Abstract

Imaging choriocapillaris (CC) is a long-term challenge for commercial OCT angiography (OCTA) systems due to limited transverse resolution. Effects of transverse resolution on the visualization of a CC microvascular network are explored and demonstrated in this paper. We use three probe beams with sizes of ~1.12 mm, ~2.51 mm and ~3.50 mm at the pupil plane, which deliver an estimated transverse resolution at the retina of 17.5 µm, 8.8 µm and 7.0 µm, respectively, to investigate the ability of OCTA to resolve the CC capillary vessels. The complex optical microangiography algorithm is applied to extract blood flow in the CC slab. Mean retinal pigment epithelium (RPE) to CC (RPE-CC) distance, mean CC inter-vascular spacing and the magnitude in the radially-averaged power spectrum are quantified. We demonstrate that a clearer CC lobular capillary network is resolved in the angiograms provided by a larger beam size. The image contrast of the CC angiogram with a large beam size of 3.50 mm is 114% higher than that with a small beam size of 1.12 mm. While the measurements of the mean RPE-CC distance and CC inter-vascular spacing are almost consistent regardless of the beam sizes, they are more reliable and stable with the larger beam size of 3.50 mm. We conclude that the beam size is a key parameter for CC angiography if the purpose of the investigation is to visualize the individual CC capillaries.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2019 (1)

2018 (5)

R. Maddipatla, J. Cervantes, Y. Otani, and B. Cense, “Retinal imaging with optical coherence tomography and low-loss adaptive optics using a 2.8-mm beam size,” J. Biophotonics 2018, e201800192 (2018).
[PubMed]

Q. Zhang, Y. Shi, H. Zhou, G. Gregori, Z. Chu, F. Zheng, E. H. Motulsky, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “Accurate estimation of choriocapillaris flow deficits beyond normal intercapillary spacing with swept source OCT angiography,” Quant. Imaging Med. Surg. 8(7), 658–666 (2018).
[Crossref] [PubMed]

C. Rochepeau, L. Kodjikian, M.-A. Garcia, C. Coulon, C. Burillon, P. Denis, B. Delaunay, and T. Mathis, “Optical Coherence Tomography Angiography Quantitative Assessment of Choriocapillaris Blood Flow in Central Serous Chorioretinopathy,” Am. J. Ophthalmol. 194, 26–34 (2018).
[Crossref] [PubMed]

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C.-L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A Novel Strategy for Quantifying Choriocapillaris Flow Voids Using Swept-Source OCT Angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Z. Chu, H. Zhou, Y. Cheng, Q. Zhang, and R. K. Wang, “Improving visualization and quantitative assessment of choriocapillaris with swept source OCTA through registration and averaging applicable to clinical systems,” Sci. Rep. 8(1), 16826 (2018).
[Crossref] [PubMed]

2017 (11)

M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
[Crossref] [PubMed]

Y. Teng, M. Yu, Y. Wang, X. Liu, Q. You, and W. Liu, “OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery,” Graefes Arch. Clin. Exp. Ophthalmol. 255(5), 893–902 (2017).
[Crossref] [PubMed]

K. Kurokawa, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography angiography for morphometric analysis of choriocapillaris,” Biomed. Opt. Express 8(3), 1803–1822 (2017).
[Crossref] [PubMed]

C.-L. Chen and R. K. Wang, “Optical coherence tomography based angiography [Invited],” Biomed. Opt. Express 8(2), 1056–1082 (2017).
[Crossref] [PubMed]

P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

A. Carnevali, R. Sacconi, E. Corbelli, L. Tomasso, L. Querques, G. Zerbini, V. Scorcia, F. Bandello, and G. Querques, “Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy,” Acta Diabetol. 54(7), 695–702 (2017).
[Crossref] [PubMed]

J. Polans, D. Cunefare, E. Cole, B. Keller, P. S. Mettu, S. W. Cousins, M. J. Allingham, J. A. Izatt, and S. Farsiu, “Enhanced visualization of peripheral retinal vasculature with wavefront sensorless adaptive optics optical coherence tomography angiography in diabetic patients,” Opt. Lett. 42(1), 17–20 (2017).
[Crossref] [PubMed]

