Abstract

Laser Doppler holography was introduced as a full-field imaging technique to measure blood flow in the retina and choroid with an as yet unrivaled temporal resolution. We here investigate separating the different contributions to the power Doppler signal in order to isolate the flow waveforms of vessels in the posterior pole of the human eye. Distinct flow behaviors are found in retinal arteries and veins with seemingly interrelated waveforms. We demonstrate a full field mapping of the local resistivity index, and the possibility to perform unambiguous identification of retinal arteries and veins on the basis of their systolodiastolic variations. Finally we investigate the arterial flow waveforms in the retina and choroid and find synchronous and similar waveforms, although with a lower pulsatility in choroidal arteries. This work demonstrates the potential held by laser Doppler holography to study ocular hemodynamics in healthy and diseased eyes.

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

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2019 (7)

J. Chua, C. W. L. Chin, J. Hong, M. L. Chee, T.-T. Le, D. S. W. Ting, T. Y. Wong, and L. Schmetterer, “Impact of hypertension on retinal capillary microvasculature using optical coherence tomographic angiography,” J. Hypertens. 37, 572–580 (2019).

M. Mujat, Y. Lu, G. Maguluri, Y. Zhao, N. Iftimia, and R. D. Ferguson, “Visualizing the vasculature of the entire human eye posterior hemisphere without a contrast agent,” Biomed. Opt. Express 10, 167–180 (2019).
[Crossref] [PubMed]

L. Puyo, M. Paques, M. Fink, J.-A. Sahel, and M. Atlan, “Choroidal vasculature imaging with laser Doppler holography,” Biomed. Opt. Express 10, 995–1012 (2019).
[Crossref] [PubMed]

D. D. Postnov, X. Cheng, S. E. Erdener, and D. A. Boas, “Choosing a laser for laser speckle contrast imaging,” Sci. Reports 9, 2542 (2019).
[Crossref]

L. Ginner, A. Wartak, M. Salas, M. Augustin, M. Niederleithner, L. M. Wurster, and R. A. Leitgeb, “Synthetic subaperture-based angle-independent Doppler flow measurements using single-beam line field optical coherence tomography in vivo,” Opt. Lett. 44, 967–970 (2019).
[Crossref] [PubMed]

A. Brodoline, N. Rawat, D. Alexandre, N. Cubedo, and M. Gross, “4d compressive sensing holographic microscopy imaging of small moving objects,” Opt. Lett. 44, 2827–2830 (2019).
[Crossref]

A. Wartak, F. Beer, S. Desissaire, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Investigating spontaneous retinal venous pulsation using Doppler optical coherence tomography,” Sci. Reports 9, 4237 (2019).
[Crossref]

2018 (7)

K. Fondi, A. M. Bata, N. Luft, K. J. Witkowska, R. M. Werkmeister, D. Schmidl, M. Bolz, L. Schmetterer, and G. Garhöfer, “Evaluation of flicker induced hyperemia in the retina and optic nerve head measured by laser speckle flowgraphy,” PloS One 13, e0207525 (2018).
[Crossref] [PubMed]

L. Puyo, M. Paques, M. Fink, J.-A. Sahel, and M. Atlan, “In vivo laser Doppler holography of the human retina,” Biomed. Opt. Express 9, 4113–4129 (2018).
[Crossref]

L. Ginner, T. Schmoll, A. Kumar, M. Salas, N. Pricoupenko, L. M. Wurster, and R. A. Leitgeb, “Holographic line field en-face OCT with digital adaptive optics in the retina in vivo,” Biomed. Opt. Express 9, 472–485 (2018).
[Crossref] [PubMed]

H. Spahr, C. Pfäffle, P. Koch, H. Sudkamp, G. Hüttmann, and D. Hillmann, “Interferometric detection of 3d motion using computational subapertures in optical coherence tomography,” Opt. express 26, 18803–18816 (2018).
[Crossref] [PubMed]

A. S. Mursch-Edlmayr, N. Luft, D. Podkowinski, M. Ring, L. Schmetterer, and M. Bolz, “Laser speckle flowgraphy derived characteristics of optic nerve head perfusion in normal tension glaucoma and healthy individuals: a pilot study,” Sci. Reports 8, 5343 (2018).
[Crossref]

B. Gu, X. Wang, M. D. Twa, J. Tam, C. A. Girkin, and Y. Zhang, “Non-invasive in vivo characterization of erythrocyte motion in human retinal capillaries using high-speed adaptive optics near-confocal imaging,” Biomed. Opt. Express 9, 3653–3677 (2018).
[Crossref] [PubMed]

