Abstract

Optical coherence tomography angiography (OCTA) has recently emerged for imaging vasculature in clinical ophthalmology. Yet, OCTA images contain artifacts that remain challenging to interpret. To help explain these artifacts, we perform contrast-enhanced OCTA with a custom-designed wide-field ophthalmoscope in rats in vivo. We choose an intravascular contrast agent (Intralipid) with particles that are more isotropically scattering and more symmetrically shaped than red blood cells (RBCs). Then, by examining how OCTA artifacts change after contrast agent injection, we attribute OCTA artifacts to RBC-specific properties. In this work, we investigate retinal and choroidal OCTA in rats with or without melanosomes, both before and after contrast agent injection, at a wavelength at which scattering dominates the image contrast (1300 nm). First, baseline images suggest that high backscattering of choroidal melanosomes accounts for the relatively dark appearance of choroidal vessel lumens in OCTA. Second, Intralipid injection tends to eliminate the hourglass pattern artifact in OCTA images of vessel lumens and highlights vertical capillaries that were previously faint in OCTA, showing that RBC orientation is important in determining OCTA signal. Third, Intralipid injection increases lumen signal without significantly affecting the tails, suggesting that projection artifacts, or tails, are due to RBC multiple scattering. Fourth, Intralipid injection increases the side-to-top signal ratio less in choroidal vessel lumens of pigmented rats, suggesting that melanosome multiple scattering makes the hourglass artifact less prominent. This study provides the first direct experimental in vivo evidence to explain light scattering-related artifacts in OCTA.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (2)

2016 (5)

2015 (12)

A. Zhang, Q. Zhang, and R. K. Wang, “Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography,” Biomed. Opt. Express 6(10), 4130–4143 (2015).
[Crossref] [PubMed]

C. Leahy, H. Radhakrishnan, G. Weiner, J. L. Goldberg, and V. J. Srinivasan, “Mapping the 3D Connectivity of the Rat Inner Retinal Vascular Network Using OCT Angiography,” Invest. Ophthalmol. Vis. Sci. 56(10), 5785–5793 (2015).
[Crossref] [PubMed]

B. Baumann, J. Schirmer, S. Rauscher, S. Fialová, M. Glösmann, M. Augustin, M. Pircher, M. Gröger, and C. K. Hitzenberger, “Melanin Pigmentation in Rat Eyes: In Vivo Imaging by Polarization-Sensitive Optical Coherence Tomography and Comparison to Histology,” Invest. Ophthalmol. Vis. Sci. 56(12), 7462–7472 (2015).
[Crossref] [PubMed]

J. Yi, W. Liu, S. Chen, V. Backman, N. Sheibani, C. M. Sorenson, A. A. Fawzi, R. A. Linsenmeier, and H. F. Zhang, “Visible light optical coherence tomography measures retinal oxygen metabolic response to systemic oxygenation,” Light Sci. Appl. 4(9), e334 (2015).
[Crossref] [PubMed]

E. Orhan, D. Dalkara, M. Neuillé, C. Lechauve, C. Michiels, S. Picaud, T. Léveillard, J.-A. Sahel, M. I. Naash, M. M. Lavail, C. Zeitz, and I. Audo, “Genotypic and Phenotypic Characterization of P23H line 1 Rat Model,” PLoS One 10(5), e0127319 (2015).
[Crossref] [PubMed]

L. C. Ho, B. Wang, I. P. Conner, Y. van der Merwe, R. A. Bilonick, S.-G. Kim, E. X. Wu, I. A. Sigal, G. Wollstein, J. S. Schuman, and K. C. Chan, “In Vivo Evaluation of White Matter Integrity and Anterograde Transport in Visual System After Excitotoxic Retinal Injury With Multimodal MRI and OCT,” Invest. Ophthalmol. Vis. Sci. 56(6), 3788–3800 (2015).
[Crossref] [PubMed]

P. E. Z. Tan, C. Balaratnasingam, J. Xu, Z. Mammo, S. X. Han, P. Mackenzie, A. W. Kirker, D. Albiani, A. B. Merkur, M. V. Sarunic, and D.-Y. Yu, “Quantitative Comparison of Retinal Capillary Images Derived By Speckle Variance Optical Coherence Tomography With Histology,” Invest. Ophthalmol. Vis. Sci. 56(6), 3989–3996 (2015).
[Crossref] [PubMed]

R. F. Spaide, J. G. Fujimoto, and N. K. Waheed, “Image Artifacts in Optical Coherence Angiography,” Retina 35(11), 2163–2180 (2015).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (2015).
[Crossref] [PubMed]

