Abstract

Progress toward understanding embryonic heart development has been hampered by the inability to image embryonic heart structure and simultaneously measure blood flow dynamics in vivo. We have developed a spectral domain optical coherence tomography system for in vivo volumetric imaging of the chicken embryo heart. We have also developed a technique called spectral Doppler velocimetry (SDV) for quantitative measurement of blood flow dynamics. We present in vivo volume images of the embryonic heart from initial tube formation to development of endocardial cushions of the same embryo over several stages of development. SDV measurements reveal the influence of heart tube structure on blood flow dynamics.

© 2008 Optical Society of America

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    [CrossRef] [PubMed]
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2008

J. Manner, L. Thrane, K. Norozi, and T. M. Yelbuz, “High-resolution in vivo imaging of the cross-sectional deformations of contracting embryonic heart loops using optical coherence tomography,” Dev. Dyn. 237, 953-961 (2008).
[CrossRef] [PubMed]

N. V. Iftimia, D. X. Hammer, R. P. Ferguson, M. Mujat, D. Vu, and A. A. Ferrante, “Dual-beam Fourier domain optical Doppler tomography of zebrafish,” Opt. Express 16, 13624-13636 (2008).
[CrossRef] [PubMed]

2007

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]

M. W. Jenkins, D. C. Adler, M. Gargesha, R. Huber, F. Rothenberg, J. Belding, M. Watanabe, D. L. Wilson, J. G. Fujimoto, and A. M. Rollins, “Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier domain mode locked laser,” Opt. Express 15, 6251-6267 (2007).
[CrossRef] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12, 041215 (2007).
[CrossRef] [PubMed]

J. T. Butcher, T. C. McQuinn, D. Sedmera, D. Turner, and R. R. Markwald, “Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition,” Circ. Res. 100, 1503-1511 (2007).
[CrossRef] [PubMed]

K. K. Linask and M. Vanauker, “A role for the cytoskeleton in heart looping,” ScientificWorldJournal 7, 280-298 (2007).
[CrossRef] [PubMed]

L. A. Taber, J. Zhang, and R. Perucchio, “Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube,” J. Biomech. Eng. 129, 441-449 (2007).
[CrossRef] [PubMed]

T. C. McQuinn, M. Bratoeva, A. DeAlmeida, M. Remond, R. P. Thompson, and D. Sedmera, “High-frequency ultrasonographic imaging of avian cardiovascular development,” Dev. Dyn. 236, 3503-3513 (2007).
[CrossRef] [PubMed]

2006

P. Vennemann, K. T. Kiger, R. Lindken, B. C. W. Groenendijk, S. Stekelenburg-de Vos, T. L. M. ten Hugen, N. T. C. Ursem, R. E. Poelmann, J. Westerweel, and B. P. Hierck, “In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart,” J. Biomech. 39, 1191-1200 (2006).
[CrossRef]

R. S. Reneman, T. Arts, and A. P. Hoeks, “Wall shear stress--an important determinant of endothelial cell function and structure--in the arterial system in vivo. Discrepancies with theory,” J. Vasc. Res. 43, 251-269 (2006).
[CrossRef] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

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]

M. W. Jenkins, F. Rothenberg, D. Roy, V. P. Nikolski, Z. Hu, 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).
[CrossRef] [PubMed]

R. Huber, D. C. Adler, and J. G. Fujimoto, “Buffered Fourier domain mode locking: unidirectional swept laser sources for optical coherence tomography imaging at 370,000 lines/s,” Opt. Lett. 31, 2975-2977 (2006).
[CrossRef] [PubMed]

2005

B. C. W. Groenendijk, B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo,” Circ. Res. 96, 1291-1298 (2005).
[CrossRef] [PubMed]

B. J. Martinsen, “Reference guide to the stages of chick heart embryology,” Dev. Dyn. 233, 1217-1237 (2005).
[CrossRef] [PubMed]

A. D. Person, S. E. Klewer, and R. B. Runyan, “Cell biology of cardiac cushion development,” Int. Rev. Cytol. 243, 287-335 (2005).
[CrossRef] [PubMed]