M. E. Safar, “Arterial stiffness as a risk factor for clinical hypertension,” Nat. Rev. Cardiol. 15, 97 (2018).
[Crossref]

2017 (1)

A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res., 7, 2 (2017).
[Crossref] [PubMed]

2016 (7)

Y. Shiga, H. Kunikata, N. Aizawa, N. Kiyota, Y. Maiya, Y. Yokoyama, K. Omodaka, H. Takahashi, T. Yasui, and K. Kato et al., “Optic nerve head blood flow, as measured by laser speckle flowgraphy, is significantly reduced in preperimetric glaucoma,” Curr. Eye Res. 41, 1447–1453 (2016).
[Crossref] [PubMed]

D. Rosenbaum, N. Kachenoura, E. Koch, M. Paques, P. Cluzel, A. Redheuil, and X. Girerd, “Relationships between retinal arteriole anatomy and aortic geometry and function and peripheral resistance in hypertensives,” Hypertens. Res. 39, 536 (2016).
[Crossref] [PubMed]

N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
[Crossref] [PubMed]

M. Pellizzari, M. Simonutti, J. Degardin, J.-A. Sahel, M. Fink, M. Paques, and M. Atlan, “High speed optical holography of retinal blood flow,” Opt. Lett. 41, 3503–3506 (2016).
[Crossref] [PubMed]

D. Donnarumma, A. Brodoline, D. Alexandre, and M. Gross, “4d holographic microscopy of zebrafish larvae microcirculation,” Opt. Express 24, 26887–26900 (2016).
[Crossref] [PubMed]

D. Hillmann, H. Spahr, C. Hain, H. Sudkamp, G. Franke, C. Pfäffle, C. Winter, and G. Hüttmann, “Aberration-free volumetric high-speed imaging of in vivo retina,” Sci. reports 6, 35209 (2016).
[Crossref]

W. H. Morgan, M. L. Hazelton, and D.-Y. Yu, “Retinal venous pulsation: Expanding our understanding and use of this enigmatic phenomenon,” Prog. In Retin. And Eye Res. 55, 82–107 (2016).
[Crossref]

2015 (3)

F. Moret, C. M. Reiff, W. A. Lagreze, and M. Bach, “Quantitative analysis of fundus-image sequences reveals phase of spontaneous venous pulsations,” Transl. Vis. Sci. & Technol. 4, 3 (2015).
[Crossref]

O. Tan, G. Liu, L. Liang, S. S. Gao, A. D. Pechauer, Y. Jia, and D. Huang, “En face Doppler total retinal blood flow measurement with 70 khz spectral optical coherence tomography,” J. Of Biomed. Opt. 20, 066004 (2015).
[Crossref]

T. Iwase, K. Yamamoto, E. Ra, K. Murotani, S. Matsui, and H. Terasaki, “Diurnal variations in blood flow at optic nerve head and choroid in healthy eyes: diurnal variations in blood flow,” Medicine 94, 519 (2015).
[Crossref]

2014 (6)

V. Doblhoff-Dier, L. Schmetterer, W. Vilser, G. Garhöfer, M. Gröschl, R. A. Leitgeb, and R. M. Werkmeister, “Measurement of the total retinal blood flow using dual beam fourier-domain Doppler optical coherence tomography with orthogonal detection planes,” Biomed. Opt. Express 5, 630–642 (2014).
[Crossref] [PubMed]

W. H. Morgan, M. L. Hazelton, B. D. Betz-Stablein, D.-Y. Yu, C. R. Lind, V. Ravichandran, and P. H. House, “Photoplethysmographic measurement of various retinal vascular pulsation parameters and measurement of the venous phase delay,” Investig. Ophthalmol. & Vis. Sci. 55, 5998–6006 (2014).
[Crossref]

C. Magnain, A. Castel, T. Boucneau, M. Simonutti, I. Ferezou, A. Rancillac, T. Vitalis, J.-A. Sahel, M. Paques, and M. Atlan, “Holographic laser Doppler imaging of microvascular blood flow,” JOSA A 31, 2723–2735 (2014).
[Crossref]

C. Demené, M. Pernot, V. Biran, M. Alison, M. Fink, O. Baud, and M. Tanter, “Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates,” J. Cereb. Blood Flow & Metab. 34, 1009–1017 (2014).
[Crossref]

S. Tsuda, H. Kunikata, M. Shimura, N. Aizawa, K. Omodaka, Y. Shiga, M. Yasuda, Y. Yokoyama, and T. Nakazawa, “Pulse-waveform analysis of normal population using laser speckle flowgraphy,” Curr. Eye Res. 39, 1207–1215 (2014).
[Crossref] [PubMed]