A. Ishibazawa, T. Nagaoka, A. Takahashi, T. Omae, T. Tani, K. Sogawa, H. Yokota, and A. Yoshida, “Optical Coherence Tomography Angiography in Diabetic Retinopathy: A Prospective Pilot Study,” Am. J. Ophthalmol. 160(1), 35–44 (2015).
[Crossref] [PubMed]

R. F. Spaide, “Optical Coherence Tomography Angiography Signs of Vascular Abnormalization With Antiangiogenic Therapy for Choroidal Neovascularization,” Am. J. Ophthalmol. 160(1), 6–16 (2015).
[Crossref] [PubMed]

T. E. de Carlo, M. A. Bonini Filho, A. T. Chin, M. Adhi, D. Ferrara, C. R. Baumal, A. J. Witkin, E. Reichel, J. S. Duker, and N. K. Waheed, “Spectral-domain optical coherence tomography angiography of choroidal neovascularization,” Ophthalmology 122(6), 1228–1238 (2015).
[Crossref] [PubMed]

2014 (11)

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]

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical coherence tomography angiography of optic disc perfusion in glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[Crossref] [PubMed]

K. V. Bhavsar, L. Branchini, H. Shah, C. V. Regatieri, and J. S. Duker, “Choroidal Thickness in Retinal Pigment Epithelial Tear as Measured by Spectral Domain Optical Coherence Tomography,” Retina 34(1), 63–68 (2014).
[Crossref] [PubMed]

A. Willerslev, X. Q. Li, I. C. Munch, and M. Larsen, “Flow patterns on spectral-domain optical coherence tomography reveal flow directions at retinal vessel bifurcations,” Acta Ophthalmol. 92(5), 461–464 (2014).
[Crossref] [PubMed]

Y. Pan, J. You, N. D. Volkow, K. Park, and C. Du, “Ultrasensitive detection of 3D cerebral microvascular network dynamics in vivo,” Neuroimage 103, 492–501 (2014).
[Crossref] [PubMed]

N. Bosschaart, G. J. Edelman, M. C. G. Aalders, T. G. van Leeuwen, and D. J. Faber, “A literature review and novel theoretical approach on the optical properties of whole blood,” Lasers Med. Sci. 29(2), 453–479 (2014).
[Crossref] [PubMed]

P. Vasa, J. A. Dharmadhikari, A. K. Dharmadhikari, R. Sharma, M. Singh, and D. Mathur, “Supercontinuum generation in water by intense, femtosecond laser pulses under anomalous chromatic dispersion,” Phys. Rev. A 89(4), 043834 (2014).
[Crossref]

W. Song, Q. Wei, W. Liu, T. Liu, J. Yi, N. Sheibani, A. A. Fawzi, R. A. Linsenmeier, S. Jiao, and H. F. Zhang, “A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography,” Sci. Rep. 4, 6525 (2014).

R. A. C. van Huet, N. M. Bax, S. C. Westeneng-Van Haaften, M. Muhamad, M. N. Zonneveld-Vrieling, L. H. Hoefsloot, F. P. M. Cremers, C. J. F. Boon, B. J. Klevering, and C. B. Hoyng, “Foveal Sparing in Stargardt Disease,” Invest. Ophthalmol. Vis. Sci. 55(11), 7467–7478 (2014).
[Crossref] [PubMed]

A. Willerslev, X. Q. Li, P. Cordtz, I. C. Munch, and M. Larsen, “Retinal and choroidal intravascular spectral-domain optical coherence tomography,” Acta Ophthalmol. 92(2), 126–132 (2014).
[Crossref] [PubMed]

D. A. Fedosov, M. Peltomäki, and G. Gompper, “Deformation and dynamics of red blood cells in flow through cylindrical microchannels,” Soft Matter 10(24), 4258–4267 (2014).
[Crossref] [PubMed]

2013 (6)

H. Radhakrishnan and V. J. Srinivasan, “Multiparametric optical coherence tomography imaging of the inner retinal hemodynamic response to visual stimulation,” J. Biomed. Opt. 18(8), 086010 (2013).
[Crossref] [PubMed]

J. Liu, I. Grulkowski, M. Kraus, B. Potsaid, C. D Lu, B. Baumann, J. Duker, J. Hornegger, and J. G Fujimoto, “In vivo imaging of the rodent eye with swept source/Fourier domain OCT,” Biomed. Opt. Express 4, 351–363 (2013).

