Abstract

Retinal hemodynamics is important for early diagnosis and precise monitoring in retinal vascular diseases. We propose a novel method for measuring absolute retinal blood flow in vivo using the combined techniques of optical coherence tomography (OCT) angiography and Doppler OCT. Doppler values can be corrected by Doppler angles extracted from OCT angiography images. A three-dimensional (3D) segmentation algorithm based on dynamic programming was developed to extract the 3D boundaries of optic disc vessels, and Doppler angles were calculated from 3D vessel geometry. The accuracy of blood flow from the Doppler OCT was validated using a flow phantom. The feasibility of the method was tested on a subject in vivo. The pulsatile retinal blood flow and the parameters for retinal hemodynamics were successfully obtained.

© 2016 Optical Society of America

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References

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2015 (4)

V. K. Katsi, M. E. Marketou, D. A. Vrachatis, A. J. Manolis, P. Nihoyannopoulos, D. Tousoulis, P. E. Vardas, and I. Kallikazaros, “Essential hypertension in the pathogenesis of age-related macular degeneration: a review of the current evidence,” J. Hypertens. 33(12), 2382–2388 (2015).
[Crossref] [PubMed]

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[Crossref] [PubMed]

S. Huang, Z. Piao, J. Zhu, F. Lu, and Z. Chen, “In vivo microvascular network imaging of the human retina combined with an automatic three-dimensional segmentation method,” J. Biomed. Opt. 20(7), 076003 (2015).
[Crossref] [PubMed]

A. Nagiel, S. R. Sadda, and D. Sarraf, “A promising future for optical coherence tomography angiography,” JAMA Ophthalmol. 133(6), 629–630 (2015).
[Crossref] [PubMed]

2014 (1)

X. Liu, M. Shen, S. Huang, L. Leng, D. Zhu, and F. Lu, “Repeatability and Reproducibility of Eight Macular Intra-Retinal Layer Thicknesses Determined by an Automated Segmentation Algorithm Using Two SD-OCT Instruments,” PLoS One 9(2), e87996 (2014).
[Crossref] [PubMed]

2013 (3)

C. Dai, X. Liu, H. F. Zhang, C. A. Puliafito, and S. Jiao, “Absolute retinal Blood Flow Measurement With a Dual-Beam Doppler Optical Coherence Tomography,” Invest. Ophthalmol. Vis. Sci. 54(13), 7998–8003 (2013).
[Crossref] [PubMed]

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. H. Luk, A. Mariampillai, and V. X. D. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
[Crossref] [PubMed]

C. Blatter, S. Coquoz, B. Grajciar, A. S. G. Singh, M. Bonesi, R. M. Werkmeister, L. Schmetterer, and R. A. Leitgeb, “Dove prism based rotating dual beam bidirectional Doppler OCT,” Biomed. Opt. Express 4(7), 1188–1203 (2013).
[Crossref] [PubMed]

2012 (4)

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express 20(4), 4710–4725 (2012).
[Crossref] [PubMed]

G. Liu, A. J. Lin, B. J. Tromberg, and Z. Chen, “A comparison of Doppler optical coherence tomography methods,” Biomed. Opt. Express 3(10), 2669–2680 (2012).
[Crossref] [PubMed]

D. Pascolini and S. P. Mariotti, “Global estimates of visual impairment: 2010,” Br. J. Ophthalmol. 96(5), 614–618 (2012).
[Crossref] [PubMed]

Y. Wang, H. Jiang, M. Shen, B. L. Lam, D. C. DeBuc, Y. Ye, M. Li, A. Tao, Y. Shao, and J. Wang, “Quantitative analysis of the intraretinal layers and optic nerve head using ultra-high resolution optical coherence tomography,” J. Biomed. Opt. 17(6), 066013 (2012).
[Crossref] [PubMed]

2011 (5)

2010 (2)

2008 (5)

2007 (4)

R. Michaely, A. H. Bachmann, M. L. Villiger, C. Blatter, T. Lasser, and R. A. Leitgeb, “Vectorial reconstruction of retinal blood flow in three dimensions measured with high resolution resonant Doppler Fourier domain optical coherence tomography,” J. Biomed. Opt. 12(4), 041213 (2007).
[Crossref] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12(4), 041215 (2007).
[Crossref] [PubMed]

