L. McWhirter, H. Noguchi, and G. Gompper, “Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries,” Proc. Natl. Acad. Sci. U.S.A. 106(15), 6039–6043 (2009).
[Crossref] [PubMed]

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H. R. Novotny and D. L. Alvis, “A Method of Photographing Fluorescence in Circulating Blood in the Human Retina,” Circulation 24(1), 82–86 (1961).
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O’Colmain, B. J.

J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
[Crossref] [PubMed]

Ohbayashi, K.

Oliveira, C. L. D. A.

R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

Ooto, S.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
[Crossref] [PubMed]

Patel, N.

J. E. Grunwald, J. Piltz, N. Patel, S. Bose, and C. E. Riva, “Effect of aging on retinal macular microcirculation: a blue field simulation study,” Invest. Ophthalmol. Vis. Sci. 34(13), 3609–3613 (1993).
[PubMed]

Pechauer, A. D.

Pessoa, C. C.

R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

Piltz, J.

J. E. Grunwald, J. Piltz, N. Patel, S. Bose, and C. E. Riva, “Effect of aging on retinal macular microcirculation: a blue field simulation study,” Invest. Ophthalmol. Vis. Sci. 34(13), 3609–3613 (1993).
[PubMed]

Pinhas, A.

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

Popel, A. S.

J. Zhang, P. C. Johnson, and A. S. Popel, “Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows,” Microvasc. Res. 77(3), 265–272 (2009).
[Crossref] [PubMed]

Potente, M.

M. Potente, H. Gerhardt, and P. Carmeliet, “Basic and therapeutic aspects of angiogenesis,” Cell 146(6), 873–887 (2011).
[Crossref] [PubMed]

Potsaid, B.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

Pries, A. R.

A. R. Pries and T. W. Secomb, “Microvascular blood viscosity in vivo and the endothelial surface layer,” Am. J. Physiol. Heart Circ. Physiol. 289(6), H2657–H2664 (2005).
[Crossref] [PubMed]

A. R. Pries, D. Neuhaus, and P. Gaehtgens, “Blood viscosity in tube flow: dependence on diameter and hematocrit,” Am. J. Physiol. 263(6 Pt 2), H1770–H1778 (1992).
[PubMed]

Pupko, O.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Razeen, M.

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

Riva, C. E.

J. E. Grunwald, J. Piltz, N. Patel, S. Bose, and C. E. Riva, “Effect of aging on retinal macular microcirculation: a blue field simulation study,” Invest. Ophthalmol. Vis. Sci. 34(13), 3609–3613 (1993).
[PubMed]

Roorda, A.

J. Tam and A. Roorda, “Speed quantification and tracking of moving objects in adaptive optics scanning laser ophthalmoscopy,” J. Biomed. Opt. 16(3), 036002 (2011).
[Crossref] [PubMed]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

J. A. Martin and A. Roorda, “Direct and noninvasive assessment of parafoveal capillary leukocyte velocity,” Ophthalmology 112(12), 2219–2224 (2005).
[Crossref] [PubMed]

Rosen, R. B.

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

Rubinstein, A.

Z. Burgansky-Eliash, A. Barak, H. Barash, D. A. Nelson, O. Pupko, A. Lowenstein, A. Grinvald, and A. Rubinstein, “Increased retinal blood flow velocity in patients with early diabetes mellitus,” Retina 32(1), 112–119 (2012).
[Crossref] [PubMed]

Sawides, L.

Schmieschek, S.

M. O. Bernabeu, M. L. Jones, J. H. Nielsen, T. Krüger, R. W. Nash, D. Groen, S. Schmieschek, J. Hetherington, H. Gerhardt, C. A. Franco, and P. V. Coveney, “Computer simulations reveal complex distribution of haemodynamic forces in a mouse retina model of angiogenesis,” J. R. Soc. Interface 11(99), 20140543 (2014).
[Crossref] [PubMed]

Schwartz, M. A.

C. Hahn and M. A. Schwartz, “Mechanotransduction in vascular physiology and atherogenesis,” Nat. Rev. Mol. Cell Biol. 10(1), 53–62 (2009).
[Crossref] [PubMed]

Scoles, D.

Secomb, T. W.

A. R. Pries and T. W. Secomb, “Microvascular blood viscosity in vivo and the endothelial surface layer,” Am. J. Physiol. Heart Circ. Physiol. 289(6), H2657–H2664 (2005).
[Crossref] [PubMed]

Shah, N.

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

Shimizu, K.

Silva, A. R.

