Abstract

The embryonic avian heart is an important model for studying cardiac developmental biology. The mechanisms that govern the development of a four-chambered heart from a peristaltic heart tube are largely unknown due in part to a lack of adequate imaging technology. Due to the small size and rapid motion of the living embryonic avian heart, an imaging system with high spatial and temporal resolution is required to study these models. Here, an optical coherence tomography (OCT) system using a buffered Fourier Domain Mode Locked (FDML) laser is applied for ultrahigh-speed non-invasive imaging of embryonic quail hearts at 100,000 axial scans per second. The high scan rate enables the acquisition of high temporal resolution 2D datasets (195 frames per second or 5.12 ms between frames) and 3D datasets (10 volumes per second). Spatio-temporal details of cardiac motion not resolvable using previous OCT technology are analyzed. Visualization and measurement techniques are developed to non-invasively observe and quantify cardiac motion throughout the brief period of systole (less than 50 msec) and diastole. This marks the first time that the preseptated embryonic avian heart has been imaged in 4D without the aid of gating and the first time it has been viewed in cross section during looping with extremely high temporal resolution, enabling the observation of morphological dynamics of the beating heart during systole.

© 2007 Optical Society of America

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2007 (4)

M.W. Jenkins, O.Q. Chughtai, A.N. Basavanhally, M. Watanabe, and A.M. Rollins, "In vivo 4D imaging of the embryonic heart using gated optical coherence tomography," JBO Letters,  12,in press (2007).

M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
[CrossRef]

D.C. Adler, R. Huber, and J.G. Fujimoto, "Phase-sensitive optical coherence tomography at up to 370,000 lines per second using buffered Fourier domain mode-locked lasers," Opt. Lett. 32, 626-628 (2007).
[CrossRef] [PubMed]

A. Mariampillai, B.A. Standish, N.R. Munce, C. Randall, G. Liu, J.Y. Jiang, A.E. Cable, I.A. Vitkin and V.X.D. Yang, "Doppler optical cardiogram gated 2D color flow imaging at 1000 fps and 4D in vivo visualization of embryonic heart at 45 fps on a swept source OCT system," Opt. Express 15, 1627-1638 (2007).
[CrossRef] [PubMed]

2006 (6)

2005 (2)

2004 (2)

D.A. Voronov, P.W. Alford, G. Xu, and L.A. Taber, "The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo," Dev. Biol. 272, 339-350 (2004).
[CrossRef] [PubMed]

N. Nassif, B. Cense, B.E. Bouma, G.J. Tearney, and J.F. de Boer, "In vivo human retinal imaging by ultrahigh-speed spectral domain optical coherence tomography," Opt. Lett. 29, 480-482 (2004).
[CrossRef] [PubMed]

2003 (8)

M. Reckova, C. Rosengarten, A. deAlmeida, C.P. Stanley, A. Wessels, R.G. Gourdie, RP Thompson, and D Sedmera, "Hemodynamics is a key epigenetic factor in development of the cardiac conduction system," Circ. Res. 93, 77-85 (2003).
[CrossRef] [PubMed]

K.E. McGrath, A.D. Koniski, J. Malik, and J. Palis, "Circulation is established in a stepwise pattern in the mammalian embryo," Blood 101, 1669-1676 (2003).
[CrossRef]

R. Leitgeb, C.K. Hitzenberger, and A.F. Fercher, "Performance of fourier domain vs. time domain optical coherence tomography," Opt. Express 11, 889-894 (2003).
[CrossRef] [PubMed]

V.X.D. Yang, M. Gordon, E. Seng-Yue, S. Lo, B. Qi, J Pekar, A. Mok, B. Wilson, and I. Vitkin, "High speed, wide velocity dynamic range Doppler optical coherence tomography (Part II): Imaging in vivo cardiac dynamics of Xenopus laevis," Opt. Express 11, 1650-1658 (2003).
[CrossRef] [PubMed]

J.F. de Boer, B. Cense, B.H. Park, M.C. Pierce, G.J. Tearney, and B.E. Bouma, "Improved signal-to-noise ratio in spectral-domain compared with time-domain optical coherence tomography," Opt. Lett. 28, 2067-2069 (2003).
[CrossRef] [PubMed]

