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Optics Express

Optics Express

  • Editor: C. Martijn de Sterke
  • Vol. 19, Iss. 2 — Jan. 17, 2011
  • pp: 1271–1283
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Comprehensive in vivo micro-vascular imaging of the human eye by dual-beam-scan Doppler optical coherence angiography

Shuichi Makita, Franck Jaillon, Masahiro Yamanari, Masahiro Miura, and Yoshiaki Yasuno  »View Author Affiliations


Optics Express, Vol. 19, Issue 2, pp. 1271-1283 (2011)
http://dx.doi.org/10.1364/OE.19.001271


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Abstract

Comprehensive angiography provides insight into the diagnosis of vascular-related diseases. However, complex microvascular networks of unstable in vivo organs such as the eye require micron-scale resolution in three dimensions and a high sampling rate to access a wide area as maintaining the high resolution. Here, we introduce dual-beam-scan Doppler optical coherence angiography (OCA) as a label-free comprehensive ophthalmic angiography that satisfies theses requirements. In addition to high resolution and high imaging speed, high sensitivity to motion for detecting tiny blood flow of microvessels is achieved by detecting two time-delayed signals with scanning of two probing beams separated on a sample. We present in vivo three-dimensional imaging of the microvasculature of the posterior part of the human eye. The demonstrated results show that this technique may be used for comprehensive ophthalmic angiography to evaluate the vasculature of the posterior human eye and to diagnose variety of vascular diseases.

© 2011 OSA

1. Introduction

Assessment of the circulatory system is essential for diagnosing diseases and investigating pathology. Vascular imaging is a powerful tool to assess of the circulatory system. In clinical ophthalmology, however, there are many difficulties in vascular imaging. The eye has one of the most complex vascular systems because of its fine anatomy to form the vision system. Fluorescence angiography is the current standard diagnostic method for assessing circulation in the posterior eye [1

1. S. Dithmar, and F. G. Holz, Fluorescence Angiography in Ophthalmology (Springer, 2008).

], providing detailed visualization of the retinal and choroidal vasculature. However, it has nearly no depth-resolving power due to the property of eye optics and sensitivity [1

1. S. Dithmar, and F. G. Holz, Fluorescence Angiography in Ophthalmology (Springer, 2008).

], making it difficult to access the longitudinal vasculature. There are several other techniques of optical blood flow imaging in vivo human posterior eye [2

2. A. Fercher and J. Briers, “Flow visualization by means of single-exposure speckle photography,” Opt. Commun. 37(5), 326–330 (1981). [CrossRef]

4

4. D. A. Nelson, S. Krupsky, A. Pollack, E. Aloni, M. Belkin, I. Vanzetta, M. Rosner, and A. Grinvald, “Special report: Noninvasive multi-parameter functional optical imaging of the eye,” Ophthalmic Surg. Lasers Imaging 36(1), 57–66 (2005). [PubMed]

]. However, all of them have the same disadvantage of axial resolution. Widely used non-ophthalmic vascular imaging such as computed tomographic and magnetic resonance angiographies [5

5. G. D. Rubin, and N. M. Rofsky, eds., CT and MR Angiography: Comprehensive Vascular Assessment (Lippincott Williams & Wilkins Publishers, Philadelphia, 2008).

] and ultrasound sonography are unsuitable because they provide poor resolutions compared to fine structures in the eye.

Angiographic imaging using optical coherence tomography (OCT) [6

6. W. Drexler, and J. G. Fujimoto, eds., Optical Coherence Tomography: Technology and Applications, Biological and Medical Physics, Biomedical Engineering (Springer, 2008).