C. T. Badea, B. Fubara, L. W. Hedlund, and G. A. Johnson, 4-D micro-CT of the mouse heart,” Mol. Imaging 4, 110-116 (2005).
[PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[CrossRef] [PubMed]

2004

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
[CrossRef] [PubMed]

W. W. Burggren, “What is the purpose of the embryonic heart beat? Or how facts can ultimately prevail over physiological dogma,” Physiol. Biochem. Zool. 77, 333-345 (2004).
[CrossRef] [PubMed]

L. Wang, Y. Wang, S. Guo, J. Zhang, M. Bachman, G. P. Li, and Z. Chen, “Frequency domain phase-resolved optical Doppler and Doppler variance tomography,” Opt. Commun. 242, 345-350 (2004).
[CrossRef]

2003

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
[CrossRef] [PubMed]

X. Zhang, T. M. Yelbuz, G. P. Kofer, M. A. Choma, M. L. Kirby, and G. A. Johnson, “Improved preparation of chick embryonic samples for magnetic resonance microscopy,” Magn. Reson. Med. 49, 1192-1195 (2003).
[CrossRef] [PubMed]

T. M. Yelbuz, X. Zhang, M. A. Choma, H. A. Stadt, M. Zdlanowicz, G. A. Johnson, and M. L. Kirby, “Approaching cardiac development in three dimensions by magnetic resonance microscopy,” Circulation 108, e154-e155 (2003).
[CrossRef] [PubMed]

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]

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]

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, 3116-3121 (2003).
[CrossRef] [PubMed]

S. H. Yun, G. Tearney, B. Bouma, B. Park, and J. de Boer, “High-speed spectral-domain optical coherence tomography at 1.3 μm wavelength,” Opt. Express 11, 3598-3604 (2003).
[CrossRef] [PubMed]

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

2002

F. S. Foster, M. Y. Zhang, Y. Q. Zhou, G. Liu, J. Mehi, E. Cherin, K. A. Harasiewicz, B. G. Starkoski, L. Zan, D. A. Knapik, and S. L. Adamson, “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound Med. Biol. 28, 1165-1172 (2002).
[CrossRef] [PubMed]

C. K. Phoon, O. Aristizabal, and D. H. Turnbull, “Spatial velocity profile in mouse embryonic aorta and Doppler-derived volumetric flow: a preliminary model,” Am. J. Physiol. Heart Circ. Physiol. 283, H908-H916 (2002).
[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]

2001

S. Radhakrishnan, A. M. Rollins, J. E. Roth, S. Yazdanfar, V. Westphal, D. S. Bardenstein, and J. A. Izatt, “Real-time optical coherence tomography of the anterior segment at 1310 nm,” Arch. Ophthalmol. (Chicago) 119, 1179-1185 (2001).

2000

K. Tobita and B. B. Keller, “Maturation of end-systolic stress-strain relations in chick embryonic myocardium,” Am. J. Physiol. Heart Circ. Physiol. 279, H216-H224 (2000).
[PubMed]

J. Männer, “Cardiac looping in the chick embryo: a morphological review with special reference to terminological and biomechanical aspects of the looping process,” Anat. Rec. 259, 248-262 (2000).
[CrossRef] [PubMed]

M. J. Paulus, S. S. Gleason, S. J. Kennel, P. R. Hunsicker, and D. K. Johnson, “High resolution x-ray computed tomography: an emerging tool for small animal cancer research,” Neoplasia 2, 62-70 (2000).
[CrossRef] [PubMed]

C. K. Phoon, O. Aristizabal, and D. H. Turnbull, “40 MHz Doppler characterization of umbilical and dorsal aortic blood flow in the early mouse embryo,” Ultrasound Med. Biol. 26, 1275-1283 (2000).
[CrossRef] [PubMed]

1999

B. Hogers, M. C. De Ruiter, A. C. Gittenberger-de Goot, and R. E. Poelmann, “Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal,” Cardiovasc. Res. 41, 87-99 (1999).
[CrossRef] [PubMed]