S.H. Yun, G.J. Tearney, J.F. de Boer, N. Iftimia, and B.E. Bouma, "High-speed optical frequency-domain imaging," Opt. Express 11, 2953-2963 (2003).
[CrossRef] [PubMed]

M.A. Choma, M.V. Sarunic, C.H. Yang, and J.A. Izatt, "Sensitivity advantage of swept source and Fourier domain optical coherence tomography," Opt. Express 11, 2183-2189 (2003).
[CrossRef] [PubMed]

P.W. Alford and L.A. Taber, "Regional epicardial strain in the embryonic chick heart during the early looping stages," J. Biomech. 36, 1135-1141 (2003).
[CrossRef] [PubMed]

2002 (3)

T.M. Yelbuz, M.A. Choma, L. Thrane, M.L. Kirby, and J.A. Izatt, "Optical coherence tomography a new high-resolution imaging technology to study cardiac development in chick embryos," Circulation 106, 2771-2774 (2002).
[CrossRef] [PubMed]

J. Rogowska and M.E. Brezinski, "Image processing techniques for noise removal, enhancement and segmentation of cartilage OCT images," Phys. Med. Biol. 47, 641-655 (2002).
[CrossRef] [PubMed]

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A.F. Fercher, "In vivo human retinal imaging by Fourier domain optical coherence tomography," J. Biomed. Opt. 7, 457-463 (2002).
[CrossRef] [PubMed]

2000 (2)

K. Tobita and B.B. Keller, "Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos," Am. J. Physiol. 279, H959-H969 (2000).

K. Tobita and B.B. Keller, "Maturation of end-systolic stress-strain relations in chick embryonic myocardium," Am. J. Physiol. 279, H216-H224 (2000).

1999 (1)

R.A. Robb, "3-D Visualization in Biomedical Applications," Annu. Rev. Biomed. Eng. 1, 377-399 (1999).
[CrossRef]

1998 (1)

G. Hausler and M.W. Linduer, "Coherence radar and spectral radar-new tools for dermatological diagnosis," J. Biomed. Opt. 3, 21-31 (1998).
[CrossRef]

1997 (2)

S.A. Boppart, G.J. Tearney, B.E. Bouma, J.F. Southern, M.E. Brezinski, and J.G. Fujimoto, "Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomograpy," Proc. Natl. Acad. Sci. USA 94, 4256-4261 (1997).
[CrossRef] [PubMed]

B. Golubovic, B.E. Bouma, G.J. Tearney, and J.G. Fujimoto, "Optical frequency-domain reflectometry using rapid wavelength tuning of a Cr4+: forsterite laser," Opt. Lett. 22, 1704-1706 (1997).
[CrossRef]

1996 (1)

J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996).
[CrossRef] [PubMed]

1995 (1)

A.F. Fercher, C.K. Hitzenberger, G. Kamp, and S.Y. Elzaiat, "Measurement of intraocular distances by backscattering spectral interferometry," Opt. Commun. 117, 43-48 (1995).
[CrossRef]

1994 (1)

B.B. Keller, J. Tinney, and N. Hu, "Embryonic ventricular diastolic and systolic pressure-volume relations," Cardiol. Young 4, 19-27 (1994).
[CrossRef]

1992 (1)

F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
[PubMed]

1991 (1)

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

1985 (1)

A. Hirota, K. Kamino, H. Komuro, T. Sakai, and T. Yada, "Optical studies of excitation-contraction coupling in the early embryonic chick heart," J. Physiol. 366, 89-106 (1985).
[PubMed]

1978 (1)

P. Craven and G. Wahba, "Smoothing noisy data with spline functions," Numerische Mathematik 31, 377-403 (1978).
[CrossRef]

1951 (1)

V. Hamburger and H. Hamilton, "Series of Embryonic Chicken Growth," J. Morphology 88, 49-92 (1951).
[CrossRef]

Adler, D.C.

Alford, P.W.

D.A. Voronov, P.W. Alford, G. Xu, and L.A. Taber, "The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo," Dev. Biol. 272, 339-350 (2004).
[CrossRef] [PubMed]

P.W. Alford and L.A. Taber, "Regional epicardial strain in the embryonic chick heart during the early looping stages," J. Biomech. 36, 1135-1141 (2003).
[CrossRef] [PubMed]

Bajraszewski, T.