J. Polans, B. Keller, O. M. Carrasco-Zevallos, F. LaRocca, E. Cole, H. E. Whitson, E. M. Lad, S. Farsiu, and J. A. Izatt, “Wide-field retinal optical coherence tomography with wavefront sensorless adaptive optics for enhanced imaging of targeted regions,” Biomed. Opt. Express 8(1), 16–37 (2017).
[Crossref] [PubMed]

Z. Chu, C.-L. Chen, Q. Zhang, K. Pepple, M. Durbin, G. Gregori, and R. K. Wang, “Complex signal-based optical coherence tomography angiography enables in vivo visualization of choriocapillaris in human choroid,” J. Biomed. Opt. 22(12), 1–10 (2017).
[Crossref] [PubMed]

M. Pircher and R. J. Zawadzki, “Review of adaptive optics OCT (AO-OCT): principles and applications for retinal imaging,” Biomed. Opt. Express 8(5), 2536–2562 (2017).
[Crossref] [PubMed]

2016 (3)

M. Lane, E. M. Moult, E. A. Novais, R. N. Louzada, E. D. Cole, B. Lee, L. Husvogt, P. A. Keane, A. K. Denniston, A. J. Witkin, C. R. Baumal, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Visualizing the choriocapillaris under drusen: comparing 1050-nm swept-source versus 840-nm spectral-domain optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT585 (2016).
[Crossref] [PubMed]

Y. Kuroda, S. Ooto, K. Yamashiro, A. Oishi, H. Nakanishi, H. Tamura, N. Ueda-Arakawa, and N. Yoshimura, “Increased choroidal vascularity in central serous chorioretinopathy quantified using swept-source optical coherence tomography,” Am. J. Ophthalmol. 169, 199–207 (2016).
[Crossref] [PubMed]

N. Jain, Y. Jia, S. S. Gao, X. Zhang, R. G. Weleber, D. Huang, and M. E. Pennesi, “Optical coherence tomography angiography in choroideremia: correlating choriocapillaris loss with overlying degeneration,” JAMA Ophthalmol. 134(6), 697–702 (2016).
[Crossref] [PubMed]

2015 (1)

A. Zhang, Q. Zhang, C.-L. Chen, and R. K. Wang, “Methods and algorithms for optical coherence tomography-based angiography: a review and comparison,” J. Biomed. Opt. 20(10), 100901 (2015).
[Crossref] [PubMed]

2014 (2)

A. Biesemeier, T. Taubitz, S. Julien, E. Yoeruek, and U. Schraermeyer, “Choriocapillaris breakdown precedes retinal degeneration in age-related macular degeneration,” Neurobiol. Aging 35(11), 2562–2573 (2014).
[Crossref] [PubMed]

X. Yin, J. R. Chao, and R. K. Wang, “User-guided segmentation for volumetric retinal optical coherence tomography images,” J. Biomed. Opt. 19(8), 086020 (2014).
[Crossref] [PubMed]

2013 (2)

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]

2010 (2)

L. An, H. M. Subhush, D. J. Wilson, and R. K. Wang, “High-resolution wide-field imaging of retinal and choroidal blood perfusion with optical microangiography,” J. Biomed. Opt. 15(2), 026011 (2010).
[Crossref] [PubMed]

R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett. 35(9), 1467–1469 (2010).
[Crossref] [PubMed]

2008 (1)

2005 (1)

P. H. Tomlins and R. Wang, “Theory, developments and applications of optical coherence tomography,” J. Phys. D Appl. Phys. 38(15), 2519–2535 (2005).
[Crossref]

2001 (1)

D. J. Moore and G. M. Clover, “The effect of age on the macromolecular permeability of human Bruch’s membrane,” Invest. Ophthalmol. Vis. Sci. 42(12), 2970–2975 (2001).
[PubMed]

2000 (1)

C. W. Spraul, G. E. Lang, H. E. Grossniklaus, and G. K. Lang, “Morphometric changes in the choriocapillaris and choroid in eyes with advanced glaucoma damage,” Ophthalmologe 97(10), 663–668 (2000).
[Crossref] [PubMed]

