Abstract

Myofiber organization in cardiac muscle plays an important role in achieving normal mechanical and electrical heart functions. An imaging tool that can reveal microstructural details of myofiber organization is valuable for both basic research and clinical applications. A high-resolution optical polarization tractography (OPT) was recently developed based on Jones matrix optical coherence tomography (JMOCT). In this study, we validated the accuracy of using OPT for measuring depth-resolved fiber orientation in fresh heart samples by comparing directly with histology images. Systematic image processing algorithms were developed to register OPT with histology images. The pixel-wise differences between the two tractographic results were analyzed in details. The results indicate that OPT can accurately image depth-resolved fiber orientation in fresh heart tissues and reveal microstructural details at the histological level.

© 2014 Optical Society of America

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2013

2012

2010

2009

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson.11(1), 47 (2009).
[CrossRef] [PubMed]

2008

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt.13(3), 030505 (2008).
[CrossRef] [PubMed]

2005

2004

2003

G. K. Rohde, A. Aldroubi, and B. M. Dawant, “The adaptive bases algorithm for intensity-based nonrigid image registration,” IEEE Trans. Med. Imaging22(11), 1470–1479 (2003).
[CrossRef] [PubMed]

1998

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

1995

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

1994

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

1969

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Aldroubi, A.

G. K. Rohde, A. Aldroubi, and B. M. Dawant, “The adaptive bases algorithm for intensity-based nonrigid image registration,” IEEE Trans. Med. Imaging22(11), 1470–1479 (2003).
[CrossRef] [PubMed]

Ambrosi, C. M.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt.17(7), 071309 (2012).
[CrossRef] [PubMed]

Baruffi, S.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Blankesteijn, W. M.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Bouts, A.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Cense, B.

Chai, L. Z.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Covell, J. W.

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

Dai, G.

D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson.11(1), 47 (2009).
[CrossRef] [PubMed]

Dawant, B. M.

G. K. Rohde, A. Aldroubi, and B. M. Dawant, “The adaptive bases algorithm for intensity-based nonrigid image registration,” IEEE Trans. Med. Imaging22(11), 1470–1479 (2003).
[CrossRef] [PubMed]

de Boer, J. F.

Edgar, S. G.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Efimov, I. R.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt.17(7), 071309 (2012).
[CrossRef] [PubMed]

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt.13(3), 030505 (2008).
[CrossRef] [PubMed]

Ershler, P. R.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Fan, C.

Fedorov, V. V.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt.17(7), 071309 (2012).
[CrossRef] [PubMed]

Fleming, C. P.

Y. Gan and C. P. Fleming, “Extracting three-dimensional orientation and tractography of myofibers using optical coherence tomography,” Biomed. Opt. Express4(10), 2150–2165 (2013).
[CrossRef] [PubMed]

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt.13(3), 030505 (2008).
[CrossRef] [PubMed]

Gan, Y.

Gavin, J. B.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Goergen, C. J.

Grulkowski, I.

Heijman, E.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Henriquez, C. S.

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

Hsu, E. W.

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

Hunter, J. J.

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

Hunter, P. J.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Izatt, J. A.

Jiao, S.

Karlon, W. J.

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

Kléber, A. G.

A. G. Kléber and Y. Rudy, “Basic Mechanisms of Cardiac Impulse Propagation and Associated arrhythmias,” Physiol. Rev.84(2), 431–488 (2004).
[CrossRef] [PubMed]

Kuo, A. N.

LeGrice, I. J.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Lo, E. H.

Lux, R. L.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Macchi, E.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Makita, S.

Mandeville, E. T.

Marcos, S.

Matulevicius, S. A.

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

McCulloch, A. D.

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

Muzikant, A. L.

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

Nicolay, K.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Omens, J. H.

W. J. Karlon, J. W. Covell, A. D. McCulloch, J. J. Hunter, and J. H. Omens, “Automated measurement of myofiber disarray in transgenic mice with ventricular expression of ras,” Anat. Rec.252(4), 612–625 (1998).
[CrossRef] [PubMed]

Ortiz, S.

Park, B. H.

Pascual, D.

Patel, D. P.

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Peeters, T. H.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Penland, R. C.

E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez, “Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation,” Am. J. Physiol.274(5 Pt 2), H1627–H1634 (1998).
[PubMed]

Pierce, M. C.

Radhakrishnan, H.

Reese, T. G.

D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson.11(1), 47 (2009).
[CrossRef] [PubMed]

Remon, L.

Ripplinger, C. M.

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt.13(3), 030505 (2008).
[CrossRef] [PubMed]

Rohde, G. K.

G. K. Rohde, A. Aldroubi, and B. M. Dawant, “The adaptive bases algorithm for intensity-based nonrigid image registration,” IEEE Trans. Med. Imaging22(11), 1470–1479 (2003).
[CrossRef] [PubMed]

Rollins, A. M.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt.17(7), 071309 (2012).
[CrossRef] [PubMed]

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt.13(3), 030505 (2008).
[CrossRef] [PubMed]

Ross, J.