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A.F. Fercher, "In vivo human retinal imaging by Fourier domain optical coherence tomography," J. Biomed. Opt. 7, 457-463 (2002).
[CrossRef] [PubMed]

Basavanhally, A.N.

M.W. Jenkins, O.Q. Chughtai, A.N. Basavanhally, M. Watanabe, and A.M. Rollins, "In vivo 4D imaging of the embryonic heart using gated optical coherence tomography," JBO Letters,  12,in press (2007).

Boppart, S.A.

W. Luo, D.L. Marks, T.S. Ralston, and S.A. Boppart, "Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system," J. Biomed. Opt. 11, 021014 (2006).
[CrossRef] [PubMed]

S.A. Boppart, G.J. Tearney, B.E. Bouma, J.F. Southern, M.E. Brezinski, and J.G. Fujimoto, "Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomograpy," Proc. Natl. Acad. Sci. USA 94, 4256-4261 (1997).
[CrossRef] [PubMed]

Bouma, B.E.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
[CrossRef] [PubMed]

W.Y. Oh, S.H. Yun, G.J. Tearney, and B.E. Bouma, "115 kHz tuning repetition rate ultrahigh-speed wavelength-swept semiconductor laser," Opt. Lett. 30, 3159-3161 (2006).
[CrossRef]

N. Nassif, B. Cense, B.E. Bouma, G.J. Tearney, and J.F. de Boer, "In vivo human retinal imaging by ultrahigh-speed spectral domain optical coherence tomography," Opt. Lett. 29, 480-482 (2004).
[CrossRef] [PubMed]

S.H. Yun, G.J. Tearney, J.F. de Boer, N. Iftimia, and B.E. Bouma, "High-speed optical frequency-domain imaging," Opt. Express 11, 2953-2963 (2003).
[CrossRef] [PubMed]

J.F. de Boer, B. Cense, B.H. Park, M.C. Pierce, G.J. Tearney, and B.E. Bouma, "Improved signal-to-noise ratio in spectral-domain compared with time-domain optical coherence tomography," Opt. Lett. 28, 2067-2069 (2003).
[CrossRef] [PubMed]

S.A. Boppart, G.J. Tearney, B.E. Bouma, J.F. Southern, M.E. Brezinski, and J.G. Fujimoto, "Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomograpy," Proc. Natl. Acad. Sci. USA 94, 4256-4261 (1997).
[CrossRef] [PubMed]

B. Golubovic, B.E. Bouma, G.J. Tearney, and J.G. Fujimoto, "Optical frequency-domain reflectometry using rapid wavelength tuning of a Cr4+: forsterite laser," Opt. Lett. 22, 1704-1706 (1997).
[CrossRef]

Brezinski, M.E.

J. Rogowska and M.E. Brezinski, "Image processing techniques for noise removal, enhancement and segmentation of cartilage OCT images," Phys. Med. Biol. 47, 641-655 (2002).
[CrossRef] [PubMed]

S.A. Boppart, G.J. Tearney, B.E. Bouma, J.F. Southern, M.E. Brezinski, and J.G. Fujimoto, "Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomograpy," Proc. Natl. Acad. Sci. USA 94, 4256-4261 (1997).
[CrossRef] [PubMed]

Cable, A.E.

Cense, B.

Chan, R.C.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
[CrossRef] [PubMed]

Chang, W

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Charles, R.

F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
[PubMed]

Choma, M.A.

M.A. Choma, M.V. Sarunic, C.H. Yang, and J.A. Izatt, "Sensitivity advantage of swept source and Fourier domain optical coherence tomography," Opt. Express 11, 2183-2189 (2003).
[CrossRef] [PubMed]

T.M. Yelbuz, M.A. Choma, L. Thrane, M.L. Kirby, and J.A. Izatt, "Optical coherence tomography a new high-resolution imaging technology to study cardiac development in chick embryos," Circulation 106, 2771-2774 (2002).
[CrossRef] [PubMed]

Chughtai, O.Q.

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M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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R. Leitgeb, C.K. Hitzenberger, and A.F. Fercher, "Performance of fourier domain vs. time domain optical coherence tomography," Opt. Express 11, 889-894 (2003).
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D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
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M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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M.W. Jenkins, O.Q. Chughtai, A.N. Basavanhally, M. Watanabe, and A.M. Rollins, "In vivo 4D imaging of the embryonic heart using gated optical coherence tomography," JBO Letters,  12,in press (2007).