C. M. Dickson, C. T. Ogbuah, and T. G. Smith, “The role of gamont entry into erythrocytes in the specificity of Hepatozoon species (Apicomplexa: Adeleida) for their frog hosts,” J. Parasitol. 99(6), 1028–1033 (2013).
[Crossref] [PubMed]

Y. Muraoka, A. Tsujikawa, T. Murakami, K. Ogino, K. Kumagai, K. Miyamoto, A. Uji, and N. Yoshimura, “Morphologic and functional changes in retinal vessels associated with branch retinal vein occlusion,” Ophthalmology 120(1), 91–99 (2013).
[Crossref] [PubMed]

W. Choi, K. J. Mohler, B. Potsaid, C. D. Lu, J. J. Liu, V. Jayaraman, A. E. Cable, J. S. Duker, R. Huber, and J. G. Fujimoto, “Choriocapillaris and choroidal microvasculature imaging with ultrahigh speed OCT angiography,” PLoS One 8(12), e81499 (2013).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, R. J. Zawadzki, S. S. Park, L. S. Morse, D. M. Schwartz, S. E. Fraser, and J. S. Werner, “Optical imaging of the chorioretinal vasculature in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 110(35), 14354–14359 (2013).
[Crossref] [PubMed]

2012 (6)

C. V. Regatieri, L. Branchini, J. G. Fujimoto, and J. S. Duker, “Choroidal imaging using spectral-domain Optical Coherence Tomography,” Retina 32(5), 865–876 (2012).
[Crossref] [PubMed]

B. Baumann, W. Choi, B. Potsaid, D. Huang, J. S. Duker, and J. G. Fujimoto, “Swept source/Fourier domain polarization sensitive optical coherence tomography with a passive polarization delay unit,” Opt. Express 20(9), 10229–10241 (2012).
[Crossref] [PubMed]

B. Baumann, S. O. Baumann, T. Konegger, M. Pircher, E. Götzinger, F. Schlanitz, C. Schütze, H. Sattmann, M. Litschauer, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Polarization sensitive optical coherence tomography of melanin provides intrinsic contrast based on depolarization,” Biomed. Opt. Express 3(7), 1670–1683 (2012).
[Crossref] [PubMed]

K. Kurokawa, K. Sasaki, S. Makita, Y.-J. Hong, and Y. Yasuno, “Three-dimensional retinal and choroidal capillary imaging by power Doppler optical coherence angiography with adaptive optics,” Opt. Express 20(20), 22796–22812 (2012).
[Crossref] [PubMed]

S. Kedenburg, M. Vieweg, T. Gissibl, and H. Giessen, “Linear refractive index and absorption measurements of nonlinear optical liquids in the visible and near-infrared spectral region,” Opt. Mater. Express 2(11), 1588–1611 (2012).
[Crossref]

D. C. Lozano and M. D. Twa, “Quantitative Evaluation of Factors Influencing the Repeatability of SD-OCT Thickness Measurements in the Rat,” Invest. Ophthalmol. Vis. Sci. 53(13), 8378–8385 (2012).
[Crossref] [PubMed]

2011 (6)

X. Zhang, J. Hu, R. W Knighton, X.-R. Huang, C. A Puliafito, and S. Jiao, “Visible light optical coherence tomography for in vivo imaging the spectral contrasts of the retinal nerve fiber layer,” Proc. SPIE 19, 19653–19659 (2011).

N. Zabouri, J. F. Bouchard, and C. Casanova, “Cannabinoid receptor type 1 expression during postnatal development of the rat retina,” J. Comp. Neurol. 519(7), 1258–1280 (2011).
[Crossref] [PubMed]

Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express 2(3), 579–591 (2011).
[Crossref] [PubMed]

V. M. Kodach, D. J. Faber, J. van Marle, T. G. van Leeuwen, and J. Kalkman, “Determination of the scattering anisotropy with optical coherence tomography,” Opt. Express 19(7), 6131–6140 (2011).
[Crossref] [PubMed]

H. C. Hendargo, R. P. McNabb, A.-H. Dhalla, N. Shepherd, and J. A. Izatt, “Doppler velocity detection limitations in spectrometer-based versus swept-source optical coherence tomography,” Biomed. Opt. Express 2(8), 2175–2188 (2011).
[Crossref] [PubMed]

P. Cimalla, J. Walther, M. Mittasch, and E. Koch, “Shear flow-induced optical inhomogeneity of blood assessed in vivo and in vitro by spectral domain optical coherence tomography in the 1.3 μm wavelength range,” J. Biomed. Opt. 16(11), 116020 (2011).
[Crossref] [PubMed]

2010 (3)

M. Diez-Silva, M. Dao, J. Han, C.-T. Lim, and S. Suresh, “Shape and Biomechanical Characteristics of Human Red Blood Cells in Health and Disease,” MRS Bull. 35(5), 382–388 (2010).
[Crossref] [PubMed]