R. P. C. Lira, C. L. D. A. Oliveira, M. V. R. B. Marques, A. R. Silva, and C. C. Pessoa, “Adverse reactions of fluorescein angiography: a prospective study,” Arq. Bras. Oftalmol. 70(4), 615–618 (2007).
[Crossref] [PubMed]

Spaan, J. A.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Stitt, A. W.

T. M. Curtis, T. A. Gardiner, and A. W. Stitt, “Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis?” Eye (Lond.) 23(7), 1496–1508 (2009).
[Crossref] [PubMed]

Stroes, E. S.

M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
[Crossref] [PubMed]

Sulai, Y. N.

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

Tam, J.

J. Tam and A. Roorda, “Speed quantification and tracking of moving objects in adaptive optics scanning laser ophthalmoscopy,” J. Biomed. Opt. 16(3), 036002 (2011).
[Crossref] [PubMed]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

Tan, O.

Y. Jia, S. T. Bailey, D. J. Wilson, O. Tan, M. L. Klein, C. J. Flaxel, B. Potsaid, J. J. Liu, C. D. Lu, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration,” Ophthalmology 121(7), 1435–1444 (2014).
[Crossref] [PubMed]

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J. H. Kempen, B. J. O’Colmain, M. C. Leske, S. M. Haffner, R. Klein, S. E. Moss, H. R. Taylor, R. F. Hamman, and Eye Diseases Prevalence Research Group, “The prevalence of diabetic retinopathy among adults in the United States,” Arch. Ophthalmol. 122(4), 552–563 (2004).
[Crossref] [PubMed]

Tumbar, R.

Uji, A.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
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Unoki, N.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
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J. B. Freund and J. Vermot, “The wall-stress footprint of blood cells flowing in microvessels,” Biophys. J. 106(3), 752–762 (2014).
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M. Nieuwdorp, H. L. Mooij, J. Kroon, B. Atasever, J. A. Spaan, C. Ince, F. Holleman, M. Diamant, R. J. Heine, J. B. Hoekstra, J. J. Kastelein, E. S. Stroes, and H. Vink, “Endothelial Glycocalyx Damage Coincides with Microalbuminuria in Type 1 Diabetes,” Diabetes 55(4), 1127–1132 (2006).
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A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

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Webb, R. H.

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A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
[Crossref] [PubMed]

M. Dubow, A. Pinhas, N. Shah, R. F. Cooper, A. Gan, R. C. Gentile, V. Hendrix, Y. N. Sulai, J. Carroll, T. Y. P. Chui, J. B. Walsh, R. Weitz, A. Dubra, and R. B. Rosen, “Classification of Human Retinal Microaneurysms using Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 55(3), 1299–1309 (2014).
[Crossref] [PubMed]

A. Pinhas, M. Dubow, N. Shah, T. Y. Chui, D. Scoles, Y. N. Sulai, R. Weitz, J. B. Walsh, J. Carroll, A. Dubra, and R. B. Rosen, “In vivo imaging of human retinal microvasculature using adaptive optics scanning light ophthalmoscope fluorescein angiography,” Biomed. Opt. Express 4(8), 1305–1317 (2013).
[Crossref] [PubMed]

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T. S. Hwang, S. S. Gao, L. Liu, A. K. Lauer, S. T. Bailey, C. J. Flaxel, D. J. Wilson, D. Huang, and Y. Jia, “Automated Quantification of Capillary Nonperfusion Using Optical Coherence Tomography Angiography in Diabetic Retinopathy,” JAMA Ophthalmol. 134(4), 367–373 (2016).
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[Crossref] [PubMed]

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N. Cheung, P. Mitchell, and T. Y. Wong, “Diabetic retinopathy,” Lancet 376(9735), 124–136 (2010).
[Crossref] [PubMed]

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Yoshitake, S.

S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
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J. Zhang, P. C. Johnson, and A. S. Popel, “Effects of erythrocyte deformability and aggregation on the cell free layer and apparent viscosity of microscopic blood flows,” Microvasc. Res. 77(3), 265–272 (2009).
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J. B. Freund and J. Vermot, “The wall-stress footprint of blood cells flowing in microvessels,” Biophys. J. 106(3), 752–762 (2014).
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Eye (Lond.) (1)

T. M. Curtis, T. A. Gardiner, and A. W. Stitt, “Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis?” Eye (Lond.) 23(7), 1496–1508 (2009).
[Crossref] [PubMed]

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S. Arichika, A. Uji, T. Murakami, N. Unoki, S. Yoshitake, Y. Dodo, S. Ooto, K. Miyamoto, and N. Yoshimura, “Retinal Hemorheologic Characterization of Early-stage Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 55(12), 8513–8522 (2014).
[Crossref] [PubMed]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci. 51(3), 1691–1698 (2010).
[Crossref] [PubMed]