M.W. Jenkins, F. Rothenberg, D. Roy, Z. Hu, V.P. Nikolski, M. Watanabe, D.L. Wilson, I.R. Efimov, and A.M. Rollins, "4D embryonic cardiography using gated optical coherence tomography," Opt. Express 14, 736-748 (2006).
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Kamino, K.

A. Hirota, K. Kamino, H. Komuro, T. Sakai, and T. Yada, "Optical studies of excitation-contraction coupling in the early embryonic chick heart," J. Physiol. 366, 89-106 (1985).
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A.F. Fercher, C.K. Hitzenberger, G. Kamp, and S.Y. Elzaiat, "Measurement of intraocular distances by backscattering spectral interferometry," Opt. Commun. 117, 43-48 (1995).
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T.M. Yelbuz, M.A. Choma, L. Thrane, M.L. Kirby, and J.A. Izatt, "Optical coherence tomography a new high-resolution imaging technology to study cardiac development in chick embryos," Circulation 106, 2771-2774 (2002).
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A. Hirota, K. Kamino, H. Komuro, T. Sakai, and T. Yada, "Optical studies of excitation-contraction coupling in the early embryonic chick heart," J. Physiol. 366, 89-106 (1985).
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M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A.F. Fercher, "In vivo human retinal imaging by Fourier domain optical coherence tomography," J. Biomed. Opt. 7, 457-463 (2002).
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F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
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R. Leitgeb, C.K. Hitzenberger, and A.F. Fercher, "Performance of fourier domain vs. time domain optical coherence tomography," Opt. Express 11, 889-894 (2003).
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D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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G. Hausler and M.W. Linduer, "Coherence radar and spectral radar-new tools for dermatological diagnosis," J. Biomed. Opt. 3, 21-31 (1998).
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Lo, S.

Luo, W.

W. Luo, D.L. Marks, T.S. Ralston, and S.A. Boppart, "Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system," J. Biomed. Opt. 11, 021014 (2006).
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K.E. McGrath, A.D. Koniski, J. Malik, and J. Palis, "Circulation is established in a stepwise pattern in the mammalian embryo," Blood 101, 1669-1676 (2003).
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Marks, D.L.

W. Luo, D.L. Marks, T.S. Ralston, and S.A. Boppart, "Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system," J. Biomed. Opt. 11, 021014 (2006).
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J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996).
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K.E. McGrath, A.D. Koniski, J. Malik, and J. Palis, "Circulation is established in a stepwise pattern in the mammalian embryo," Blood 101, 1669-1676 (2003).
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J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996).
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Montano, M.M.

M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
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Nassif, N.

Nikolski, V.P.

Nishioka, N.S.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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W.Y. Oh, S.H. Yun, G.J. Tearney, and B.E. Bouma, "115 kHz tuning repetition rate ultrahigh-speed wavelength-swept semiconductor laser," Opt. Lett. 30, 3159-3161 (2006).
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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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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F. de Jong, T. Opthof, A.A. Wilde, M.J. Janse, R. Charles, W.H. Lamers, and A.F. Moorman, "Persisting zones of slow impulse conduction in developing chicken hearts," Circ. Res. 71, 240-250 (1992).
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Palis, J.

K.E. McGrath, A.D. Koniski, J. Malik, and J. Palis, "Circulation is established in a stepwise pattern in the mammalian embryo," Blood 101, 1669-1676 (2003).
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Patel, P.

M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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Pierce, M.C.

Puliafito, CA

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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Ralston, T.S.

W. Luo, D.L. Marks, T.S. Ralston, and S.A. Boppart, "Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system," J. Biomed. Opt. 11, 021014 (2006).
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M. Reckova, C. Rosengarten, A. deAlmeida, C.P. Stanley, A. Wessels, R.G. Gourdie, RP Thompson, and D Sedmera, "Hemodynamics is a key epigenetic factor in development of the cardiac conduction system," Circ. Res. 93, 77-85 (2003).
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M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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M.W. Jenkins, O.Q. Chughtai, A.N. Basavanhally, M. Watanabe, and A.M. Rollins, "In vivo 4D imaging of the embryonic heart using gated optical coherence tomography," JBO Letters,  12,in press (2007).