P. Bonnin, J.-A. C. Pournaras, K. Makowiecka, V. Krivosic, A. W. Kedra, J.-F. Le Gargasson, A. Gaudric, B. I. Levy, Y. S. Cohen, and R. Tadayoni et al., “Ultrasound assessment of ocular vascular effects of repeated intravitreal injections of ranibizumab for wet age-related macular degeneration,” Acta Ophthalmol. 92, e382–e387 (2014).
[Crossref] [PubMed]

2013 (1)

S. Mrejen and R. F. Spaide, “Optical coherence tomography: imaging of the choroid and beyond,” Surv. Ophthalmol. 58, 387–429 (2013).
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2012 (1)

W. H. Morgan, C. R. Lind, S. Kain, N. Fatehee, A. Bala, and D.-Y. Yu, “Retinal vein pulsation is in phase with intracranial pressure and not intraocular pressure,” Investig. Ophthalmol. & Vis. Sci. 53, 4676–4681 (2012).
[Crossref]

2011 (2)

R. D. Plumb, P. K. Hamilton, D. J. Rea, S. A. Wright, S. M. Hughes, R. C. McGivern, and G. E. McVeigh, “Wave reflection signatures: identifying early microvascular abnormalities in type 2 diabetes,” The Br. J. Diabetes & Vasc. Dis. 11, 243–248 (2011).
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E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods 8, 662 (2011).
[Crossref] [PubMed]

2010 (2)

C. E. Riva, M. Geiser, and B. L. Petrig, “Ocular blood flow assessment using continuous laser Doppler flowmetry,” Acta Ophthalmol. 88, 622–629 (2010).
[Crossref]

S. Kain, W. H. Morgan, and D.-Y. Yu, “New observations concerning the nature of central retinal vein pulsation,” Br. J. Ophthalmol. 94, 854–857 (2010).
[Crossref]

2009 (1)

A. P. Avolio, M. Butlin, and A. Walsh, “Arterial blood pressure measurement and pulse wave analysis: their role in enhancing cardiovascular assessment,” Physiol. Meas. 31, R1 (2009).
[Crossref]

2007 (1)

M. E. Safar and P. Lacolley, “Disturbance of macro-and microcirculation: relations with pulse pressure and cardiac organ damage,” Am. J. Physiol. Circ. Physiol. 293, H1–H7 (2007).
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2006 (1)

S. Laurent, J. Cockcroft, L. Van Bortel, P. Boutouyrie, C. Giannattasio, D. Hayoz, B. Pannier, C. Vlachopoulos, I. Wilkinson, and H. Struijker-Boudier, “Expert consensus document on arterial stiffness: methodological issues and clinical applications,” Eur. Hear. J. 27, 2588–2605 (2006).
[Crossref]

2005 (2)

A. Serov and T. Lasser, “High-speed laser Doppler perfusion imaging using an integrating cmos image sensor,” Opt. Express 13, 6416–6428 (2005).
[Crossref] [PubMed]

M. Paques, O. Baillart, O. Genevois, A. Gaudric, B. Lévy, and J. Sahel, “Systolodiastolic variations of blood flow during central retinal vein occlusion: exploration by dynamic angiography,” Br. J. Ophthalmol. 89, 1036–1040 (2005).
[Crossref] [PubMed]

2003 (2)

H. Isono, S. Kishi, Y. Kimura, N. Hagiwara, N. Konishi, and H. Fujii, “Observation of choroidal circulation using index of erythrocytic velocity,” Arch. Ophthalmol. 121, 225–231 (2003).
[Crossref] [PubMed]

F. Tranquart, O. Bergès, P. Koskas, S. Arsene, C. Rossazza, P.-J. Pisella, and L. Pourcelot, “Color Doppler imaging of orbital vessels: personal experience and literature review,” J. Clin. Ultrasound 31, 258–273 (2003).
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2002 (1)

G. E. McVeigh, P. K. Hamilton, and D. R. Morgan, “Evaluation of mechanical arterial properties: clinical, experimental and therapeutic aspects,” Clin. Sci. 102, 51–67 (2002).
[Crossref]

2001 (3)

W. W. Nichols and D. G. Edwards, “Arterial elastance and wave reflection augmentation of systolic blood pressure: deleterious effects and implications for therapy,” J. Cardiovasc. Pharmacol. Ther. 6, 5–21 (2001).
[Crossref] [PubMed]

E. Polska, K. Kircher, P. Ehrlich, P. V. Vecsei, and L. Schmetterer, “Ri in central retinal artery as assessed by cdi does not correspond to retinal vascular resistance,” Am. J. Physiol. Circ. Physiol. 280, H1442–H1447 (2001).
[Crossref]