] is a possible alternative to current methods. OCT with a spectrally resolved detection scheme [7

7. A. Fercher, C. Hitzenberger, G. Kamp, and S. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995). [CrossRef]

10

10. N. A. Nassif, B. Cense, B. H. Park, M. C. Pierce, S. H. Yun, B. E. Bouma, G. J. Tearney, T. C. Chen, and J. F. de Boer, “In vivo high-resolution video-rate spectral-domain optical coherence tomography of the human retina and optic nerve,” Opt. Express 12(3), 367–376 (2004). [CrossRef] [PubMed]

] enables high-speed three-dimensional volumetric imaging in vivo [11

11. U. Schmidt-Erfurth, R. A. Leitgeb, S. Michels, B. Povazay, S. Sacu, B. Hermann, C. Ahlers, H. Sattmann, C. Scholda, A. F. Fercher, and W. Drexler, “Three-dimensional ultrahigh-resolution optical coherence tomography of macular diseases,” Invest. Ophthalmol. Vis. Sci. 46(9), 3393–3402 (2005). [CrossRef] [PubMed]

15

15. S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, and B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2007). [CrossRef]

]. Volumetric vasculature imaging [16

16. S. Makita, Y. Hong, M. Yamanari, T. Yatagai, and Y. Yasuno, “Optical coherence angiography,” Opt. Express 14(17), 7821–7840 (2006). [CrossRef] [PubMed]

21

21. V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, “Quantitative cerebral blood flow with optical coherence tomography,” Opt. Express 18(3), 2477–2494 (2010). [CrossRef] [PubMed]

] is also enabled by high-speed blood flow detection with OCT [22

22. R. Leitgeb, L. Schmetterer, W. Drexler, A. Fercher, R. Zawadzki, and T. Bajraszewski, “Real-time assessment of retinal blood flow with ultrafast acquisition by color Doppler Fourier domain optical coherence tomography,” Opt. Express 11(23), 3116–3121 (2003). [CrossRef] [PubMed]

,23

23. B. R. White, M. C. Pierce, N. Nassif, B. Cense, B. H. Park, G. J. Tearney, B. E. Bouma, T. C. Chen, and J. F. de Boer, “In vivo dynamic human retinal blood flow imaging using ultra-high-speed spectral domain optical coherence tomography,” Opt. Express 11(25), 3490–3497 (2003). [CrossRef] [PubMed]

]. High-sensitive angiographic OCTs are recently presented by using Doppler phase shift between successive B-scans or specialized beam-scan pattern [24

24. B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009). [CrossRef] [PubMed]

27

27. 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]

]. However, to obtain high sensitivity, still the options of spatial sampling configuration are limited. This limitation causes the loss of imaging speed and a disadvantage for high-speed and high-sensitive angiography of in vivo eye imaging.

In this paper, we developed three-dimensional angiography with high-speed OCT, called optical coherence angiography (OCA) [16

16. S. Makita, Y. Hong, M. Yamanari, T. Yatagai, and Y. Yasuno, “Optical coherence angiography,” Opt. Express 14(17), 7821–7840 (2006). [CrossRef] [PubMed]

], with dual-beam-scan Doppler detection. Time-delayed dual scan with two probes is used to achieve high sensitivity and high speed imaging. We demonstrate the utility of dual-beam-scan Doppler OCA to perform high-speed, high-resolution three-dimensional imaging of the vasculature in the in vivo human eye.

2. Method

2.1. Principle of dual-beam-scan Doppler detection

2.2. System configuration

The polarization controller in the SM fiber regulated the polarization state at the connection between the SM and PM fibers to ensure identical optical powers in each mode and the same sensitivity in both polarization channels. The optical power on a sample is 370 μW for each polarization mode. The total power is 740 μW, which is lower than the safe exposure limit according to the ANSI standard (Z136.1). The predicted shot-noise-limited sensitivity is 100 dB with an integration time of 34.8 μs. The sensitivity was measured as 94 and 93 dB for each channel, which was approximately 6 dB lower than the shot-noise-limited sensitivity. This is reasonable since the optical power loss of the system was measured to be 6.5 dB, which may be due to the loss at fiber re-coupling, polarization crosstalk in optical components, the alignment error of the mirror sample for sensitivity measurement because of the difficulty to align the mirror for both separated sampling beams. The beam diameter at 1/e2 on the cornea is about 820 μm: the beam spot diameter on the retina is around 13 μm (FWHM). The axial resolution of approximately 8 μm (FWHM) in air is achieved.