S. Jiao, M. Jiang, J. Hu, A. Fawzi, Q. Zhou, K. K. Shung, C. A. Puliafito, and H. F. Zhang, “Photoacoustic ophthalmoscopy for in vivo retinal imaging,” Opt. Express 18(4), 3967–3972 (2010).
[Crossref] [PubMed]

R. Nachabé, B. H. Hendriks, A. E. Desjardins, M. van der Voort, M. B. van der Mark, and H. J. Sterenborg, “Estimation of lipid and water concentrations in scattering media with diffuse optical spectroscopy from 900 to 1,600 nm,” J. Biomed. Opt. 15(3), 037015 (2010).
[Crossref] [PubMed]

2009 (1)

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

2008 (2)

E. Götzinger, M. Pircher, W. Geitzenauer, C. Ahlers, B. Baumann, S. Michels, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Retinal pigment epithelium segmentation by polarization sensitive optical coherence tomography,” Opt. Express 16(21), 16410–16422 (2008).
[Crossref] [PubMed]

D. P. Popescu and M. G. Sowa, “In Vitro Assessment of Optical Properties of Blood by Applying the Extended Huygens-Fresnel Principle to Time-Domain Optical Coherence Tomography Signal at 1300 nm,” Int. J. Biomed. Imaging 2008, 591618 (2008).
[Crossref] [PubMed]

2006 (1)

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S.-E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive Volumetric Imaging and Morphometry of the Rodent Retina with High-Speed, Ultrahigh-Resolution Optical Coherence Tomography,” Invest. Ophthalmol. Vis. Sci. 47(12), 5522–5528 (2006).
[Crossref] [PubMed]

2005 (2)

S. S. Sandhu and S. J. Talks, “Correlation of optical coherence tomography, with or without additional colour fundus photography, with stereo fundus fluorescein angiography in diagnosing choroidal neovascular membranes,” Br. J. Ophthalmol. 89(8), 967–970 (2005).
[Crossref] [PubMed]

H. Noguchi and G. Gompper, “Shape transitions of fluid vesicles and red blood cells in capillary flows,” Proc. Natl. Acad. Sci. U.S.A. 102(40), 14159–14164 (2005).
[Crossref] [PubMed]

2004 (1)

2001 (2)

T. R. Gregory, “The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates,” Blood Cells Mol. Dis. 27(5), 830–843 (2001).
[Crossref] [PubMed]

M. Hammer, A. N. Yaroslavsky, and D. Schweitzer, “A scattering phase function for blood with physiological haematocrit,” Phys. Med. Biol. 46(3), N65–N69 (2001).
[Crossref] [PubMed]

1999 (2)

A. Roggan, M. Friebel, K. Dö Rschel, A. Hahn, and G. Mü Ller, “Optical Properties of Circulating Human Blood in the Wavelength Range 400-2500 nm,” J. Biomed. Opt. 4(1), 36–46 (1999).
[Crossref] [PubMed]

K. Sugiyama, Z.-B. Gu, C. Kawase, T. Yamamoto, and Y. Kitazawa, “Optic Nerve and Peripapillary Choroidal Microvasculature of the Rat Eye,” Invest. Ophthalmol. Vis. Sci. 40(13), 3084–3090 (1999).
[PubMed]

1991 (1)

C. M. Hawkey, P. M. Bennett, S. C. Gascoyne, M. G. Hart, and J. K. Kirkwood, “Erythrocyte size, number and haemoglobin content in vertebrates,” Br. J. Haematol. 77(3), 392–397 (1991).
[Crossref] [PubMed]

1988 (1)

S. Banerjee, K. Misra, S. Banerjee, and S. Ray‐Chaudhuri, “Chromosome numbers, genome sizes, cell volumes and evolution of snake‐head fish (family Channidae),” J. Fish Biol. 33(5), 781–789 (1988).
[Crossref]

1984 (1)

P. B. Canham, R. F. Potter, and D. Woo, “Geometric accommodation between the dimensions of erythrocytes and the calibre of heart and muscle capillaries in the rat,” J. Physiol. 347(1), 697–712 (1984).
[Crossref] [PubMed]

1980 (1)

H. Yoshimoto, M. Murata, K. Yamagami, and S. Matsuyama, “Studies on the angioarchitecture of the posterior choroid in rat and role of posterior ciliary vein,” Invest. Ophthalmol. Vis. Sci. 19(10), 1245–1250 (1980).
[PubMed]

1979 (1)

A. Hughes and H. Wässle, “An estimate of image quality in the rat eye,” Invest. Ophthalmol. Vis. Sci. 18(8), 878–881 (1979).
[PubMed]

1977 (2)

W. Frair, “Sea turtle red blood cell parameters correlated with carapace lengths,” Comp. Biochem. Physiol. Part A. Physiol. 56(4), 467–472 (1977).
[Crossref]

W. Frair, “Turtle red blood cell packed volumes, sizes, and numbers,” Herpetologica 33, 167–190 (1977).

1941 (1)

L. G. Henyey and J. L. Greenstein, “Diffuse radiation in the galaxy,” Astrophys. J. 93, 70–83 (1941).
[Crossref]

1937 (1)

P. Bartsch, W. Ball, W. Rosenzweig, and S. Salman, “Size of red blood corpuscles and their nucleus in fifty North American birds,” Auk 54(4), 516–519 (1937).
[Crossref]

Aalders, M. C. G.