D. Squirrell, A. Watts, D. Evans, C. Mody, and J. Talbot, “A prospective evaluation of the heidelberg retina flowmeter in diagnosing ischaemia following branch retinal vein occlusion: a masked, controlled comparison with fluorescein angiography,” Eye 15, 261 (2001).
[Crossref] [PubMed]

1999 (2)

R. O. Bude and J. M. Rubin, “Relationship between the resistive index and vascular compliance and resistance,” Radiology 211, 411–417 (1999).
[Crossref] [PubMed]

R. O. Bude and J. M. Rubin, “Effect of downstream cross-sectional area of an arterial bed on the resistive index and the early systolic acceleration,” Radiology 212, 732–738 (1999).
[Crossref] [PubMed]

1998 (1)

E. J. Halpern, D. A. Merton, and F. Forsberg, “Effect of distal resistance on Doppler US flow patterns,” Radiology 206, 761–766 (1998).
[Crossref] [PubMed]

1997 (1)

G. Michelson and J. Harazny, “Relationship between ocular pulse pressures and retinal vessel velocities,” Ophthalmology 104, 664–671 (1997).
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1996 (1)

G. Michelson, B. Schmauss, M. Langhans, J. Harazny, and M. Groh, “Principle, validity, and reliability of scanning laser Doppler flowmetry,” J. Glaucoma. 5, 99–105 (1996).
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1994 (1)

C. Riva, S. Cranstoun, J. Grunwald, and B. Petrig, “Choroidal blood flow in the foveal region of the human ocular fundus,” Invest. Ophthalmol. Vis. Sci. 35, 4273–4281 (1994).
[PubMed]

1991 (1)

W. E. Lieb, S. M. Cohen, D. A. Merton, J. A. Shields, D. G. Mitchell, and B. B. Goldberg, “Color Doppler imaging of the eye and orbit: technique and normal vascular anatomy,” Arch. Ophthalmol. 109, 527–531 (1991).
[Crossref] [PubMed]

1988 (1)

H. S. Brar and L. D. Platt, “Reverse end-diastolic flow velocity on umbilical artery velocimetry in high-risk pregnancies: an ominous finding with adverse pregnancy outcome,” Am. J. Obstet. Gynecol. 159, 559–561 (1988).
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1985 (1)

S. M. Toy, J. Melbin, and A. Noordergraaf, “Reduced models of arterial systems,” IEEE Transactions on Biomed. Eng. 1985174–176 (1985).
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1974 (1)

L. Pourcelot, “Applications cliniques de l’examen Doppler transcutane,” Velocim. Ultrason. Doppler 34, 780–785 (1974).

Aizawa, N.

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Alison, M.

C. Demené, M. Pernot, V. Biran, M. Alison, M. Fink, O. Baud, and M. Tanter, “Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates,” J. Cereb. Blood Flow & Metab. 34, 1009–1017 (2014).
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Arsene, S.

F. Tranquart, O. Bergès, P. Koskas, S. Arsene, C. Rossazza, P.-J. Pisella, and L. Pourcelot, “Color Doppler imaging of orbital vessels: personal experience and literature review,” J. Clin. Ultrasound 31, 258–273 (2003).
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N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
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Augustin, M.

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A. P. Avolio, M. Butlin, and A. Walsh, “Arterial blood pressure measurement and pulse wave analysis: their role in enhancing cardiovascular assessment,” Physiol. Meas. 31, R1 (2009).
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F. Moret, C. M. Reiff, W. A. Lagreze, and M. Bach, “Quantitative analysis of fundus-image sequences reveals phase of spontaneous venous pulsations,” Transl. Vis. Sci. & Technol. 4, 3 (2015).
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Baillart, O.

M. Paques, O. Baillart, O. Genevois, A. Gaudric, B. Lévy, and J. Sahel, “Systolodiastolic variations of blood flow during central retinal vein occlusion: exploration by dynamic angiography,” Br. J. Ophthalmol. 89, 1036–1040 (2005).
[Crossref] [PubMed]

Bala, A.