1999 (1)

C. W. Spraul, G. E. Lang, H. E. Grossniklaus, and G. K. Lang, “Histologic and morphometric analysis of the choroid, Bruch’s membrane, and retinal pigment epithelium in postmortem eyes with age-related macular degeneration and histologic examination of surgically excised choroidal neovascular membranes,” Surv. Ophthalmol. 44(Suppl 1), S10–S32 (1999).
[Crossref] [PubMed]

1994 (3)

H. R. Zhang, “Scanning electron-microscopic study of corrosion casts on retinal and choroidal angioarchitecture in man and animals,” Prog. Retin. Eye Res. 13(1), 243–270 (1994).
[Crossref]

D. S. McLeod and G. A. Lutty, “High-resolution histologic analysis of the human choroidal vasculature,” Invest. Ophthalmol. Vis. Sci. 35(11), 3799–3811 (1994).
[PubMed]

A. W. Fryczkowski, “Anatomical and functional choroidal lobuli,” Int. Ophthalmol. 18(3), 131–141 (1994).
[Crossref] [PubMed]

Allingham, M. J.

Al-Sheikh, M.

M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
[Crossref] [PubMed]

An, L.

Azimipour, M.

Bandello, F.

A. Carnevali, R. Sacconi, E. Corbelli, L. Tomasso, L. Querques, G. Zerbini, V. Scorcia, F. Bandello, and G. Querques, “Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy,” Acta Diabetol. 54(7), 695–702 (2017).
[Crossref] [PubMed]

Baumal, C. R.

M. Lane, E. M. Moult, E. A. Novais, R. N. Louzada, E. D. Cole, B. Lee, L. Husvogt, P. A. Keane, A. K. Denniston, A. J. Witkin, C. R. Baumal, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Visualizing the choriocapillaris under drusen: comparing 1050-nm swept-source versus 840-nm spectral-domain optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT585 (2016).
[Crossref] [PubMed]

Biesemeier, A.

A. Biesemeier, T. Taubitz, S. Julien, E. Yoeruek, and U. Schraermeyer, “Choriocapillaris breakdown precedes retinal degeneration in age-related macular degeneration,” Neurobiol. Aging 35(11), 2562–2573 (2014).
[Crossref] [PubMed]

Burillon, C.

C. Rochepeau, L. Kodjikian, M.-A. Garcia, C. Coulon, C. Burillon, P. Denis, B. Delaunay, and T. Mathis, “Optical Coherence Tomography Angiography Quantitative Assessment of Choriocapillaris Blood Flow in Central Serous Chorioretinopathy,” Am. J. Ophthalmol. 194, 26–34 (2018).
[Crossref] [PubMed]

Cable, A. E.

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]

Carnevali, A.

A. Carnevali, R. Sacconi, E. Corbelli, L. Tomasso, L. Querques, G. Zerbini, V. Scorcia, F. Bandello, and G. Querques, “Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy,” Acta Diabetol. 54(7), 695–702 (2017).
[Crossref] [PubMed]

Carrasco-Zevallos, O. M.

Cense, B.

R. Maddipatla, J. Cervantes, Y. Otani, and B. Cense, “Retinal imaging with optical coherence tomography and low-loss adaptive optics using a 2.8-mm beam size,” J. Biophotonics 2018, e201800192 (2018).
[PubMed]

Cervantes, J.

R. Maddipatla, J. Cervantes, Y. Otani, and B. Cense, “Retinal imaging with optical coherence tomography and low-loss adaptive optics using a 2.8-mm beam size,” J. Biophotonics 2018, e201800192 (2018).
[PubMed]

Chai, H.

