Abstract

We demonstrate a new noninvasive method to assess biomechanical properties of the retinal vascular system. Phase-sensitive full-field swept-source optical coherence tomography (PhS-FF-SS-OCT) is used to investigate retinal vascular dynamics at unprecedented temporal resolution. The motion of retinal tissue that is induced by expansion of the vessels therein is measured with an accuracy of about 10 nm. The pulse shapes of arterial and venous pulsations, their temporal delays, as well as the frequency-dependent pulse propagation through the capillary bed, are determined. For the first time, imaging speed and motion sensitivity are sufficient for a direct measurement of pulse waves propagating with more than 600 mm/s in retinal vessels of a healthy young subject.

© 2015 Optical Society of America

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References

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  1. K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
    [Crossref]
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  3. T. Otto, “Modellierung des retinalen Blutflusses durch Auswertung bewegungskorrigierter Angiographie-Bildfolgen (Parametrization of the retinal blood flow by analysis of motion compensated angiography image sequences),” Ph.D. thesis (University of Heidelberg, 2000).
  4. C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).
  5. J. Seki, Am. J. Physiol. 266, H811 (1994).
  6. S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
    [Crossref]
  7. K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
    [Crossref]
  8. L. An, J. Chao, M. Johnstone, and R. K. Wang, Opt. Lett. 38, 1512 (2013).
    [Crossref]
  9. D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).
  10. O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).
  11. K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
    [Crossref]

2014 (1)

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

2013 (3)

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).

L. An, J. Chao, M. Johnstone, and R. K. Wang, Opt. Lett. 38, 1512 (2013).
[Crossref]

2012 (1)

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

2011 (1)

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

2006 (1)

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

1994 (1)

J. Seki, Am. J. Physiol. 266, H811 (1994).

An, L.

Avolio, A.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Baumann, M.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

Butlin, M.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Chao, J.

Eberhardt, K.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Flammer, J.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Franke, G.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Golzan, S. M.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Graham, S. L.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Gugleta, K.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Gupta, V.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Hain, C.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Halle, M.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Hanssen, H.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Heemann, U.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Hillmann, D.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Hinkel, L.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Hu, S.

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

Hüttmann, G.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Johnstone, M.

Katamay, R.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Kochkorov, A.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Kotliar, K.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

Kouchaki, Z.

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Lanzl, I. M.

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

Maslov, K.

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

Moens, A. I.

A. I. Moens, “Over de voortplantingssnelheid van den pols (On the propagation of pulse),” Ph.D. thesis (S.C. Van Doesburgh, 1877).

Orgul, S.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Otto, T.

T. Otto, “Modellierung des retinalen Blutflusses durch Auswertung bewegungskorrigierter Angiographie-Bildfolgen (Parametrization of the retinal blood flow by analysis of motion compensated angiography image sequences),” Ph.D. thesis (University of Heidelberg, 2000).

Papaioannou, T. G.

O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).

Schmaderer, C.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Seki, J.

J. Seki, Am. J. Physiol. 266, H811 (1994).

Spahr, H.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Stergiopulos, N.

O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).

Sudkamp, H.

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

Vardoulis, O.

O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).

Vilser, W.

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

Wang, L. V.

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

Wang, R. K.

Yeh, C.

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

Zawinka, C.

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

Am. J. Physiol. (2)

J. Seki, Am. J. Physiol. 266, H811 (1994).

O. Vardoulis, T. G. Papaioannou, and N. Stergiopulos, Am. J. Physiol. 304, H1558 (2013).

Br. J. Ophthalmol. (1)

K. Kotliar, M. Baumann, W. Vilser, and I. M. Lanzl, Br. J. Ophthalmol. 95, 675 (2011).
[Crossref]

Invest. Ophthalmol. Visual Sci. (1)

K. Gugleta, A. Kochkorov, R. Katamay, C. Zawinka, J. Flammer, and S. Orgul, Invest. Ophthalmol. Visual Sci. 47, 4019 (2006).
[Crossref]

J. Biomed. Opt. (1)

C. Yeh, S. Hu, K. Maslov, and L. V. Wang, J. Biomed. Opt. 17, 070504 (2012).

Microcirculation (1)

K. Kotliar, H. Hanssen, K. Eberhardt, W. Vilser, C. Schmaderer, M. Halle, U. Heemann, and M. Baumann, Microcirculation 20, 405 (2013).
[Crossref]

Microvasc. Res. (1)

S. M. Golzan, M. Butlin, Z. Kouchaki, V. Gupta, A. Avolio, and S. L. Graham, Microvasc. Res. 92, 56 (2014).
[Crossref]

Opt. Lett. (1)

Other (3)

D. Hillmann, H. Spahr, H. Sudkamp, C. Hain, L. Hinkel, G. Franke, and G. Hüttmann, “Off-axis full-field swept-source OCT and holoscopy,” Opt. Express (in preparation).

A. I. Moens, “Over de voortplantingssnelheid van den pols (On the propagation of pulse),” Ph.D. thesis (S.C. Van Doesburgh, 1877).

T. Otto, “Modellierung des retinalen Blutflusses durch Auswertung bewegungskorrigierter Angiographie-Bildfolgen (Parametrization of the retinal blood flow by analysis of motion compensated angiography image sequences),” Ph.D. thesis (University of Heidelberg, 2000).

Supplementary Material (1)

NameDescription
» Visualization 1: MP4 (2829 KB)      Retinal thickness changes during four complete cardiac cycles

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Figures (6)

Fig. 1.
Fig. 1. Setup for FF-SS-OCT. The light of a wavelength tuned laser source is split into sample illumination (blue) and reference wave (green). The latter is superimposed with backscattered sample light (red) on the 2D camera sensor. To split the field of view, the components in frame (a) were replaced by those in frame (b).
Fig. 2.
Fig. 2. (a) SLO image showing the investigated areas on the retina. The behavior of arterial and venous pulsations is analyzed in the region marked by the large yellow frame. Red/orange (A1/A2) and blue/green (V1/V2) frames indicate the two fields of view that were used for the measurement of arterial and venous PWV, respectively. (b) OCT angiography of the yellow framed area measured using FF-SS-OCT. The black line indicates the position of the B-scan shown in (c), where the measurement principle is demonstrated: The pressure-induced expansion of the vascular system causes axial motion of the surrounding tissue, which is measured by PhS-FF-SS-OCT.
Fig. 3.
Fig. 3. Retinal thickness changes during four complete cardiac cycles are shown in Visualization 1. Here, six representative frames of the first cycle are shown. First the artery expands; then the vein follows. When the pulse wave has passed, the tissue returns to its initial state until the next pulse wave arrives.
Fig. 4.
Fig. 4. Retinal pulsation near the artery and vein extracted at the locations indicated in Fig. 2(b). Additionally, the band-pass filtered pulsation is shown. The time delay between the band-pass filtered curves is 99 ms, while the foot-to-foot delay of the measured curves is just 19 ± 4 ms .
Fig. 5.
Fig. 5. Frequency spectra of the pulsation near the artery (red) and vein (blue). Additionally, the frequency-dependent time delay between arterial and venous pulsation is calculated using the corresponding phase differences of the Fourier spectra.
Fig. 6.
Fig. 6. Pulsation of a proximal and a distal segment of a large retinal artery and vein, respectively.

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