W. H. Morgan, C. R. Lind, S. Kain, N. Fatehee, A. Bala, and D.-Y. Yu, “Retinal vein pulsation is in phase with intracranial pressure and not intraocular pressure,” Investig. Ophthalmol. & Vis. Sci. 53, 4676–4681 (2012).
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G. E. McVeigh, A. J. Bank, and J. N. Cohn, “Arterial compliance,” in Cardiovascular Medicine, (Springer, 2007), pp. 1811–1831.
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K. Fondi, A. M. Bata, N. Luft, K. J. Witkowska, R. M. Werkmeister, D. Schmidl, M. Bolz, L. Schmetterer, and G. Garhöfer, “Evaluation of flicker induced hyperemia in the retina and optic nerve head measured by laser speckle flowgraphy,” PloS One 13, e0207525 (2018).
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N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
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C. Demené, M. Pernot, V. Biran, M. Alison, M. Fink, O. Baud, and M. Tanter, “Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates,” J. Cereb. Blood Flow & Metab. 34, 1009–1017 (2014).
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E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods 8, 662 (2011).
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A. Wartak, F. Beer, S. Desissaire, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Investigating spontaneous retinal venous pulsation using Doppler optical coherence tomography,” Sci. Reports 9, 4237 (2019).
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A. Wartak, F. Beer, S. Desissaire, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Investigating spontaneous retinal venous pulsation using Doppler optical coherence tomography,” Sci. Reports 9, 4237 (2019).
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F. Tranquart, O. Bergès, P. Koskas, S. Arsene, C. Rossazza, P.-J. Pisella, and L. Pourcelot, “Color Doppler imaging of orbital vessels: personal experience and literature review,” J. Clin. Ultrasound 31, 258–273 (2003).
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W. H. Morgan, M. L. Hazelton, B. D. Betz-Stablein, D.-Y. Yu, C. R. Lind, V. Ravichandran, and P. H. House, “Photoplethysmographic measurement of various retinal vascular pulsation parameters and measurement of the venous phase delay,” Investig. Ophthalmol. & Vis. Sci. 55, 5998–6006 (2014).
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C. Demené, M. Pernot, V. Biran, M. Alison, M. Fink, O. Baud, and M. Tanter, “Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates,” J. Cereb. Blood Flow & Metab. 34, 1009–1017 (2014).
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D. D. Postnov, X. Cheng, S. E. Erdener, and D. A. Boas, “Choosing a laser for laser speckle contrast imaging,” Sci. Reports 9, 2542 (2019).
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A. S. Mursch-Edlmayr, N. Luft, D. Podkowinski, M. Ring, L. Schmetterer, and M. Bolz, “Laser speckle flowgraphy derived characteristics of optic nerve head perfusion in normal tension glaucoma and healthy individuals: a pilot study,” Sci. Reports 8, 5343 (2018).
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K. Fondi, A. M. Bata, N. Luft, K. J. Witkowska, R. M. Werkmeister, D. Schmidl, M. Bolz, L. Schmetterer, and G. Garhöfer, “Evaluation of flicker induced hyperemia in the retina and optic nerve head measured by laser speckle flowgraphy,” PloS One 13, e0207525 (2018).
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N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
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R. F. Bonner and R. Nossal, “Principles of laser-Doppler flowmetry,” in Laser-Doppler Blood Flowmetry, (Springer, 1990), pp. 17–45.
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P. Bonnin, J.-A. C. Pournaras, K. Makowiecka, V. Krivosic, A. W. Kedra, J.-F. Le Gargasson, A. Gaudric, B. I. Levy, Y. S. Cohen, and R. Tadayoni et al., “Ultrasound assessment of ocular vascular effects of repeated intravitreal injections of ranibizumab for wet age-related macular degeneration,” Acta Ophthalmol. 92, e382–e387 (2014).
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C. Magnain, A. Castel, T. Boucneau, M. Simonutti, I. Ferezou, A. Rancillac, T. Vitalis, J.-A. Sahel, M. Paques, and M. Atlan, “Holographic laser Doppler imaging of microvascular blood flow,” JOSA A 31, 2723–2735 (2014).
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S. Laurent, J. Cockcroft, L. Van Bortel, P. Boutouyrie, C. Giannattasio, D. Hayoz, B. Pannier, C. Vlachopoulos, I. Wilkinson, and H. Struijker-Boudier, “Expert consensus document on arterial stiffness: methodological issues and clinical applications,” Eur. Hear. J. 27, 2588–2605 (2006).
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Brar, H. S.

H. S. Brar and L. D. Platt, “Reverse end-diastolic flow velocity on umbilical artery velocimetry in high-risk pregnancies: an ominous finding with adverse pregnancy outcome,” Am. J. Obstet. Gynecol. 159, 559–561 (1988).
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Brodoline, A.

Bude, R. O.

R. O. Bude and J. M. Rubin, “Relationship between the resistive index and vascular compliance and resistance,” Radiology 211, 411–417 (1999).
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R. O. Bude and J. M. Rubin, “Effect of downstream cross-sectional area of an arterial bed on the resistive index and the early systolic acceleration,” Radiology 212, 732–738 (1999).
[Crossref] [PubMed]

Butlin, M.