P. K. Yu, C. Balaratnasingam, W. H. Morgan, S. J. Cringle, I. L. McAllister, and D. Y. Yu, “The structural relationship between the microvasculature, neurons, and glia in the human retina,” Invest. Ophthalmol. Vis. Sci. 51(1), 447–458 (2010).
[Crossref] [PubMed]

A. Pinhas, M. Razeen, M. Dubow, A. Gan, T. Y. Chui, N. Shah, M. Mehta, R. C. Gentile, R. Weitz, J. B. Walsh, Y. N. Sulai, J. Carroll, A. Dubra, and R. B. Rosen, “Assessment of Perfused Foveal Microvascular Density and Identification of Nonperfused Capillaries in Healthy and Vasculopathic Eyes,” Invest. Ophthalmol. Vis. Sci. 55(12), 8056–8066 (2014).
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[Crossref] [PubMed]

T. Nagaoka and A. Yoshida, “Noninvasive evaluation of wall shear stress on retinal microcirculation in humans,” Invest. Ophthalmol. Vis. Sci. 47(3), 1113–1119 (2006).
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J. E. Grunwald, J. Piltz, N. Patel, S. Bose, and C. E. Riva, “Effect of aging on retinal macular microcirculation: a blue field simulation study,” Invest. Ophthalmol. Vis. Sci. 34(13), 3609–3613 (1993).
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Supplementary Material (1)

NameDescription
» Visualization 1: AVI (6021 KB)      Blood cell aggregation tracking video

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Figures (8)

Fig. 1
Fig. 1 AOSLO system schematic layout (not to scale).
Fig. 2
Fig. 2 AOSLO perfusion maps montaged at fovea over fundus photograph. Control group case (Eye #5). Scale bar = 500 µm.
Fig. 3
Fig. 3 Parafoveal capillary network from control group (Eye #5). Left: central 3 ° × 3° of the capillary network (Auto-Blended in Photoshop). Right: segmentation results from AOSLO image with the same field of view. Scale bar = 100µm.
Fig. 4
Fig. 4 3D view of the reconstructed luminal surface with close-up of one of the corrected vessel crossings (indicated by the arrow).
Fig. 5
Fig. 5 CPP and WSS map from a control (Eye #5, top panel) and DR case (Eye #4, bottom panel). Left panel: CPP across the network (defined as the pressure difference with respect to the network outlets). Right panel: WSS magnitudes across the network. Scale bar = 100µm.
Fig. 6
Fig. 6 Subsets of the network from Eye #5 directly perfused by two of the dominant inlets (solid arrowheads) in the superior half of the parafoveal region (left and right panel, respectively). Colored streamlines define the path followed by the bloodstream starting at each of the inlets labeled with solid arrowheads. Additional neighboring inlets are labeled with empty arrowheads. Streamlines were computed based on the simulation results with the Paraview (Kitware Inc.) software.
Fig. 7
Fig. 7 Top left panel: BCA tracking vessel segments in Eye #5. Top right panel: Velocity results comparison between BCA tracking and flow model in Eye #5. Bottom left panel: BCA tracking vessel segments in Eye #4. Bottom right panel: Velocity results comparison between BCA tracking and flow model in Eye #4. Highlighted segments are where path with visible BCA.
Fig. 8
Fig. 8 Example of BCA tracking in 5 sequential frames in Eye #5, Segment #3 (Fig. 7 top left panel). Frame rate 29 Hz (Visualization 1).

Tables (3)

Tables Icon

Table 1 Study Eye and Participant Demographics

Tables Icon

Table 2 Summary statistics of the main hemodynamic variables of interest for all the flow models developed. Velocity, wall shear stress magnitude (WSS), and capillary perfusion pressure (CPP).

Tables Icon

Table 3 Comparison on velocity between BCA tracking vs. flow model

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

v = 0 ρ ( v t + v v ) = P + ,
T i , j = 2 η S i j S i j = 1 2 ( v j x i + v i x j )   ,
γ ˙ = 2 S i j S i j ,
v ( x , 0 ) = 0 ,       x ϵ Ω ¯ ,
v = 0 ,       x ϵ Ω w , P n ^ η ρ v n ^ = P o n ^   ,       x ϵ Ω o , v ( x , t ) = v i ( r ) ,       x ϵ Ω i   ,       t > 0 ,
v i ( r ) = V m a x ( 1 r 2 R i 2 )   n ^ ,

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