A cross coupling between the polarization channels could cause a ghost image in PM fiber-based system [31

31. M. K. Al-Qaisi and T. Akkin, “Polarization-sensitive optical coherence tomography based on polarization-maintaining fibers and frequency multiplexing,” Opt. Express 16(17), 13032–13041 (2008). [CrossRef] [PubMed]

,32

32. E. Götzinger, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Polarization maintaining fiber based ultra-high resolution spectral domain polarization sensitive optical coherence tomography,” Opt. Express 17(25), 22704–22717 (2009). [CrossRef]

]. However, this ghost image is negligible in our system by the following reasons. (1) In the sample arm, backscattering at the tissue will cause the alteration of the state of polarization, and cross-polarized component generated by the alteration will cause the cross coupling. However, in our system, the Wollaston prism directs the cross-polarized component out of the fiber core, and it does not contribute to the generation of the ghost image. (2) In the reference arm, since there are only a few optical elements and no polarization component, the polarization cross coupling is small. In addition, the extinction ratios of all the polarizing optics are high for the entire bandwidth, because the light source employed in our system is not ultra-broadband. Because of these reasons the cross coupling are reasonably small and the ghost image is negligible.

2.3. Flow image processing

Flow signal is obtained with post-signal processing. Two OCT signals are aligned horizontally and longitudinally. The lateral displacement is corrected by accounting the observation time. Fiber-length-mismatch between the sample and reference arms and its resulting group delay mismatch between two polarization channels of PM fiber causes axial displacement between the two OCT signals. The variance of the phase difference of two OCT signals takes its minimum when this axial displacement was cancelled. In the system calibration process, this displacement was determined by minimizing the phase variance of OCT signals obtained from a static turbid phantom, and numerically cancelled in the true measurement process. Two OCT signals at the same location are obtained. The phase shift between them is provided by using the Kasai auto-correlation Δφ(xi,zj)=Arg[kMlNΓf(xi+k+n,zj+l)Γ(xi+k,zj+l)p*], where Γp and Γf are axial complex OCT signals obtained by preceding and following probing beams, respectively, i and j are indices of pixel, n is the number of axial scans in time delay ΔT, and M and N are lateral and axial window sizes, respectively.

One important post-image processing is removing low signal region. Since the low signal-to-noise ratio exhibits random phase distribution, it disturbs flow images. Doppler phase shift are masked for display by applying a particular threshold to averaged auto-correlation g(xi,zj)=1MN|kMlNΓf(xi+k+n,zj+l)Γ(xi+k,zj+l)p*|. Since this averaging makes g approaching to the population correlation, it will be suppressed and to be zero in the case of completely random noise while maintained for the correlated signals. The threshold level can be set lower and classification accuracy will be high. As for additive white noise, SD-OCT noise is a zero-mean circular Gaussian variable, where the amplitude is a random Rayleigh variable. The probability density distribution of the amplitude of the product of the noise is a double-Rayleigh distribution [33

33. J. Salo, H. El-Sallabi, and P. Vainikainen, “The Distribution of the Product of Independent Rayleigh Random Variables,” IEEE Trans. Antenn. Propag. 54(2), 639–643 (2006). [CrossRef]

]. The threshold level was determined from the mean πσ 2/4 and deviation 16π2σ2/4 of the amplitude of correlation and the averaging window size M and N as
Δφ'(xi,zj)={Δφ(xi,zj),g(xi,zj)(π4+α16π24)σ2MN0,otherwise
(2)
where σ is the standard deviation of amplitude noise in the OCT signal and α is a constant factor set as 4 or 6.

Squared Doppler phase shift is calculated from the result of Eq. (2) and used for qualitative vasculature imaging. Projection images are created by integrating the squared phase shift along the depth. Stereograms, which are pairs of projections from slightly different angle, are provided to show three-dimensional distribution of vasculature. Boundary segmentation algorithm has been applied to separate the retina and the choroid [16

16. S. Makita, Y. Hong, M. Yamanari, T. Yatagai, and Y. Yasuno, “Optical coherence angiography,” Opt. Express 14(17), 7821–7840 (2006). [CrossRef] [PubMed]

].