A. P. Avolio, M. Butlin, and A. Walsh, “Arterial blood pressure measurement and pulse wave analysis: their role in enhancing cardiovascular assessment,” Physiol. Meas. 31, R1 (2009).
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C. Magnain, A. Castel, T. Boucneau, M. Simonutti, I. Ferezou, A. Rancillac, T. Vitalis, J.-A. Sahel, M. Paques, and M. Atlan, “Holographic laser Doppler imaging of microvascular blood flow,” JOSA A 31, 2723–2735 (2014).
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J. Chua, C. W. L. Chin, J. Hong, M. L. Chee, T.-T. Le, D. S. W. Ting, T. Y. Wong, and L. Schmetterer, “Impact of hypertension on retinal capillary microvasculature using optical coherence tomographic angiography,” J. Hypertens. 37, 572–580 (2019).

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A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res., 7, 2 (2017).
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D. D. Postnov, X. Cheng, S. E. Erdener, and D. A. Boas, “Choosing a laser for laser speckle contrast imaging,” Sci. Reports 9, 2542 (2019).
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J. Chua, C. W. L. Chin, J. Hong, M. L. Chee, T.-T. Le, D. S. W. Ting, T. Y. Wong, and L. Schmetterer, “Impact of hypertension on retinal capillary microvasculature using optical coherence tomographic angiography,” J. Hypertens. 37, 572–580 (2019).

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J. Chua, C. W. L. Chin, J. Hong, M. L. Chee, T.-T. Le, D. S. W. Ting, T. Y. Wong, and L. Schmetterer, “Impact of hypertension on retinal capillary microvasculature using optical coherence tomographic angiography,” J. Hypertens. 37, 572–580 (2019).

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D. Rosenbaum, N. Kachenoura, E. Koch, M. Paques, P. Cluzel, A. Redheuil, and X. Girerd, “Relationships between retinal arteriole anatomy and aortic geometry and function and peripheral resistance in hypertensives,” Hypertens. Res. 39, 536 (2016).
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S. Laurent, J. Cockcroft, L. Van Bortel, P. Boutouyrie, C. Giannattasio, D. Hayoz, B. Pannier, C. Vlachopoulos, I. Wilkinson, and H. Struijker-Boudier, “Expert consensus document on arterial stiffness: methodological issues and clinical applications,” Eur. Hear. J. 27, 2588–2605 (2006).
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E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods 8, 662 (2011).
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Cohen, S. M.

W. E. Lieb, S. M. Cohen, D. A. Merton, J. A. Shields, D. G. Mitchell, and B. B. Goldberg, “Color Doppler imaging of the eye and orbit: technique and normal vascular anatomy,” Arch. Ophthalmol. 109, 527–531 (1991).
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P. Bonnin, J.-A. C. Pournaras, K. Makowiecka, V. Krivosic, A. W. Kedra, J.-F. Le Gargasson, A. Gaudric, B. I. Levy, Y. S. Cohen, and R. Tadayoni et al., “Ultrasound assessment of ocular vascular effects of repeated intravitreal injections of ranibizumab for wet age-related macular degeneration,” Acta Ophthalmol. 92, e382–e387 (2014).
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Cohn, J. N.

G. E. McVeigh, A. J. Bank, and J. N. Cohn, “Arterial compliance,” in Cardiovascular Medicine, (Springer, 2007), pp. 1811–1831.
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C. Riva, S. Cranstoun, J. Grunwald, and B. Petrig, “Choroidal blood flow in the foveal region of the human ocular fundus,” Invest. Ophthalmol. Vis. Sci. 35, 4273–4281 (1994).
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Degardin, J.

Demené, C.

C. Demené, M. Pernot, V. Biran, M. Alison, M. Fink, O. Baud, and M. Tanter, “Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates,” J. Cereb. Blood Flow & Metab. 34, 1009–1017 (2014).
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Desissaire, S.

A. Wartak, F. Beer, S. Desissaire, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Investigating spontaneous retinal venous pulsation using Doppler optical coherence tomography,” Sci. Reports 9, 4237 (2019).
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Ehrlich, P.

E. Polska, K. Kircher, P. Ehrlich, P. V. Vecsei, and L. Schmetterer, “Ri in central retinal artery as assessed by cdi does not correspond to retinal vascular resistance,” Am. J. Physiol. Circ. Physiol. 280, H1442–H1447 (2001).
[Crossref]

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D. D. Postnov, X. Cheng, S. E. Erdener, and D. A. Boas, “Choosing a laser for laser speckle contrast imaging,” Sci. Reports 9, 2542 (2019).
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D. Squirrell, A. Watts, D. Evans, C. Mody, and J. Talbot, “A prospective evaluation of the heidelberg retina flowmeter in diagnosing ischaemia following branch retinal vein occlusion: a masked, controlled comparison with fluorescein angiography,” Eye 15, 261 (2001).
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W. H. Morgan, C. R. Lind, S. Kain, N. Fatehee, A. Bala, and D.-Y. Yu, “Retinal vein pulsation is in phase with intracranial pressure and not intraocular pressure,” Investig. Ophthalmol. & Vis. Sci. 53, 4676–4681 (2012).
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Ferezou, I.