N. Bosschaart, G. J. Edelman, M. C. G. Aalders, T. G. van Leeuwen, and D. J. Faber, “A literature review and novel theoretical approach on the optical properties of whole blood,” Lasers Med. Sci. 29(2), 453–479 (2014).
[Crossref] [PubMed]

Adhi, M.

T. E. de Carlo, M. A. Bonini Filho, A. T. Chin, M. Adhi, D. Ferrara, C. R. Baumal, A. J. Witkin, E. Reichel, J. S. Duker, and N. K. Waheed, “Spectral-domain optical coherence tomography angiography of choroidal neovascularization,” Ophthalmology 122(6), 1228–1238 (2015).
[Crossref] [PubMed]

Ahlers, C.

Albiani, D.

P. E. Z. Tan, C. Balaratnasingam, J. Xu, Z. Mammo, S. X. Han, P. Mackenzie, A. W. Kirker, D. Albiani, A. B. Merkur, M. V. Sarunic, and D.-Y. Yu, “Quantitative Comparison of Retinal Capillary Images Derived By Speckle Variance Optical Coherence Tomography With Histology,” Invest. Ophthalmol. Vis. Sci. 56(6), 3989–3996 (2015).
[Crossref] [PubMed]

Armour, R. L.

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical coherence tomography angiography of optic disc perfusion in glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[Crossref] [PubMed]

Audo, I.

E. Orhan, D. Dalkara, M. Neuillé, C. Lechauve, C. Michiels, S. Picaud, T. Léveillard, J.-A. Sahel, M. I. Naash, M. M. Lavail, C. Zeitz, and I. Audo, “Genotypic and Phenotypic Characterization of P23H line 1 Rat Model,” PLoS One 10(5), e0127319 (2015).
[Crossref] [PubMed]

Augustin, M.

M. Salas, M. Augustin, L. Ginner, A. Kumar, B. Baumann, R. Leitgeb, W. Drexler, S. Prager, J. Hafner, U. Schmidt-Erfurth, and M. Pircher, “Visualization of micro-capillaries using optical coherence tomography angiography with and without adaptive optics,” Biomed. Opt. Express 8(1), 207–222 (2017).
[Crossref] [PubMed]

B. Baumann, J. Schirmer, S. Rauscher, S. Fialová, M. Glösmann, M. Augustin, M. Pircher, M. Gröger, and C. K. Hitzenberger, “Melanin Pigmentation in Rat Eyes: In Vivo Imaging by Polarization-Sensitive Optical Coherence Tomography and Comparison to Histology,” Invest. Ophthalmol. Vis. Sci. 56(12), 7462–7472 (2015).
[Crossref] [PubMed]

Backman, V.

J. Yi, W. Liu, S. Chen, V. Backman, N. Sheibani, C. M. Sorenson, A. A. Fawzi, R. A. Linsenmeier, and H. F. Zhang, “Visible light optical coherence tomography measures retinal oxygen metabolic response to systemic oxygenation,” Light Sci. Appl. 4(9), e334 (2015).
[Crossref] [PubMed]

Bailey, S. T.

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (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. E. Z. Tan, C. Balaratnasingam, J. Xu, Z. Mammo, S. X. Han, P. Mackenzie, A. W. Kirker, D. Albiani, A. B. Merkur, M. V. Sarunic, and D.-Y. Yu, “Quantitative Comparison of Retinal Capillary Images Derived By Speckle Variance Optical Coherence Tomography With Histology,” Invest. Ophthalmol. Vis. Sci. 56(6), 3989–3996 (2015).
[Crossref] [PubMed]

Ball, W.

P. Bartsch, W. Ball, W. Rosenzweig, and S. Salman, “Size of red blood corpuscles and their nucleus in fifty North American birds,” Auk 54(4), 516–519 (1937).
[Crossref]

Banerjee, S.