T. G. van Leeuwen, M. D. Kulkarni, S. Yazdanfar, A. M. Rollins, and J. A. Izatt, “High-flow-velocity and shear-rate imaging by use of color Doppler optical coherence tomography,” Opt. Lett. 24, 1584-1586 (1999).
[CrossRef]

1997

S. Yazdanfar, M. D. Kulkarni, and J. A. Izatt, “High resolution imaging of in vivo cardiac dynamics using color Doppler optical coherence tomography,” Opt. Express 1, 424-431 (1997).
[CrossRef] [PubMed]

Z. Chen, T. E. Milner, S. Srinivas, X. Wang, A. Malekafzali, M. J. C. Van Gemart, and J. S. Nelson, “Noninvasive imaging of in vivo blood flow velocity using optical Doppler tomography,” Opt. Lett. 22, 1119-1121 (1997).
[CrossRef] [PubMed]

M. C. Fishman and K. R. Chien, “Fashioning the vertebrate heart: earliest embryonic decisions,” Development 124, 2099-2117 (1997).
[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 tomography,” Proc. Natl. Acad. Sci. U.S.A. 94, 4256-4261 (1997).
[CrossRef] [PubMed]

1995

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

1993

D. W. Holdsworth, M. Drangova, and A. Fenster, “A high-resolution XRII-based quantitative volume CT scanner,” Med. Phys. 20, 449-462 (1993).
[CrossRef] [PubMed]

1991

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

1989

N. Hu and E. B. Clark, “Hemodynamics of the stage 12 to stage 29 chick embryo,” Circ. Res. 65, 1665-1670 (1989).
[PubMed]

1987

1951

V. Hamburger and H. L. Hamilton, “A series of normal stages in the development of the chick embryo,” J. Morphol. 88, 49-92 (1951).
[CrossRef]

Acevando-Bolton, G.

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
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F. S. Foster, M. Y. Zhang, Y. Q. Zhou, G. Liu, J. Mehi, E. Cherin, K. A. Harasiewicz, B. G. Starkoski, L. Zan, D. A. Knapik, and S. L. Adamson, “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound Med. Biol. 28, 1165-1172 (2002).
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Aristizabal, O.

C. K. Phoon, O. Aristizabal, and D. H. Turnbull, “Spatial velocity profile in mouse embryonic aorta and Doppler-derived volumetric flow: a preliminary model,” Am. J. Physiol. Heart Circ. Physiol. 283, H908-H916 (2002).
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C. K. Phoon, O. Aristizabal, and D. H. Turnbull, “40 MHz Doppler characterization of umbilical and dorsal aortic blood flow in the early mouse embryo,” Ultrasound Med. Biol. 26, 1275-1283 (2000).
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Arts, T.

R. S. Reneman, T. Arts, and A. P. Hoeks, “Wall shear stress--an important determinant of endothelial cell function and structure--in the arterial system in vivo. Discrepancies with theory,” J. Vasc. Res. 43, 251-269 (2006).
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Bachman, M.

L. Wang, Y. Wang, S. Guo, J. Zhang, M. Bachman, G. P. Li, and Z. Chen, “Frequency domain phase-resolved optical Doppler and Doppler variance tomography,” Opt. Commun. 242, 345-350 (2004).
[CrossRef]

Badea, C. T.

C. T. Badea, B. Fubara, L. W. Hedlund, and G. A. Johnson, 4-D micro-CT of the mouse heart,” Mol. Imaging 4, 110-116 (2005).
[PubMed]

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B. C. W. Groenendijk, B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo,” Circ. Res. 96, 1291-1298 (2005).
[CrossRef] [PubMed]

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Bardenstein, D. S.

S. Radhakrishnan, A. M. Rollins, J. E. Roth, S. Yazdanfar, V. Westphal, D. S. Bardenstein, and J. A. Izatt, “Real-time optical coherence tomography of the anterior segment at 1310 nm,” Arch. Ophthalmol. (Chicago) 119, 1179-1185 (2001).