3. Results

To demonstrate the use of wide-field angiography in the in vivo human eye, six sections were scanned to compose wide-field images. The mosaic of vasculature images at the retina and the choroid are shown in Fig. 4a
Fig. 4 Wide-field mosaic images of the (a) retinal and (b) choroidal vasculature. Six sessions with scan size of 30 × 30 degrees (512 × 256 lines) comprise the mosaic image. The observation time of local motion ΔΤ is 396 μs. Acquisition time is around 5 seconds.
and 4b. Each section was acquired in 5 s and covers an approximate 7.8 × 7.8 mm2 area. The total acquisition time was 30 s and the mosaic image covers around 16 × 20 mm2. Owing to the high-resolution three-dimensional imaging, two overlaid vasculatures, the retina and the choroid, can be discriminated. Major retinal vessels around the optic nerve head (ONH) and the macula were observed (Fig. 4a). Fine branches around the fovea were also clearly visualized. In Fig. 4b, the fine choroidal vasculature of the peripapillary region was well contrasted. It shows macroscopic structural properties of vasculature in the posterior eye.

Abnormal choroidal vasculature imaging is a significant application for optical coherence angiography [34

34. M. Miura, S. Makita, T. Iwasaki, and Y. Yasuno, “Three-dimensional visualization of ocular vascular pathology by optical coherence angiography in vivo,” Invest. Ophthalmol. Vis. Sci. (to be published). [PubMed]

]. Vasculature imaging has also been used in polypoidal choroidal vasculopathy (PCV) to show the ability of the dual-beam-scan Doppler OCA to the abnormal vasculature investigation. Five pathologic eyes of 4 subjects with PCV were scanned over a 3.9 × 3.9 mm2 area with 512 × 256 points around the macula. The observation time of Doppler detection was 792 μs, namely, a single location on the retina was scanned twice with the time separation of 792 μs. Abnormal choroidal vascular network and detachment and elevation of the retinal pigment epithelium (RPE) are characteristics of PCV [35

35. A. P. Ciardella, I. M. Donsoff, S. J. Huang, D. L. Costa, and L. A. Yannuzzi, “Polypoidal choroidal vasculopathy,” Surv. Ophthalmol. 49(1), 25–37 (2004). [CrossRef] [PubMed]

,36

36. R. A. Costa, E. V. Navajas, M. E. Farah, D. Calucci, J. A. Cardillo, and I. U. Scott, “Polypoidal choroidal vasculopathy: angiographic characterization of the network vascular elements and a new treatment paradigm,” Prog. Retin. Eye Res. 24(5), 560–586 (2005). [CrossRef] [PubMed]

]. The representative images are shown in Fig. 5
Fig. 5 Abnormal vasculature distribution of a polypoidal choroidal vasculopathy eye. a, Wall-eyed stereoview showing three-dimensional vasculature at a lesion. b, Registered fluorescence image obtained by Indocyanine green angiography (ICGA). c, An OCT image shows the cross-sectional morphology at the lesion (white line in d). d, An en-face cross section of OCT and OCA shows the longitudinal position of the abnormal vasculature (yellow line in c).
. The depth resolved vasculatures can be observed in a stereogram (Fig. 5a). There is a thick abnormal vascular network under the RPE at the fovea. Figure 5a also indicates that the network is located above the surrounding choroidal vessels. Retinal vessels undulated in the longitudinal direction since the retina was elevated. In PCV, polyp-like lesions with pigment epithelium detachment (PED) occur around the abnormal vascular network, visualization of which was provided by the dual-beam-scan Doppler OCA image. In a comparison with Indocyanine green angiography (ICGA) (Fig. 5b), it is found that the remarkable abnormal vasculature generated a similar pattern in both OCA and ICGA images. The longitudinal location of the vascular network can be identified by simultaneously displaying cross-sectional tomography of the eye. A cross-sectional structure of the posterior part is observed by OCT image (Fig. 5c). The RPE was elevated and the complex tissue existed between the RPE and the choroid. In the en-face cross section of the blood flow image overlaid on the OCT image (Fig. 5d), the abnormal vasculature existed at this layer. Although the origin of these abnormal vessels is controversial, dual-beam-scan Doppler OCA will provide a new insight to the debate about this pathology.

4. Discussion

FA and ICGA are current clinical standard for ophthalmic angiography. Dual-beam-scan Doppler OCA possesses two evident advantages to these conventional angiographies. First, OCA can assess full three dimensional structure of vasculatures, while FA and ICGA are nominally two-dimensional modalities. Second, OCA is totally non-invasive, while FA and ICGA are known to have moderate but frequent adverse reactions, e.g. nausea, and rare but severe reactions, e.g. anaphylaxes. These two advantages will make OCA as a tool for routine assessment.