S. Banerjee, K. Misra, S. Banerjee, and S. Ray‐Chaudhuri, “Chromosome numbers, genome sizes, cell volumes and evolution of snake‐head fish (family Channidae),” J. Fish Biol. 33(5), 781–789 (1988).
[Crossref]

S. Banerjee, K. Misra, S. Banerjee, and S. Ray‐Chaudhuri, “Chromosome numbers, genome sizes, cell volumes and evolution of snake‐head fish (family Channidae),” J. Fish Biol. 33(5), 781–789 (1988).
[Crossref]

Bartsch, P.

P. Bartsch, W. Ball, W. Rosenzweig, and S. Salman, “Size of red blood corpuscles and their nucleus in fifty North American birds,” Auk 54(4), 516–519 (1937).
[Crossref]

Baumal, C. R.

T. E. de Carlo, M. A. Bonini Filho, A. T. Chin, M. Adhi, D. Ferrara, C. R. Baumal, A. J. Witkin, E. Reichel, J. S. Duker, and N. K. Waheed, “Spectral-domain optical coherence tomography angiography of choroidal neovascularization,” Ophthalmology 122(6), 1228–1238 (2015).
[Crossref] [PubMed]

Baumann, B.

M. Salas, M. Augustin, L. Ginner, A. Kumar, B. Baumann, R. Leitgeb, W. Drexler, S. Prager, J. Hafner, U. Schmidt-Erfurth, and M. Pircher, “Visualization of micro-capillaries using optical coherence tomography angiography with and without adaptive optics,” Biomed. Opt. Express 8(1), 207–222 (2017).
[Crossref] [PubMed]

B. Baumann, J. Schirmer, S. Rauscher, S. Fialová, M. Glösmann, M. Augustin, M. Pircher, M. Gröger, and C. K. Hitzenberger, “Melanin Pigmentation in Rat Eyes: In Vivo Imaging by Polarization-Sensitive Optical Coherence Tomography and Comparison to Histology,” Invest. Ophthalmol. Vis. Sci. 56(12), 7462–7472 (2015).
[Crossref] [PubMed]

J. Liu, I. Grulkowski, M. Kraus, B. Potsaid, C. D Lu, B. Baumann, J. Duker, J. Hornegger, and J. G Fujimoto, “In vivo imaging of the rodent eye with swept source/Fourier domain OCT,” Biomed. Opt. Express 4, 351–363 (2013).

B. Baumann, W. Choi, B. Potsaid, D. Huang, J. S. Duker, and J. G. Fujimoto, “Swept source/Fourier domain polarization sensitive optical coherence tomography with a passive polarization delay unit,” Opt. Express 20(9), 10229–10241 (2012).
[Crossref] [PubMed]

B. Baumann, S. O. Baumann, T. Konegger, M. Pircher, E. Götzinger, F. Schlanitz, C. Schütze, H. Sattmann, M. Litschauer, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Polarization sensitive optical coherence tomography of melanin provides intrinsic contrast based on depolarization,” Biomed. Opt. Express 3(7), 1670–1683 (2012).
[Crossref] [PubMed]

E. Götzinger, M. Pircher, W. Geitzenauer, C. Ahlers, B. Baumann, S. Michels, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Retinal pigment epithelium segmentation by polarization sensitive optical coherence tomography,” Opt. Express 16(21), 16410–16422 (2008).
[Crossref] [PubMed]

Baumann, S. O.

Bax, N. M.

R. A. C. van Huet, N. M. Bax, S. C. Westeneng-Van Haaften, M. Muhamad, M. N. Zonneveld-Vrieling, L. H. Hoefsloot, F. P. M. Cremers, C. J. F. Boon, B. J. Klevering, and C. B. Hoyng, “Foveal Sparing in Stargardt Disease,” Invest. Ophthalmol. Vis. Sci. 55(11), 7467–7478 (2014).
[Crossref] [PubMed]

Bennett, P. M.

C. M. Hawkey, P. M. Bennett, S. C. Gascoyne, M. G. Hart, and J. K. Kirkwood, “Erythrocyte size, number and haemoglobin content in vertebrates,” Br. J. Haematol. 77(3), 392–397 (1991).
[Crossref] [PubMed]

Bernucci, M.

C. Leahy, H. Radhakrishnan, M. Bernucci, and V. J. Srinivasan, “Imaging and graphing of cortical vasculature using dynamically focused optical coherence microscopy angiography,” J. Biomed. Opt. 21(2), 020502 (2016).
[Crossref] [PubMed]

Bhavsar, K. V.

K. V. Bhavsar, L. Branchini, H. Shah, C. V. Regatieri, and J. S. Duker, “Choroidal Thickness in Retinal Pigment Epithelial Tear as Measured by Spectral Domain Optical Coherence Tomography,” Retina 34(1), 63–68 (2014).
[Crossref] [PubMed]

Bilonick, R. A.