Belding, J.

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).
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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 tomography,” Proc. Natl. Acad. Sci. U.S.A. 94, 4256-4261 (1997).
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Bouma, B. E.

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).
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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 tomography,” Proc. Natl. Acad. Sci. U.S.A. 94, 4256-4261 (1997).
[CrossRef] [PubMed]

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Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12, 041215 (2007).
[CrossRef] [PubMed]

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T. C. McQuinn, M. Bratoeva, A. DeAlmeida, M. Remond, R. P. Thompson, and D. Sedmera, “High-frequency ultrasonographic imaging of avian cardiovascular development,” Dev. Dyn. 236, 3503-3513 (2007).
[CrossRef] [PubMed]

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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 tomography,” Proc. Natl. Acad. Sci. U.S.A. 94, 4256-4261 (1997).
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W. W. Burggren, “What is the purpose of the embryonic heart beat? Or how facts can ultimately prevail over physiological dogma,” Physiol. Biochem. Zool. 77, 333-345 (2004).
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J. T. Butcher, T. C. McQuinn, D. Sedmera, D. Turner, and R. R. Markwald, “Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition,” Circ. Res. 100, 1503-1511 (2007).
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Cense, B.

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Chen, Z.

L. Wang, Y. Wang, S. Guo, J. Zhang, M. Bachman, G. P. Li, and Z. Chen, “Frequency domain phase-resolved optical Doppler and Doppler variance tomography,” Opt. Commun. 242, 345-350 (2004).
[CrossRef]

Z. Chen, T. E. Milner, S. Srinivas, X. Wang, A. Malekafzali, M. J. C. Van Gemart, and J. S. Nelson, “Noninvasive imaging of in vivo blood flow velocity using optical Doppler tomography,” Opt. Lett. 22, 1119-1121 (1997).
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F. S. Foster, M. Y. Zhang, Y. Q. Zhou, G. Liu, J. Mehi, E. Cherin, K. A. Harasiewicz, B. G. Starkoski, L. Zan, D. A. Knapik, and S. L. Adamson, “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound Med. Biol. 28, 1165-1172 (2002).
[CrossRef] [PubMed]

Chien, K. R.

M. C. Fishman and K. R. Chien, “Fashioning the vertebrate heart: earliest embryonic decisions,” Development 124, 2099-2117 (1997).
[PubMed]

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X. Zhang, T. M. Yelbuz, G. P. Kofer, M. A. Choma, M. L. Kirby, and G. A. Johnson, “Improved preparation of chick embryonic samples for magnetic resonance microscopy,” Magn. Reson. Med. 49, 1192-1195 (2003).
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M. A. Choma, M. Sarunic, C. Yang, and J. Izatt, “Sensitivity advantage of swept-source and Fourier-domain optical coherence tomography,” Opt. Express 11, 2183-2189 (2003).
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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).
[CrossRef] [PubMed]

Clark, E. B.

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
[CrossRef] [PubMed]

N. Hu and E. B. Clark, “Hemodynamics of the stage 12 to stage 29 chick embryo,” Circ. Res. 65, 1665-1670 (1989).
[PubMed]

Davis, A. M.

A. M. Davis, J. A. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (to be published).

de Boer, J.

de Boer, J. F.

De Ruiter, M. C.

B. Hogers, M. C. De Ruiter, A. C. Gittenberger-de Goot, and R. E. Poelmann, “Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal,” Cardiovasc. Res. 41, 87-99 (1999).
[CrossRef] [PubMed]

DeAlmeida, A.

T. C. McQuinn, M. Bratoeva, A. DeAlmeida, M. Remond, R. P. Thompson, and D. Sedmera, “High-frequency ultrasonographic imaging of avian cardiovascular development,” Dev. Dyn. 236, 3503-3513 (2007).
[CrossRef] [PubMed]

Dickinson, M. E.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[CrossRef] [PubMed]

Drangova, M.