In the current system, dual probing beams are provided with mutually orthogonal linear polarization states. Hence, the phase shift between two channels due to birefringence of tissue will be occurred and results in artifacts. The flow images are possibly disturbed at and beneath thick and/or high birefringent tissues, such as thick nerve fiber layer close to the optic nerve head, nerve fiber in the optic disc, and the sclera. The polarization scrambling also causes phase retardation between two different polarization states [48

48. M. Pircher, E. Götzinger, O. Findl, S. Michels, W. Geitzenauer, C. Leydolt, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Human macula investigated in vivo with polarization-sensitive optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 47(12), 5487–5494 (2006). [CrossRef] [PubMed]

]. Although the RPE is known to cause polarization scrambling [48

48. M. Pircher, E. Götzinger, O. Findl, S. Michels, W. Geitzenauer, C. Leydolt, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Human macula investigated in vivo with polarization-sensitive optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 47(12), 5487–5494 (2006). [CrossRef] [PubMed]

], the polarization change at pigments [49

49. B. Baumann, S. O. Baumann, T. Konegger, M. Pircher, E. Gotzinger, H. Sattmann, M. Litschauer, and C. K. Hitzenberger, “Polarization sensitive optical coherence tomography of melanin provides tissue inherent contrast based on depolarization,” Proc. SPIE 7554, 75541M, 75541M-6 (2010), https://cogrt.bk.tsukuba.ac.jp/COG/locked/yasuno/papers/BiOS2010Proceedings/DATA/7554_57.PDF. [CrossRef]

] may be caused by scattering, and hence the light passing through the RPE without scattering might not be suffered by the polarization change. Hence the polarization scrambling at the RPE may not affect to choroidal flow imaging. In contrast, choroidal pigments may disturb the flow imaging.

Fast bulk eye motion such as saccade can cause large shift between two channels laterally and longitudinally. The shift due to the bulk motion decreases correlation between two channels and results in increased phase shift noise. During in vivo eye imaging, flow images were corrupted if saccade occurred. However, if the shift is only along axial and beam separation directions, it could be compensated by post-image registration.

At the macula, very rich choroidal perfusion and dense network of fine vessels are expected. Perhaps due to resolution limitations, the capillary network in the choroid was not resolved in current dual-beam-scan Doppler OCA images. To visualize large choroidal vessels, more high penetration to the choroid will be needed. The combination of recently developed high-penetration OCT with 1-um wavelength probe [50

50. B. Povazay, B. Hermann, B. Hofer, V. Kajić, E. Simpson, T. Bridgford, and W. Drexler, “Wide-field optical coherence tomography of the choroid in vivo,” Invest. Ophthalmol. Vis. Sci. 50(4), 1856–1863 (2008). [CrossRef] [PubMed]

,51

51. Y. Yasuno, M. Miura, K. Kawana, S. Makita, M. Sato, F. Okamoto, M. Yamanari, T. Iwasaki, T. Yatagai, and T. Oshika, “Visualization of sub-retinal pigment epithelium morphologies of exudative macular diseases by high-penetration optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 50(1), 405–413 (2008). [CrossRef] [PubMed]

] and the dual-beam-scan scheme may enable the visualization of large choroidal vessels in the future.

5. Conclusion

Conventional techniques remain limited for vasculature imaging. On the other hand, the investigation of the dynamics of blood flow is fundamental for a comprehensive assessment of the circulatory system, and it requires high-speed, high-sensitivity, and high-resolution flow measurement. The dual-beam-scan method is able to provide these three requirements simultaneously. Further improvements of the acquisition system, particularly in its speed, will enable four dimensional imaging of microvessel perfusion and further assessment of circulatory system.

Acknowledgements

This research is partially supported by Japan Science and Technology Agency through the contract of Development of Systems and Technology for Advanced Measurement and Analysis.

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C. K. Hitzenberger and A. F. Fercher, “Differential phase contrast in optical coherence tomography,” Opt. Lett. 24(9), 622–624 (1999). [CrossRef]

29.