M.W. Jenkins, F. Rothenberg, D. Roy, Z. Hu, V.P. Nikolski, M. Watanabe, D.L. Wilson, I.R. Efimov, and A.M. Rollins, "4D embryonic cardiography using gated optical coherence tomography," Opt. Express 14, 736-748 (2006).
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M. Reckova, C. Rosengarten, A. deAlmeida, C.P. Stanley, A. Wessels, R.G. Gourdie, RP Thompson, and D Sedmera, "Hemodynamics is a key epigenetic factor in development of the cardiac conduction system," Circ. Res. 93, 77-85 (2003).
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Roy, D.

Sakai, T.

A. Hirota, K. Kamino, H. Komuro, T. Sakai, and T. Yada, "Optical studies of excitation-contraction coupling in the early embryonic chick heart," J. Physiol. 366, 89-106 (1985).
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Schuman, JS

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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Sedmera, D

M. Reckova, C. Rosengarten, A. deAlmeida, C.P. Stanley, A. Wessels, R.G. Gourdie, RP Thompson, and D Sedmera, "Hemodynamics is a key epigenetic factor in development of the cardiac conduction system," Circ. Res. 93, 77-85 (2003).
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Shishkov, M.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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S.A. Boppart, G.J. Tearney, B.E. Bouma, J.F. Southern, M.E. Brezinski, and J.G. Fujimoto, "Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomograpy," Proc. Natl. Acad. Sci. USA 94, 4256-4261 (1997).
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Stanley, C.P.

M. Reckova, C. Rosengarten, A. deAlmeida, C.P. Stanley, A. Wessels, R.G. Gourdie, RP Thompson, and D Sedmera, "Hemodynamics is a key epigenetic factor in development of the cardiac conduction system," Circ. Res. 93, 77-85 (2003).
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Stinson, WG

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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Suter, M.J.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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Swanson, E.A.

D. Huang, E.A. Swanson, C.P. Lin, JS Schuman, WG Stinson, W Chang, MR Hee, T Flotte, K Gregory, CA Puliafito, and JG Fujimoto, "Optical Coherence Tomography," Science 254, 1178-1181 (1991).
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W.Y. Oh, S.H. Yun, G.J. Tearney, and B.E. Bouma, "115 kHz tuning repetition rate ultrahigh-speed wavelength-swept semiconductor laser," Opt. Lett. 30, 3159-3161 (2006).
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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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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Vakoc, B.J.

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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M.W. Jenkins, P. Patel, H. Deng, M.M. Montano, M. Watanabe, and A.M. Rollins, "Phenotyping transgenic embryonic murine hearts using optical coherence tomography," App. Opt. 46, 1776-1781 (2007).
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M.W. Jenkins, O.Q. Chughtai, A.N. Basavanhally, M. Watanabe, and A.M. Rollins, "In vivo 4D imaging of the embryonic heart using gated optical coherence tomography," JBO Letters,  12,in press (2007).

Nature Medicine (1)

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. Jang, N.S. Nishioka, J.F. de Boer, and B.E. Bouma, "Comprehensive volumetric optical microscopy in vivo," Nature Medicine 12, 1429-1433 (2006).
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Supplementary Material (7)

» Media 1: AVI (2475 KB)     
» Media 2: AVI (367 KB)     
» Media 3: AVI (2456 KB)     
» Media 4: AVI (2294 KB)     
» Media 5: AVI (2488 KB)     
» Media 6: AVI (2441 KB)     
» Media 7: AVI (2343 KB)     

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Figures (9)

Fig. 1.
Fig. 1.

Setup for imaging embryonic quail hearts The embryos were placed on a heating pad situated underneath the sample arm of the OCT system. The heating pad was set to 37 °C and a strip of Parafilm was placed over the Petri dish with a small hole cut out at the location of the heart.

Fig. 2
Fig. 2

(2.36 MB) Sum voxel projection of a beating stage 14 quail heart. The heart tube is clearly visible and the inner lumen of the heart can be seen filling and ejecting blood. The arrows point in the direction of blood flow. Vent - ventricle [Media 1]

Fig. 3
Fig. 3

(544 KB) Top view (ventral) of a beating stage 14 quail heart. A 3D Sobel mask was applied to the data volume corresponding to each phase of the cardiac cycle. Interaction between the heart tube and the surrounding tissue can be clearly visualized. Vent - ventricle [Media 2]

Fig. 4
Fig. 4

(2.47 MB) Beating and rotating heart inside the embryonic volume of stage 14 quail. A cut-away operation is performed as the heart beats to enable visualization of internal structures. [Media 3]

Fig. 5.
Fig. 5.