R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, and A. Gruber, “Three dimensional optical angiography,” Opt. Express 15(7), 4083–4097 (2007).
[Crossref] [PubMed]

Y. Yasuno, Y. Hong, S. Makita, M. Yamanari, M. Akiba, M. Miura, and T. Yatagai, “In vivo high-contrast imaging of deep posterior eye by 1- um swept source optical coherence tomography and scattering optical coherence angiography,” Opt. Express 15(10), 6121–6139 (2007).
[Crossref] [PubMed]

2006 (1)

2004 (3)

N. Nassif, B. Cense, B. H. Park, S. H. Yun, T. C. Chen, B. E. Bouma, G. J. Tearney, and J. F. de Boer, “In vivo human retinal imaging by ultrahigh-speed spectral domain optical coherence tomography,” Opt. Lett. 29(5), 480–482 (2004).
[Crossref] [PubMed]

J. Bellner, B. Romner, P. Reinstrup, K.-A. Kristiansson, E. Ryding, and L. Brandt, “Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP),” Surg. Neurol. 62(1), 45–51 (2004).
[Crossref] [PubMed]

T. Gracner, “Ocular blood flow velocity determined by color Doppler imaging in diabetic retinopathy,” Ophthalmologica 218(4), 237–242 (2004).
[Crossref] [PubMed]

2003 (1)

J. Radermacher, M. Mengel, S. Ellis, S. Stuht, M. Hiss, A. Schwarz, U. Eisenberger, M. Burg, F. C. Luft, W. Gwinner, and H. Haller, “The renal arterial resistance index and renal allograft survival,” N. Engl. J. Med. 349(2), 115–124 (2003).
[Crossref] [PubMed]

2002 (1)

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J.-P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res. 21(4), 359–393 (2002).
[Crossref] [PubMed]

2001 (1)

H. S. Stone, M. T. Orchard, E. C. Chang, and S. A. Martucci, “A fast direct Fourier-based algorithm for subpixel registration of images,” IEEE Trans. Geosci. Remote Sens. 39(10), 2235–2243 (2001).
[Crossref]

2000 (2)

1997 (1)

1996 (1)

T. H. Williamson and A. Harris, “Color Doppler ultrasound imaging of the eye and orbit,” Surv. Ophthalmol. 40(4), 255–267 (1996).
[Crossref] [PubMed]

1993 (1)

S. P. Sutera and R. Skalak, “The history of Poiseuille’s law,” Annu. Rev. Fluid Mech. 25(1), 1–20 (1993).
[Crossref]

1988 (1)

Akiba, M.

An, L.

L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt. 16(10), 106013 (2011).
[Crossref] [PubMed]

Bachmann, A. H.

R. Michaely, A. H. Bachmann, M. L. Villiger, C. Blatter, T. Lasser, and R. A. Leitgeb, “Vectorial reconstruction of retinal blood flow in three dimensions measured with high resolution resonant Doppler Fourier domain optical coherence tomography,” J. Biomed. Opt. 12(4), 041213 (2007).
[Crossref] [PubMed]

Baumann, B.

Bellner, J.

J. Bellner, B. Romner, P. Reinstrup, K.-A. Kristiansson, E. Ryding, and L. Brandt, “Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP),” Surg. Neurol. 62(1), 45–51 (2004).
[Crossref] [PubMed]

Bernardes, R.

P. Guimarães, P. Rodrigues, D. Celorico, P. Serranho, and R. Bernardes, “Three-dimensional segmentation and reconstruction of the retinal vasculature from spectral-domain optical coherence tomography,” J. Biomed. Opt. 20(1), 016006 (2015).
[Crossref] [PubMed]

Blatter, C.

C. Blatter, S. Coquoz, B. Grajciar, A. S. G. Singh, M. Bonesi, R. M. Werkmeister, L. Schmetterer, and R. A. Leitgeb, “Dove prism based rotating dual beam bidirectional Doppler OCT,” Biomed. Opt. Express 4(7), 1188–1203 (2013).
[Crossref] [PubMed]

R. Michaely, A. H. Bachmann, M. L. Villiger, C. Blatter, T. Lasser, and R. A. Leitgeb, “Vectorial reconstruction of retinal blood flow in three dimensions measured with high resolution resonant Doppler Fourier domain optical coherence tomography,” J. Biomed. Opt. 12(4), 041213 (2007).
[Crossref] [PubMed]

Bonesi, M.