L. C. Ho, B. Wang, I. P. Conner, Y. van der Merwe, R. A. Bilonick, S.-G. Kim, E. X. Wu, I. A. Sigal, G. Wollstein, J. S. Schuman, and K. C. Chan, “In Vivo Evaluation of White Matter Integrity and Anterograde Transport in Visual System After Excitotoxic Retinal Injury With Multimodal MRI and OCT,” Invest. Ophthalmol. Vis. Sci. 56(6), 3788–3800 (2015).
[Crossref] [PubMed]

Bonini Filho, M. A.

T. E. de Carlo, M. A. Bonini Filho, A. T. Chin, M. Adhi, D. Ferrara, C. R. Baumal, A. J. Witkin, E. Reichel, J. S. Duker, and N. K. Waheed, “Spectral-domain optical coherence tomography angiography of choroidal neovascularization,” Ophthalmology 122(6), 1228–1238 (2015).
[Crossref] [PubMed]

Boon, C. J. F.

R. A. C. van Huet, N. M. Bax, S. C. Westeneng-Van Haaften, M. Muhamad, M. N. Zonneveld-Vrieling, L. H. Hoefsloot, F. P. M. Cremers, C. J. F. Boon, B. J. Klevering, and C. B. Hoyng, “Foveal Sparing in Stargardt Disease,” Invest. Ophthalmol. Vis. Sci. 55(11), 7467–7478 (2014).
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Figures (11)