D. P. Davé and T. E. Milner, “Optical low-coherence reflectometer for differential phase measurement,” Opt. Lett. 25(4), 227–229 (2000). [CrossRef]

30.

M. Yamanari, S. Makita, V. D. Madjarova, T. Yatagai, and Y. Yasuno, “Fiber-based polarization-sensitive Fourier domain optical coherence tomography using B-scan-oriented polarization modulation method,” Opt. Express 14(14), 6502–6515 (2006). [CrossRef] [PubMed]

31.

M. K. Al-Qaisi and T. Akkin, “Polarization-sensitive optical coherence tomography based on polarization-maintaining fibers and frequency multiplexing,” Opt. Express 16(17), 13032–13041 (2008). [CrossRef] [PubMed]

32.

E. Götzinger, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Polarization maintaining fiber based ultra-high resolution spectral domain polarization sensitive optical coherence tomography,” Opt. Express 17(25), 22704–22717 (2009). [CrossRef]

33.

J. Salo, H. El-Sallabi, and P. Vainikainen, “The Distribution of the Product of Independent Rayleigh Random Variables,” IEEE Trans. Antenn. Propag. 54(2), 639–643 (2006). [CrossRef]

34.

M. Miura, S. Makita, T. Iwasaki, and Y. Yasuno, “Three-dimensional visualization of ocular vascular pathology by optical coherence angiography in vivo,” Invest. Ophthalmol. Vis. Sci. (to be published). [PubMed]

35.

A. P. Ciardella, I. M. Donsoff, S. J. Huang, D. L. Costa, and L. A. Yannuzzi, “Polypoidal choroidal vasculopathy,” Surv. Ophthalmol. 49(1), 25–37 (2004). [CrossRef] [PubMed]

36.

R. A. Costa, E. V. Navajas, M. E. Farah, D. Calucci, J. A. Cardillo, and I. U. Scott, “Polypoidal choroidal vasculopathy: angiographic characterization of the network vascular elements and a new treatment paradigm,” Prog. Retin. Eye Res. 24(5), 560–586 (2005). [CrossRef] [PubMed]

37.

M. Levoy, “Display of surfaces from volume data,” IEEE Comput. Graph. Appl. 8(3), 29–37 (1988). [CrossRef]

38.

G. A. Cioffi, E. Granstam, and A. Alm, Adler’s Physiology of the Eye: Clinical Application (Mosby, Inc., 2003), chap. 33, p. 747, 10th ed.

39.

D. Toussaint, T. Kuwabara, and D. G. Cogan, “Retinal vascular patterns. II. Human retinal vessels studied in three dimensions,” Arch. Ophthalmol. 65, 575–581 (1961). [PubMed]

40.

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]

41.

G. H. Bresnick, R. Condit, S. Syrjala, M. Palta, A. Groo, and K. Korth, “Abnormalities of the foveal avascular zone in diabetic retinopathy,” Arch. Ophthalmol. 102(9), 1286–1293 (1984). [PubMed]

42.

O. Arend, S. Wolf, F. Jung, B. Bertram, H. Pöstgens, H. Toonen, and M. Reim, “Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network,” Br. J. Ophthalmol. 75(9), 514–518 (1991). [CrossRef] [PubMed]

43.

J. Conrath, R. Giorgi, D. Raccah, and B. Ridings, “Foveal avascular zone in diabetic retinopathy: quantitative vs qualitative assessment,” Eye (Lond.) 19(3), 322–326 (2005). [CrossRef]

44.

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006). [CrossRef] [PubMed]

45.

J. B. Pawley, ed., Handbook of biological confocal microscopy (Plenum Press, New York, 1995), 2nd ed.

46.

B. J. Vakoc, G. J. Tearney, and B. E. Bouma, “Statistical properties of phase-decorrelation in phase-resolved Doppler optical coherence tomography,” IEEE Trans. Med. Imaging 28(6), 814–821 (2009). [CrossRef] [PubMed]

47.

S. Wolf, O. Arend, K. Schulte, T. H. Ittel, and M. Reim, “Quantification of retinal capillary density and flow velocity in patients with essential hypertension,” Hypertension 23(4), 464–467 (1994). [PubMed]

48.