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Z. Chu, H. Zhou, Y. Cheng, Q. Zhang, and R. K. Wang, “Improving visualization and quantitative assessment of choriocapillaris with swept source OCTA through registration and averaging applicable to clinical systems,” Sci. Rep. 8(1), 16826 (2018).
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R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett. 35(9), 1467–1469 (2010).
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Y. Teng, M. Yu, Y. Wang, X. Liu, Q. You, and W. Liu, “OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery,” Graefes Arch. Clin. Exp. Ophthalmol. 255(5), 893–902 (2017).
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N. Jain, Y. Jia, S. S. Gao, X. Zhang, R. G. Weleber, D. Huang, and M. E. Pennesi, “Optical coherence tomography angiography in choroideremia: correlating choriocapillaris loss with overlying degeneration,” JAMA Ophthalmol. 134(6), 697–702 (2016).
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Wilson, D. J.

L. An, H. M. Subhush, D. J. Wilson, and R. K. Wang, “High-resolution wide-field imaging of retinal and choroidal blood perfusion with optical microangiography,” J. Biomed. Opt. 15(2), 026011 (2010).
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Y. Kuroda, S. Ooto, K. Yamashiro, A. Oishi, H. Nakanishi, H. Tamura, N. Ueda-Arakawa, and N. Yoshimura, “Increased choroidal vascularity in central serous chorioretinopathy quantified using swept-source optical coherence tomography,” Am. J. Ophthalmol. 169, 199–207 (2016).
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X. Yin, J. R. Chao, and R. K. Wang, “User-guided segmentation for volumetric retinal optical coherence tomography images,” J. Biomed. Opt. 19(8), 086020 (2014).
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A. Biesemeier, T. Taubitz, S. Julien, E. Yoeruek, and U. Schraermeyer, “Choriocapillaris breakdown precedes retinal degeneration in age-related macular degeneration,” Neurobiol. Aging 35(11), 2562–2573 (2014).
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Yoshimura, N.

Y. Kuroda, S. Ooto, K. Yamashiro, A. Oishi, H. Nakanishi, H. Tamura, N. Ueda-Arakawa, and N. Yoshimura, “Increased choroidal vascularity in central serous chorioretinopathy quantified using swept-source optical coherence tomography,” Am. J. Ophthalmol. 169, 199–207 (2016).
[Crossref] [PubMed]

You, Q.

Y. Teng, M. Yu, Y. Wang, X. Liu, Q. You, and W. Liu, “OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery,” Graefes Arch. Clin. Exp. Ophthalmol. 255(5), 893–902 (2017).
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Yu, M.

Y. Teng, M. Yu, Y. Wang, X. Liu, Q. You, and W. Liu, “OCT angiography quantifying choriocapillary circulation in idiopathic macular hole before and after surgery,” Graefes Arch. Clin. Exp. Ophthalmol. 255(5), 893–902 (2017).
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Zawadzki, R. J.

Zerbini, G.

A. Carnevali, R. Sacconi, E. Corbelli, L. Tomasso, L. Querques, G. Zerbini, V. Scorcia, F. Bandello, and G. Querques, “Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy,” Acta Diabetol. 54(7), 695–702 (2017).
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Zhang, A.

A. Zhang, Q. Zhang, C.-L. Chen, and R. K. Wang, “Methods and algorithms for optical coherence tomography-based angiography: a review and comparison,” J. Biomed. Opt. 20(10), 100901 (2015).
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Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C.-L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A Novel Strategy for Quantifying Choriocapillaris Flow Voids Using Swept-Source OCT Angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Z. Chu, H. Zhou, Y. Cheng, Q. Zhang, and R. K. Wang, “Improving visualization and quantitative assessment of choriocapillaris with swept source OCTA through registration and averaging applicable to clinical systems,” Sci. Rep. 8(1), 16826 (2018).
[Crossref] [PubMed]

Q. Zhang, Y. Shi, H. Zhou, G. Gregori, Z. Chu, F. Zheng, E. H. Motulsky, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “Accurate estimation of choriocapillaris flow deficits beyond normal intercapillary spacing with swept source OCT angiography,” Quant. Imaging Med. Surg. 8(7), 658–666 (2018).
[Crossref] [PubMed]

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Figures (5)