C. Magnain, A. Castel, T. Boucneau, M. Simonutti, I. Ferezou, A. Rancillac, T. Vitalis, J.-A. Sahel, M. Paques, and M. Atlan, “Holographic laser Doppler imaging of microvascular blood flow,” JOSA A 31, 2723–2735 (2014).
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Fink, M.

Fondi, K.

K. Fondi, A. M. Bata, N. Luft, K. J. Witkowska, R. M. Werkmeister, D. Schmidl, M. Bolz, L. Schmetterer, and G. Garhöfer, “Evaluation of flicker induced hyperemia in the retina and optic nerve head measured by laser speckle flowgraphy,” PloS One 13, e0207525 (2018).
[Crossref] [PubMed]

N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
[Crossref] [PubMed]

Forsberg, F.

E. J. Halpern, D. A. Merton, and F. Forsberg, “Effect of distal resistance on Doppler US flow patterns,” Radiology 206, 761–766 (1998).
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Gahm, J. K.

A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res., 7, 2 (2017).
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K. Fondi, A. M. Bata, N. Luft, K. J. Witkowska, R. M. Werkmeister, D. Schmidl, M. Bolz, L. Schmetterer, and G. Garhöfer, “Evaluation of flicker induced hyperemia in the retina and optic nerve head measured by laser speckle flowgraphy,” PloS One 13, e0207525 (2018).
[Crossref] [PubMed]

N. Luft, P. A. Wozniak, G. C. Aschinger, K. Fondi, A. M. Bata, R. M. Werkmeister, D. Schmidl, K. J. Witkowska, M. Bolz, and G. Garhöfer et al., “Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy,” PLoS One 11, e0168190 (2016).
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P. Bonnin, J.-A. C. Pournaras, K. Makowiecka, V. Krivosic, A. W. Kedra, J.-F. Le Gargasson, A. Gaudric, B. I. Levy, Y. S. Cohen, and R. Tadayoni et al., “Ultrasound assessment of ocular vascular effects of repeated intravitreal injections of ranibizumab for wet age-related macular degeneration,” Acta Ophthalmol. 92, e382–e387 (2014).
[Crossref] [PubMed]

M. Paques, O. Baillart, O. Genevois, A. Gaudric, B. Lévy, and J. Sahel, “Systolodiastolic variations of blood flow during central retinal vein occlusion: exploration by dynamic angiography,” Br. J. Ophthalmol. 89, 1036–1040 (2005).
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Supplementary Material (5)

NameDescription
» Visualization 1       Laser Doppler holography: power Doppler movie during cardiac cycles, uncorrected and corrected from the dominant signal
» Visualization 2       Laser Doppler holography: Movie of the mean frequency shift during cardiac cycles, uncorrected and corrected from the dominant signal
» Visualization 3       Laser Doppler holography: power Doppler movie
» Visualization 4       Laser Doppler holography: power Doppler monitored in a vein and an artery over cardiac cycles
» Visualization 5       Laser Doppler holography: power Doppler monitored in a vein and an artery over cardiac cycles

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Figures (9)