Bouma, B. E.

Bower, B. A.

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12(4), 041215 (2007).
[Crossref] [PubMed]

Brandt, L.

J. Bellner, B. Romner, P. Reinstrup, K.-A. Kristiansson, E. Ryding, and L. Brandt, “Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP),” Surg. Neurol. 62(1), 45–51 (2004).
[Crossref] [PubMed]

Burg, M.

J. Radermacher, M. Mengel, S. Ellis, S. Stuht, M. Hiss, A. Schwarz, U. Eisenberger, M. Burg, F. C. Luft, W. Gwinner, and H. Haller, “The renal arterial resistance index and renal allograft survival,” N. Engl. J. Med. 349(2), 115–124 (2003).
[Crossref] [PubMed]

Cable, A.

Cable, A. E.

Cadotte, D. W.

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. H. Luk, A. Mariampillai, and V. X. D. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
[Crossref] [PubMed]

Celorico, D.

P. Guimarães, P. Rodrigues, D. Celorico, P. Serranho, and R. Bernardes, “Three-dimensional segmentation and reconstruction of the retinal vasculature from spectral-domain optical coherence tomography,” J. Biomed. Opt. 20(1), 016006 (2015).
[Crossref] [PubMed]

Cense, B.

Chang, E. C.

H. S. Stone, M. T. Orchard, E. C. Chang, and S. A. Martucci, “A fast direct Fourier-based algorithm for subpixel registration of images,” IEEE Trans. Geosci. Remote Sens. 39(10), 2235–2243 (2001).
[Crossref]

Chen, T. C.

Chen, Z.

S. Huang, Z. Piao, J. Zhu, F. Lu, and Z. Chen, “In vivo microvascular network imaging of the human retina combined with an automatic three-dimensional segmentation method,” J. Biomed. Opt. 20(7), 076003 (2015).
[Crossref] [PubMed]

G. Liu, A. J. Lin, B. J. Tromberg, and Z. Chen, “A comparison of Doppler optical coherence tomography methods,” Biomed. Opt. Express 3(10), 2669–2680 (2012).
[Crossref] [PubMed]

G. Liu, L. Chou, W. Jia, W. Qi, B. Choi, and Z. Chen, “Intensity-based modified Doppler variance algorithm: application to phase instable and phase stable optical coherence tomography systems,” Opt. Express 19(12), 11429–11440 (2011).
[Crossref] [PubMed]

L. Yu and Z. Chen, “Doppler variance imaging for three-dimensional retina and choroid angiography,” J. Biomed. Opt. 15(1), 016029 (2010).
[Crossref] [PubMed]

B. Rao, L. Yu, H. K. Chiang, L. C. Zacharias, R. M. Kurtz, B. D. Kuppermann, and Z. Chen, “Imaging pulsatile retinal blood flow in human eye,” J. Biomed. Opt. 13(4), 040505 (2008).
[Crossref] [PubMed]

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25(2), 114–116 (2000).
[Crossref] [PubMed]

Z. Chen, T. E. Milner, D. Dave, and J. S. Nelson, “Optical Doppler tomographic imaging of fluid flow velocity in highly scattering media,” Opt. Lett. 22(1), 64–66 (1997).
[Crossref] [PubMed]

Chiang, H. K.

B. Rao, L. Yu, H. K. Chiang, L. C. Zacharias, R. M. Kurtz, B. D. Kuppermann, and Z. Chen, “Imaging pulsatile retinal blood flow in human eye,” J. Biomed. Opt. 13(4), 040505 (2008).
[Crossref] [PubMed]

Chiu, S. J.

Choi, B.

Chou, L.

Coquoz, S.

Costa, V. P.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J.-P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res. 21(4), 359–393 (2002).
[Crossref] [PubMed]

Dai, C.

C. Dai, X. Liu, H. F. Zhang, C. A. Puliafito, and S. Jiao, “Absolute retinal Blood Flow Measurement With a Dual-Beam Doppler Optical Coherence Tomography,” Invest. Ophthalmol. Vis. Sci. 54(13), 7998–8003 (2013).
[Crossref] [PubMed]

Dave, D.

Davé, D. P.

de Boer, J. F.

de Kinkelder, R.