Fig. 1
Fig. 1 Experimental arrangements to demonstrate the effect of the probe beam size on the ability to resolve the capillary vessels in the CC layer. (A) Experimental setup for CC imaging using SS-OCT system. There are three different configurations for the components denoted by star (*) in the sample arm for delivering a beam with various diameters into the eye. DCM: dichroic mirror. (B) Experimental setup for system transverse resolution measurement. A pair of convex lenses (0.5-inch diameter, 16.5 mm equivalent focal length) was used as a phantom eye to focus the beam onto USAF 1951 resolution target. System transverse resolution was then evaluated on the resulting images of the resolution target pattern. (C) Measured two-dimensional beam intensity maps (first row, gray scale) and their corresponding radially-averaged profiles (second row, line charts) of three different sample arm configurations.
Fig. 2
Fig. 2 OCTA image resulted from large probe beam size of 3.50 mm can resolve the individual capillary vessels in the CC at the posterior pole, providing an opportunity to quantify the CC integrity. (A) Cross-sectional OCT and OCTA images extracted from the volumetric data sets acquired at fovea in subject 3. (B) Normalized mean OCT and OCTA depth profiles of cross-sectional images in (A). The three most prominent peaks in the structure intensity profile (black) are inner/outer segment junction (IS/OS), cone outer segments tips (COST) and RPE. (C) En-face retina (left) and CC (right) OCTA images (FOV: ~0.6 × 0.8 mm2). Yellow dashed frame indicates square area external to the vertexes of the FAZ for further comparison and morphology analysis. (D) cropped en-face CC OCTA image at FAZ (FOV: ~0.5 × 0.5 mm2) and its corresponding 2D power spectrum. (E) Left: normalized radially-averaged power spectrum of en-face CC OCTA image at FAZ. The offset was fitted into power function (red dashed line). Right: Power spectrum of en-face CC OCTA image after offset removal and its corresponding Gaussian fitting. All scale bars: 100 µm.
Fig. 3
Fig. 3 The system transverse resolution was tested by the use of a standard USAF resolution target. (A-C) Resultant en-face images of the resolution target imaged with various beam diameters: A) 1.12 mm; B) 2.51 mm; and C) 3.50 mm, respectively. Small sub-frames on the right show the zoomed-in views for patterns of group 6 and 7. The small yellow arrows denote the minimum visually resolvable pattern for each beam size. (D) Normalized vertical (up) and horizontal (down) intensity profiles of USAF resolution target patterns (group 5) imaged by the beam diameter of 1.12 mm. (E) Normalized vertical (up) and horizontal (down) intensity profiles of USAF resolution target patterns (group 6) imaged by the beam diameter of 2.51 mm. (F) Normalized vertical (up) and horizontal (down) intensity profiles of USAF resolution target patterns (group 7) imaged by the beam diameter of 3.50 mm.
Fig. 4
Fig. 4 The clarity of the OCTA vascular image is affected by the incident beam size. (A) En-face retina OCTA images at FAZ region imaged by the beam diameters of 1.12 mm, 2.51 mm and 3.50 mm (from left to right), respectively. (B) Corresponding en-face CC OCTA images. (C) 2D power spectrums of en-face CC OCTA images for all three beam diameters. (D) Offset-removed radially-averaged power spectrums of CC (solid line, thin, blue for the beam diameter of 1.12 mm, red for the beam diameter of 2.51 mm and black for the beam diameter of 3.50 mm) and their corresponding Gaussian fitting curves (solid line, bold).
Fig. 5
Fig. 5 The choriocapillaris lobular network under the central fovea region can be resolved by a commercial grade SS-OCT system with an incident probe beam diameter of ~3.50 mm at the pupil plane. (A) En-face OCTA images of the CC slab at the posterior pole region acquired from 4 normal subjects. (B) Measured mean RPE-CC distance (mean ± std) of the 4 subjects. (C) Measured mean CC inter-vascular spacing (mean ± std) of the subjects.

Tables (2)

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Table 1 Detailed parameters for each sample arm configuration

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Table 2 Details of the 4 healthy subjects

Equations (3)

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Δz= 2ln2 λ c 2 πΔλ
Δx= 1.22 λ c 2N A obj = 1.22 λ c f eye D
DO F Z OCT =2 Z R = 2πΔ x 2 λ c

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