M. Pircher, E. Götzinger, O. Findl, S. Michels, W. Geitzenauer, C. Leydolt, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Human macula investigated in vivo with polarization-sensitive optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 47(12), 5487–5494 (2006). [CrossRef] [PubMed]

49.

B. Baumann, S. O. Baumann, T. Konegger, M. Pircher, E. Gotzinger, H. Sattmann, M. Litschauer, and C. K. Hitzenberger, “Polarization sensitive optical coherence tomography of melanin provides tissue inherent contrast based on depolarization,” Proc. SPIE 7554, 75541M, 75541M-6 (2010), https://cogrt.bk.tsukuba.ac.jp/COG/locked/yasuno/papers/BiOS2010Proceedings/DATA/7554_57.PDF. [CrossRef]

50.

B. Povazay, B. Hermann, B. Hofer, V. Kajić, E. Simpson, T. Bridgford, and W. Drexler, “Wide-field optical coherence tomography of the choroid in vivo,” Invest. Ophthalmol. Vis. Sci. 50(4), 1856–1863 (2008). [CrossRef] [PubMed]

51.

Y. Yasuno, M. Miura, K. Kawana, S. Makita, M. Sato, F. Okamoto, M. Yamanari, T. Iwasaki, T. Yatagai, and T. Oshika, “Visualization of sub-retinal pigment epithelium morphologies of exudative macular diseases by high-penetration optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 50(1), 405–413 (2008). [CrossRef] [PubMed]

OCIS Codes
(170.3890) Medical optics and biotechnology : Medical optics instrumentation
(170.4460) Medical optics and biotechnology : Ophthalmic optics and devices
(170.4470) Medical optics and biotechnology : Ophthalmology
(170.4500) Medical optics and biotechnology : Optical coherence tomography

ToC Category:
Medical Optics and Biotechnology

History
Original Manuscript: November 24, 2010
Revised Manuscript: January 7, 2011
Manuscript Accepted: January 9, 2011
Published: January 11, 2011

Virtual Issues
Vol. 6, Iss. 2 Virtual Journal for Biomedical Optics

Citation
Shuichi Makita, Franck Jaillon, Masahiro Yamanari, Masahiro Miura, and Yoshiaki Yasuno, "Comprehensive in vivo micro-vascular imaging of the human eye by dual-beam-scan Doppler optical coherence angiography," Opt. Express 19, 1271-1283 (2011)
http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-19-2-1271