R. de Kinkelder, J. Kalkman, D. J. Faber, O. Schraa, P. H. Kok, F. D. Verbraak, and T. G. van Leeuwen, “Heartbeat-induced axial motion artifacts in optical coherence tomography measurements of the retina,” Invest. Ophthalmol. Vis. Sci. 52(6), 3908–3913 (2011).
[Crossref] [PubMed]

DeBuc, D. C.

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Figures (8)

Fig. 1
Fig. 1 Flow diagram for three-dimensional segmentation of retinal blood vessels. ILM, inner limiting membrane; RPE, retinal pigment epithelium; 3D, three dimensional; 2D, two dimensional.
Fig. 2
Fig. 2 2D geometry structure extraction of retinal vessels. (a) Flow diagram of interactive 2D segmentation. (b) En face view of retinal vessels in the optic disc area. (c) The filtered image of retinal vessels in the optic disc area. (d) and (e) Illustration of segment results at the start and end points. (f) 2D geometric structure of the vessels.
Fig. 3
Fig. 3 Diagram of 3D boundary detection for a retinal vessel. (a, b) Estimate of vessel diameter. (c) Estimate of vessel depth. (d) Illustration of resample and “unfolding” of 3D data set for retinal vessel. (e) Cross-section view of boundary detection results. (f) 3D visualization of vessel morphology.
Fig. 4
Fig. 4 Validation of Doppler OCT. (a) OCT intensity image of the flow phantom at a Doppler angle of 77.4°. (b) Lateral projection of flow phantom at a Doppler angle of 77.4°. (c) Doppler OCT image corresponding to the intensity image in (a). (d) The blue line is the phase difference profile that is marked by the blue line in (c), and the red line is the result of parabolic fitting. (e) Comparison between pumped flow and detected flow with the fixed Doppler angle. (f) Validation of relationship between Doppler angle and phase difference with fixed pumped flow.
Fig. 5
Fig. 5 Registration between OCT angiography and Doppler OCT. The blue circular line indicates the circular scan position corresponding to the en face view of the OCT angiography image. The circular view of the Doppler image was merged with the angiography image. Eight major vessels were selected, and the locations of the measured vessels were indicated by short red lines. The boundaries of the measured vessels were also overlaid on the angiography image, and the green lines indicate the center of each vessel. The red color indicates arteries and blue color indicates veins.
Fig. 6
Fig. 6 OCT angiography and three-dimensional segmentation of retinal vessels on the optic disc. (a) En face view of the intensity image and the OCT angiography image. (b) Rendered 3D volume of OCT angiography. (c) 3D reconstruction of the selected vessels. The green lines indicate the center of each vessel. The red color indicates arteries and blue color indicates veins. (d) OCT angiography image overlayed with boundaries of the reconstructed vessels.
Fig. 7
Fig. 7 Comparison between OCT angiography and Doppler OCT. (a) Intensity image of optic disk area with circular scan. (b) OCT angiography image and (c) Doppler image in which two vessels required phase unwrapping (blue arrows). (d) Averaged shifted histogram of the A-scan marked by the blue line in (c). The black arrows indicate bulk phase shift and red arrows indicate phase noise of the in vivo retina.
Fig. 8
Fig. 8 Pulsatile flow of a retinal vessel. (a) Doppler OCT image for a circular scan of the optic disc. (b) Enlarged Doppler OCT image of the selected vessel marked by the blue rectangle in (a). (c) Pulsatile velocity profile of the selected vessel within a time span of ~6 s. Red profile, velocity before Doppler angle correction; blue profile, corresponding velocity after correction. Green dashed lines: top, peak systolic velocity (S); middle, average velocity (A), bottom, end diastolic velocity (D).

Tables (1)

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Table 1 Blood flow measurements of retinal vesselsa

Equations (6)

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σ 2 = 1 T 2 [ 1 m=1 M n=1 N1 ( | A n,m || A n+1,m | ) m=1 M n=1 N1 1 2 ( | A n,m | 2 + | A n+1,m | 2 ) ]
Δϕ=arctan{ j=1 J m=1 M [ Im( A j+1,m )Re( A j,m )Im( A j,m )Re( A j+1,m ) ] j=1 J m=1 M [ Re( A j,m )Re( A j+1,m )+Im( A j,m )Im( A j+1,m ) ] }
v z = λ c Δϕ 4πnΔT
v= v z cosα
Φ= v c 2 π D 2 4 == D 2 λ c Δ ϕ c 16 2 n p ΔTcosα
σ avg = σ N

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