Fig. 1
Fig. 1 Optical properties, size, and shape of Intralipid particles are distinct from those of RBCs. A) Blood (RBC suspension) scattering phase function (red, Gegenbauer-Kernel, g = 0.95, α = 0.49) versus Intralipid scattering phase function (green, Henyey-Greenstein, g = 0.35), showing that blood has a significantly higher anisotropy. Forward scattering corresponds to 0° and backscattering corresponds to 180°. Note that phase functions are based on approximate anisotropy (g) values at 1300 nm [40, 52]. (B) Asymmetric RBCs orient themselves due to shear flow in the vessel lumen, with their flat faces pointing outwards, where θ is the angle incident light makes with the RBC normal vector. (C) By comparison, Intralipid particles are smaller than RBCs and more spherically symmetric, with no orientation per se. (D) Similarly, in diving or ascending vessels, RBCs are more likely oriented away from the incident light than RBCs in perpendicular capillaries (i.e. capillaries in the en face plane). Note, that although RBCs in capillary high shear flow may deform [54–56] from their typical biconcave disk shape, they still retain the orientation shown. (E) By comparison, Intralipid particles lack an intrinsic orientation.
Fig. 2
Fig. 2 (A) Schematic of ophthalmoscope based on modifying a Thorlabs TELESTO-II OCT system. In the sample arm, optics were added to demagnify the beam to 1.1 mm, and in the reference arm, dispersion-matched optics were added on a translation stage (double sided arrow) with a mirror. (B) Schematic of optical components inside TELESTO-II chassis. (C) Thorlabs source and spectrometer that fiber couples to TELESTO-II chassis (B). (D) Optical ray trace through a 3D rendering of the ophthalmoscope, showing a 53° angular field-of-view. (E) Photo of ophthalmoscope. L1: feff = 100 mm achromatic doublet pair, L2: feff = 25 mm achromatic doublet pair, S: sample arm, R: reference arm, GM: galvanometer mirror, BS: beam splitter, LSC: line-scan camera, DG: diffraction grating, SLD: superluminescent diode, FL: focusing lens. Solid black lines indicate optical fibers, while red lines indicate free-space infrared paths.
Fig. 3
Fig. 3 (A) Angiogram of the posterior pole of a pigmented rat, showing ROIs chosen for analysis: retinal and choroidal vessel lumens (red and green), retinal and choroidal vascular projections (yellow and orange), and “non-tails” in the inner retina and sclera (blue and purple). (B-C) Areas of retinal and choroidal lumens selected for enhancement factor calculations in unpigmented (SD) and pigmented (LE) animals. (D) An example mean signal time course, with baseline, bolus passage, and recirculation before a steady state is reached. Error bars indicate standard errors.
Fig. 4
Fig. 4 Pigmentation affects the appearance of “projection” artifacts of choroidal vessels. Sprague-Dawley (SD) and Long Evans (LE) OCT intensity and angiogram images (first column), along with zooms of choroid (Ch) and sclera (Sc) (second column), are shown. (A,B,E,F) Projections of choroidal vessels in a Sprague-Dawley rat are visible but not prominent in scleral regions. (C,D,G,H) Projections of choroidal vessels in a Long Evans rat are much more prominent in scleral regions. Projections are always more prominent in angiograms (B,F,D,H) than intensity images (A,C,E,G). Images are on a logarithmic scale (color bars in log units).
Fig. 5
Fig. 5 (A) Baseline OCT angiogram, showing RBC backscattering in the posterior pole of an unpigmented Sprague-Dawley rat. (B) Tracer signal during bolus passage. (C) Color overlay of (A) and (B), where red represents RBC signal, green represents tracer signal, and yellow includes both. Regions with large enhancement factors [Eq. (1)] are green, while regions with small enhancement factors are red. (D) The long posterior ciliary vessels seen within the sclera also demonstrate a prominent hourglass pattern. (E) Zoom of the inner retinal vasculature shows that vertical capillaries and retinal vessel sides are greener (tracer signal weighted), horizontal capillaries and retinal vessel tops are more yellow and red, and retinal vessel tails are purely red (RBC signal weighted).
Fig. 6
Fig. 6 Enhanced visualization of vascular networks in the retina and choroid was achieved by Intralipid contrast injection, and further improved by the Frangi filter. (A,D,G,J) Pre-contrast, (B,E,H,K) post-contrast, and Frangi filter enhanced (C,F,I,L) retinal and choroidal angiograms of unpigmented Sprague-Dawley (SD) and pigmented Long Evans (LE) rats are shown. Images are on a linear scale (color bars in linear units).
Fig. 7
Fig. 7 Visualization of the dense microvascular networks of the choriocapillaris of an unpigmented rat was achieved with Intralipid contrast. (A) Color-coded en face image of vasculature underlying the RPE (inset: depth ranges for green and red channels). (B-C) Image formed by selecting depths corresponding to the choriocapillaris. (D,E,F) A three-dimensional Hessian-based Frangi filter was applied to aid in visualizing the delicate and intricate choriocapillaris network.
Fig. 8
Fig. 8 Angiograms of the posterior pole in a Sprague-Dawley and a Long Evans rat at baseline (A,D,G,J), during bolus passage (B,E,H,K), and at steady state (C,F,I,L) are shown. At baseline, a Sprague-Dawley choroidal vessel lumen (G,H,I) and a Long Evans retinal vessel lumen (J,K,L) show an hourglass shape, which disappears after the introduction of Intralipid tracer into vasculature. Images are on a linear scale.
Fig. 9
Fig. 9 Enhancement factors [Eq. (1)] for retinal and choroidal vessels and tails in individual Sprague-Dawley (SD, n = 4) and Long Evans (LE, n = 3) rats, and averages for each strain. Similar trends in retinal and choroidal vessel enhancement factors were observed in all rats. Since experimental data were approximately Gaussian (not shown), parametric statistical tests were used. Colored horizontal brackets indicate statistically significant paired t-tests between vessels and tails for the retina (red) and the choroid (green). Black horizontal brackets indicate statistically significant unpaired t-tests between retinal and choroidal vessels: p < 0.05 (*) and p < 0.01 (**). Error bars indicate standard errors.
Fig. 10
Fig. 10 Enhancement factors [Eq. (1)] for retinal and choroidal tails and non-tails in individual Sprague-Dawley (SD, n = 4) and Long Evans (LE, n = 3) rats, and averages for each strain. No consistent trends in retinal and choroidal tail and non-tail enhancement factors were observed across rats. Asterisks indicate statistically significant t-tests for each measurement group: p < 0.05 (*) and p < 0.01 (**). Error bars indicate standard errors.
Fig. 11
Fig. 11 Quantification of relative signal enhancement in different regions of the hourglass pattern. (A) Red dashed ROIs indicate the sides of the vessel lumen, while the white dashed ROI indicates the top of the lumen. Both red dashed ROIs provide a single sides signal for each vessel. (B,C) The fractional change [Eq. (2)] of the sides-to-top signal ratio is shown for each vessel type (retina and choroid), with vessels pooled across all rats of the same strain: Sprague-Dawley (SD) or Long Evans (LE). Among retinal vessels, only superficial (vitreal) vessels were included in this analysis. Horizontal brackets indicate statistically significant unpaired t-tests between retinal and choroidal lumens, while asterisks directly above bars indicate t-tests for individual groups: p < 0.05 (*) and p < 0.01 (**). Error bars indicate standard errors.

Tables (1)

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Table 1 ROI number for enhancement factor measurements (Fig. 3)

Equations (2)

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enhancement factor = tracer angiogram signal baseline angiogram signal
fractional change = enhanced sides-to-top ratio baseline sides-to-top ratio -1 = sides enhancement factor + 1 top enhancement factor + 1 -1

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