(2.36 MB) Beating 2D slices from different orthogonal orientations of a stage 14 quail heart. Along the top row (A-C) are three different 2D slices sagittal to the body of the embryo. The 3D reconstruction to the right (D) shows the location of the three slices as planes cutting through the heart. The planes from top to bottom correspond to the images starting from the left and moving right. The middle row (E-G) represents three 2D slices cut coronal to the body of the embryo. The 3D reconstruction (H) of the heart to the right marks the left to right images as planes going from front to back in the image. The bottom row (I-K) shows three 2D slices of the heart cut transverse to the body of the embryo. The 3D reconstruction (L) to the right marks the left to right images as planes going from left to right in the image. White arrows point to the location of possible tethers connecting the endocardium to the myocardium. The green arrowheads point to asymmetry in the cardiac wall. The scale bar in F corresponds to all 2D slices, while the scale bar in L corresponds all 3D reconstructions. [Media 4]

Fig. 6.
Fig. 6.

Time series of coronal sections through the same location of two quail hearts using ultrahigh-speed OCT. A-C (2.29 MB) stage 10–12 from the same quail embryo, D-F (2.42 MB) stage 13–15 from a different quail embryo, same orientation and location. All images are oriented such that the inflow region is on the right, and the outflow tract is on the left. Blood flow was, therefore, right to left. (A-C) The playback rate of the movies has been slowed to ~1/7th the original speed. Stage 10–12: Heart was a single midline tube, looping not yet evident in panel A. Peristaltic contraction leading to forward flow of blood (to the left) was observed in all three panels. The sinus venosus does not contract, but blood flow is observed during systole. Individual red blood cells were observed in the earliest stages of development, with apparent increase in number as the embryo developed. The cardiac jelly had rare cellular content, and the endocardium appeared smooth throughout systole and diastole in these 2D + time movies. The heart showed symmetric contraction at stage 10. By stage 11, a shallow bend appeared on the dorsal aspect of the heart tube, more evident during systole, and more prominent at stage 12. The heart tube is distinctly asymmetric at stage 12 during systole and diastole. [Media 5] (D-F) Stage 13–15: A stricture formed separating the inflow and outflow regions into rapidly (inflow) and slowly (outflow) contracting myocardium. During systole, small wrinkles in the endocardial lining were observed extending outward to the myocardium. These bands became more prominent as the heart developed. Erythrocytes filled the cardiac chamber, and the heart rate appeared to increase. Contraction appears to be moving toward pulsatile flow. White arrows point to the location of possible tethers connecting the endocardium to the myocardium. Myo – myocardium, SV – sinus venosus, CJ – cardiac jelly, EC – endocardium, In – inflow and Out - outflow [Media 6]

Fig. 7.
Fig. 7.

Histologic sections through a stage 11 embryonic quail heart (A and B - same section) and a stage 13 heart, (panels C and D – same section) are shown. A and C were immunohistochemically labeled with anti-myosin antibody MF20 (green) that label striated muscle. B and D are images taken with Hoffman Optics of the same sections in A and C, performed to demonstrate the appearance of the myocardium relative to the endocardium. Tethers connect the endocardium (arrows) to the myocardium (arrowheads). The dotted outline shows tissue folding, an artifact of the histological process. Myo – myocardium, CJ – cardiac jelly and EC – endocardium

Fig. 8.
Fig. 8.

Heart tube diameter, wall displacement velocity and CWPV measurements were computed from a 2D + time coronal dataset. (A) Line positions for the proximal end of the heart tube, (B) normalized tube diameter versus time (C) wall displacement velocity versus time, (D) Line positions for the distal end of the heart tube, (E) normalized tube diameter versus time, and (F) wall displacement velocity versus time.

Fig 9
Fig 9

(2.06 MB). Movie showing the effects of high and low temporal sampling rate on the visualization of heart dynamics. A higher temporal sampling rate allows for the visualization of the fast systolic kick, which is missed in the case of lower temporal sampling. In – inflow and Out - outflow [Media 7]

Tables (1)

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Table 1. Maximum Displacement Error

Equations (1)

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MDE = ( L R ) * V ,

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