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Rudy, Y.

A. G. Kléber and Y. Rudy, “Basic Mechanisms of Cardiac Impulse Propagation and Associated arrhythmias,” Physiol. Rev.84(2), 431–488 (2004).
[CrossRef] [PubMed]

Sakadžic, S.

Sanders, H. M.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Schuessler, R. B.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt.17(7), 071309 (2012).
[CrossRef] [PubMed]

Siedlecki, D.

Smaill, B. H.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol.-Heart. C.269(2 38–2), 571–582 (1995).

Sonnenblick, E. H.

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Sosnovik, D. E.

Spaggiari, S.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Spotnitz, H. M.

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Srinivasan, V. J.

Stoica, G.

Streeter, D. D.

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber orientation in the canine left ventricle during diastole and systole,” Circ. Res.24(3), 339–347 (1969).
[CrossRef] [PubMed]

Strijkers, G. J.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Taccardi, B.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation90(6), 3076–3090 (1994).
[CrossRef] [PubMed]

Todorovic, M.

van Prooijen, M. C.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Vilanova, A.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. Peeters, A. Vilanova, M. C. van Prooijen, H. M. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed.22(2), 182–190 (2009).
[CrossRef] [PubMed]

Vyhmeister, Y.

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D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson.11(1), 47 (2009).
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Figures (8)

Fig. 1
Fig. 1

An illustration of image distortion induced by surface refraction. The incident light (A-scan) is aligned with the z-axis. (N) is the surface normal vector at the light incidence point. The en face x-y plane formed by the B- and C-scan are equivalent to the histology sectioning plane. The incident light is deviated by Δθ within the incident plane (formed by the incident light and the surface normal vector) due to optical refraction at the sample surface.

Fig. 2
Fig. 2

(a) The 3D OCT intensity images obtained in a piece of heart tissue. The example en face images of (b) intensity (I), (c) local retardation (δ), (d) local diattenuation (σ), and (e) local optical axis (θ) extracted at a depth of 0.56 mm from surface. (f) A tractographic representation of fiber orientation using the streamline plot. The size bars in the images represent 0.5 mm.

Fig. 3
Fig. 3

An example of the surface refraction correction. (a) The histology image obtained at 0.35 mm beneath the epicardium surface. (b) The tractographic result obtained from the histology image. (c) The OPT result without correcting the surface refraction. (d) The OPT after surface refraction correction. The corresponding distribution of pixel-by-pixel difference between histology and OPT before and after correction are shown in (e) and (f), respectively.

Fig. 4
Fig. 4

A direct comparison of the depth-resolved myocardial fiber orientation measured from histology and OPT. The three ROIs were selected from the heart sample as shown in (a). The size of the ROI is 92 × 92 µm2. Error bars indicate standard deviation.

Fig. 5
Fig. 5

(a) The linear correlation between OPT and histology results (R2 = 0.85). (b) The distribution of the difference between the fiber orientation angles measured using OPT and histology. The data represented depth-resolved orientation (Fig. 4) measured from a total of 21 ROIs selected from the heart samples in 7 mice. The red dashed line in (b) represents a Gaussian fitting.

Fig. 6
Fig. 6

An example comparison of tractography computed using OPT and histology at depths of 0.34 mm and 0.66 mm from the epicardium in a heart tissue sample. The corresponding tractography was overlaid over the histology and OCT intensity images, respectively. Also shown are the corresponding distributions of the pixel-by-pixel orientation difference, in which the dashed lines were fitting results using a Gaussian function. The white dashed boxes highlight the difference between histology and OPT. The size bar indicates 100 μm.

Fig. 7
Fig. 7

(a) The potential misalignment between the histology sectioning plane and en face OCT scanning plane. (b) The histology tractography and (c) OPT in a tissue sample located at 0.34 mm beneath the epicardium. (d) OPT results of the same tissue region with the en face plane tilted 2.0°. (e) The high resolution histology tractography and (f) OPT in a tissue region with intensity variations.

Fig. 8
Fig. 8

A comparison of the (a) histology tractography and (b) OPT in a tissue sample with a significant amount of orientation changes and tissue deformation caused by histology processing. The corresponding tractography results were overlaid over the histology and OCT intensity images, respectively.

Equations (5)

Equations on this page are rendered with MathJax. Learn more.

G(i,j)= G x 2 (i,j)+ G y 2 (i,j) ϕ(i,j)= tan 1 G y (i,j) G x (i,j)
θ= tan 1 N x 2 + N y 2 N z . ϕ= tan 1 N y N x
x'=x+zsinΔθcosϕ y'=y+zsinΔθsinϕ, z'=zcosΔθ
Δθ=θ sin 1 ( sinθ n ).
β'= tan 1 ( cosΔθcosφsinβsinφcosβ cosΔθsinφsinβ+cosφcosβ ),

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