Fig. 1
Fig. 1 Analysis of the dynamic changes in power Doppler signal and mean Doppler frequency shift, which supposedly yield volume and velocity, respectively. (a) and (b): power Doppler image M0(x, y) and mean frequency shift fmean(x, y) temporally averaged; the red, blue, and green ROIs mark a retinal artery (RA), a retinal vein (RV), and the background (B), respectively. (c) and (d) temporal traces of M0 and fmean in the depicted ROIs. (e) and (f): temporal traces in the same ROIs when subtracting the spatially averaged signal over the entire image, i.e. M0 − 〈M0x,y, and fmean − 〈fmeanx,y. See Visualization 1 and Visualization 2 for the juxtaposed movies of M0 and fmean corrected and not-corrected from the spatial average. Removing the spatial average allows to reveal the retinal flow waveforms.
Fig. 2
Fig. 2 Dependence of the retinal arterial waveform profile upon the Doppler frequency range. All curves are obtained from the same LDH measurements, only with different processing. (a) and (b): dynamic raw power Doppler and power Doppler corrected from the spatial average for three frequency ranges: 6–10 kHz in the pink solid line, 10–20 kHz in the red dashed line, and 20–37 kHz in the deep red dotted line. (c) and (d): waveform profile averaged over three cardiac cycle with variations normalized between 0 and 1. The waveform profile calculated with the frequency band 6–10 kHz shows a pulsatile signal tainted by bulk motion (attributed by unexpected oscillations); the normalized arterial waveform calculated with the very high frequency range appears steeper due to the velocity thresholding effect.
Fig. 3
Fig. 3 Venous and arterial retinal waveforms compared to the spatial average in three examples close to the ONH. Left column: normalized waveform in a retinal vein and artery (’RV’ in blue, and ’RA’ in red), and normalized waveform of the spatial average (over the entire image) in black. As seen from the red and black dashed lines indicating the end of systole, the venous minimum is more contemporary with the retinal arterial flow maximum than with the maximum of the spatial average. See Visualization 3 and Visualization 4.
Fig. 4
Fig. 4 Mapping in three different eyes of the local blood velocity, RI, and CV indices; all images are displayed on the same gray/color scale. First row: mean Doppler frequency shift fmean(x, y). Second row: resistivity map calculated according to the Pourcelot index on the flow variations corrected from the baseline signal RIM0−〈M0x,y ; the RI value in the arteries is around 0.7. Third row: coefficient of variation map of the raw signal CVM0.
Fig. 5
Fig. 5 Comparison of CV maps obtained from the variation of M0 and fmean in the right and left eye of the same subject. From top to down: M0(x, y), CVM0(x, y), fmean(x, y), and CVfmean(x, y). The coefficient of variation in the optic disc differs significantly between the two methods. The arrow ’1’ and ’2’ point to areas where the Doppler broadening is undersampled and to low frequency noise, respectively.
Fig. 6
Fig. 6 Laser Doppler measurements in choroidal arteries in the macular and peripheral regions. (a) and (b): Mean frequency images with ROIs on a large choroidal artery (’CA’, purple) and the background (’B’, green). (c) and (d): Raw power Doppler signal M0 in the ROIs. (e) and (f): Power Doppler signal in the same ROIs when subtracting the spatially averaged dynamic value, i.e., M0 − 〈M0x,y. In the peripheral region the power Doppler signal in ’CA’ corrected from the dominant signal yields a arterial-like waveform whereas the power Doppler signal measured in ’CA’ in the macular region shows only noise. This is probably because of the higher photoreceptors/RPE density, and because the dynamic signal measured in ’CA’ in the macula is exactly like the spatial average signal.
Fig. 7
Fig. 7 Pulsatile flow in the retina and choroid. (a) Power Doppler image M0(x, y) indicating the ROIs; the red, blue, green, purple boxes mark a retinal artery and vein, the background, and a choroidal artery, respectively. (b) Mean frequency shift image fmean(x, y). (c) Waveform of M0 − 〈M0x,y in the ROIs. (d) Coefficient of variation map CVM0(x, y): the choroidal artery has a coefficient of variation close to the values found in retinal veins, despite exhibiting an arterial waveform profile. See the power Doppler movie in Visualization 5.
Fig. 8
Fig. 8 Retinal and choroidal arterial waveforms compared to the spatial average in three examples in peripheral regions. Left column: normalized waveform of power Doppler corrected from the spatial average in a retinal and a choroidal artery (’RA’ in red, and ’CA’ in purple), and normalized waveform of the Doppler signal spatially averaged over the entire image (’D’ in black). The dominant signal waveform has an arterial waveform, which strongly resembles that of choroidal arteries.
Fig. 9
Fig. 9 Arteriovenous differentiation in the retina and choroid. (a) and (b): mean Doppler frequency fmean(x, y). (c) and (d): coefficient of variation CVM0 revealing retinal arteries and veins. (e) and (f): color composite images obtained by merging low frequency and high (2.5–6 kHz, 10–30 kHz) power Doppler images in cyan and red, allowing identification of choroidal arteries and veins (colorbars are only indicative).

Equations (6)

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S ( x , y , t n , f ) = | t n t n + t win H ( x , y , τ ) exp ( 2 i π f τ ) d τ | 2
M 0 ( x , y , t n ) = S ( x , y , t n , f ) d f
M 1 ( x , y , t n ) = S ( x , y , t n , f ) f d f
f mean ( x , y , t n ) = S ( x , y , t n , f ) f d f S ( x , y , t n , f ) d f = M 1 ( x , y , t n ) M 0 ( x , y , t n )
RI g ( x , y ) = g ( x , y , t syst ) g ( x , y , t diast ) g ( x , y , t syst )
CV g ( x , y ) = σ g ( x , y ) μ g ( x , y )