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  28. C. K. Hitzenberger and A. F. Fercher, “Differential phase contrast in optical coherence tomography,” Opt. Lett. 24(9), 622–624 (1999). [CrossRef]
  29. D. P. Davé and T. E. Milner, “Optical low-coherence reflectometer for differential phase measurement,” Opt. Lett. 25(4), 227–229 (2000). [CrossRef]
  30. M. Yamanari, S. Makita, V. D. Madjarova, T. Yatagai, and Y. Yasuno, “Fiber-based polarization-sensitive Fourier domain optical coherence tomography using B-scan-oriented polarization modulation method,” Opt. Express 14(14), 6502–6515 (2006). [CrossRef] [PubMed]
  31. M. K. Al-Qaisi and T. Akkin, “Polarization-sensitive optical coherence tomography based on polarization-maintaining fibers and frequency multiplexing,” Opt. Express 16(17), 13032–13041 (2008). [CrossRef] [PubMed]
  32. E. Götzinger, B. Baumann, M. Pircher, and C. K. Hitzenberger, “Polarization maintaining fiber based ultra-high resolution spectral domain polarization sensitive optical coherence tomography,” Opt. Express 17(25), 22704–22717 (2009). [CrossRef]
  33. J. Salo, H. El-Sallabi, and P. Vainikainen, “The Distribution of the Product of Independent Rayleigh Random Variables,” IEEE Trans. Antenn. Propag. 54(2), 639–643 (2006). [CrossRef]
  34. M. Miura, S. Makita, T. Iwasaki, and Y. Yasuno, “Three-dimensional visualization of ocular vascular pathology by optical coherence angiography in vivo,” Invest. Ophthalmol. Vis. Sci. (to be published). [PubMed]
  35. A. P. Ciardella, I. M. Donsoff, S. J. Huang, D. L. Costa, and L. A. Yannuzzi, “Polypoidal choroidal vasculopathy,” Surv. Ophthalmol. 49(1), 25–37 (2004). [CrossRef] [PubMed]
  36. R. A. Costa, E. V. Navajas, M. E. Farah, D. Calucci, J. A. Cardillo, and I. U. Scott, “Polypoidal choroidal vasculopathy: angiographic characterization of the network vascular elements and a new treatment paradigm,” Prog. Retin. Eye Res. 24(5), 560–586 (2005). [CrossRef] [PubMed]
  37. M. Levoy, “Display of surfaces from volume data,” IEEE Comput. Graph. Appl. 8(3), 29–37 (1988). [CrossRef]
  38. G. A. Cioffi, E. Granstam, and A. Alm, Adler’s Physiology of the Eye: Clinical Application (Mosby, Inc., 2003), chap. 33, p. 747, 10th ed.
  39. D. Toussaint, T. Kuwabara, and D. G. Cogan, “Retinal vascular patterns. II. Human retinal vessels studied in three dimensions,” Arch. Ophthalmol. 65, 575–581 (1961). [PubMed]
  40. 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]
  41. G. H. Bresnick, R. Condit, S. Syrjala, M. Palta, A. Groo, and K. Korth, “Abnormalities of the foveal avascular zone in diabetic retinopathy,” Arch. Ophthalmol. 102(9), 1286–1293 (1984). [PubMed]
  42. O. Arend, S. Wolf, F. Jung, B. Bertram, H. Pöstgens, H. Toonen, and M. Reim, “Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network,” Br. J. Ophthalmol. 75(9), 514–518 (1991). [CrossRef] [PubMed]
  43. J. Conrath, R. Giorgi, D. Raccah, and B. Ridings, “Foveal avascular zone in diabetic retinopathy: quantitative vs qualitative assessment,” Eye (Lond.) 19(3), 322–326 (2005). [CrossRef]
  44. H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006). [CrossRef] [PubMed]
  45. J. B. Pawley, ed., Handbook of biological confocal microscopy (Plenum Press, New York, 1995), 2nd ed.
  46. B. J. Vakoc, G. J. Tearney, and B. E. Bouma, “Statistical properties of phase-decorrelation in phase-resolved Doppler optical coherence tomography,” IEEE Trans. Med. Imaging 28(6), 814–821 (2009). [CrossRef] [PubMed]
  47. S. Wolf, O. Arend, K. Schulte, T. H. Ittel, and M. Reim, “Quantification of retinal capillary density and flow velocity in patients with essential hypertension,” Hypertension 23(4), 464–467 (1994). [PubMed]
  48. M. Pircher, E. Götzinger, O. Findl, S. Michels, W. Geitzenauer, C. Leydolt, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Human macula investigated in vivo with polarization-sensitive optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 47(12), 5487–5494 (2006). [CrossRef] [PubMed]
  49. B. Baumann, S. O. Baumann, T. Konegger, M. Pircher, E. Gotzinger, H. Sattmann, M. Litschauer, and C. K. Hitzenberger, “Polarization sensitive optical coherence tomography of melanin provides tissue inherent contrast based on depolarization,” Proc. SPIE 7554, 75541M, 75541M-6 (2010), https://cogrt.bk.tsukuba.ac.jp/COG/locked/yasuno/papers/BiOS2010Proceedings/DATA/7554_57.PDF . [CrossRef]
  50. B. Povazay, B. Hermann, B. Hofer, V. Kajić, E. Simpson, T. Bridgford, and W. Drexler, “Wide-field optical coherence tomography of the choroid in vivo,” Invest. Ophthalmol. Vis. Sci. 50(4), 1856–1863 (2008). [CrossRef] [PubMed]
  51. Y. Yasuno, M. Miura, K. Kawana, S. Makita, M. Sato, F. Okamoto, M. Yamanari, T. Iwasaki, T. Yatagai, and T. Oshika, “Visualization of sub-retinal pigment epithelium morphologies of exudative macular diseases by high-penetration optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 50(1), 405–413 (2008). [CrossRef] [PubMed]

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