D. W. Holdsworth, M. Drangova, and A. Fenster, “A high-resolution XRII-based quantitative volume CT scanner,” Med. Phys. 20, 449-462 (1993).
[CrossRef] [PubMed]

Drexler, W.

Efimov, I. R.

El-Zaiat, S. Y.

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

Fenster, A.

D. W. Holdsworth, M. Drangova, and A. Fenster, “A high-resolution XRII-based quantitative volume CT scanner,” Med. Phys. 20, 449-462 (1993).
[CrossRef] [PubMed]

Fercher, A.

Fercher, A. F.

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]

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

Ferguson, R. P.

Ferrante, A. A.

Fishman, M. C.

M. C. Fishman and K. R. Chien, “Fashioning the vertebrate heart: earliest embryonic decisions,” Development 124, 2099-2117 (1997).
[PubMed]

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Forouhar, A. S.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[CrossRef] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
[CrossRef] [PubMed]

Foster, F. S.

F. S. Foster, M. Y. Zhang, Y. Q. Zhou, G. Liu, J. Mehi, E. Cherin, K. A. Harasiewicz, B. G. Starkoski, L. Zan, D. A. Knapik, and S. L. Adamson, “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound Med. Biol. 28, 1165-1172 (2002).
[CrossRef] [PubMed]

Fraser, S. E.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[CrossRef] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
[CrossRef] [PubMed]

Fubara, B.

C. T. Badea, B. Fubara, L. W. Hedlund, and G. A. Johnson, 4-D micro-CT of the mouse heart,” Mol. Imaging 4, 110-116 (2005).
[PubMed]

Fujimoto, J. G.

M. W. Jenkins, D. C. Adler, M. Gargesha, R. Huber, F. Rothenberg, J. Belding, M. Watanabe, D. L. Wilson, J. G. Fujimoto, and A. M. Rollins, “Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier domain mode locked laser,” Opt. Express 15, 6251-6267 (2007).
[CrossRef] [PubMed]

R. Huber, D. C. Adler, and J. G. Fujimoto, “Buffered Fourier domain mode locking: unidirectional swept laser sources for optical coherence tomography imaging at 370,000 lines/s,” Opt. Lett. 31, 2975-2977 (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 tomography,” Proc. Natl. Acad. Sci. U.S.A. 94, 4256-4261 (1997).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Gargesha, M.

Gharib, M.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[CrossRef] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
[CrossRef] [PubMed]

Ghiglia, D. C.

D. C. Ghiglia, G. A. Mastin, and L. A. Romero, “Cellular-automata method for phase unwrapping,” J. Opt. Soc. Am. A 4, 267-280 (1987).
[CrossRef]

D. C. Ghiglia and M. D. Pritt, Two Dimensional Phase Unwrapping, Theory, Algorithms, and Software (Wiley, 1998).

Gittenberger-de Goot, A. C.

B. Hogers, M. C. De Ruiter, A. C. Gittenberger-de Goot, and R. E. Poelmann, “Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal,” Cardiovasc. Res. 41, 87-99 (1999).
[CrossRef] [PubMed]

Gittenberger-de Groot, A. C.

B. C. W. Groenendijk, B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo,” Circ. Res. 96, 1291-1298 (2005).
[CrossRef] [PubMed]

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
[CrossRef] [PubMed]

Gleason, S. S.

M. J. Paulus, S. S. Gleason, S. J. Kennel, P. R. Hunsicker, and D. K. Johnson, “High resolution x-ray computed tomography: an emerging tool for small animal cancer research,” Neoplasia 2, 62-70 (2000).
[CrossRef] [PubMed]

Gregory, K.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Groenendijk, B. C. W.

P. Vennemann, K. T. Kiger, R. Lindken, B. C. W. Groenendijk, S. Stekelenburg-de Vos, T. L. M. ten Hugen, N. T. C. Ursem, R. E. Poelmann, J. Westerweel, and B. P. Hierck, “In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart,” J. Biomech. 39, 1191-1200 (2006).
[CrossRef]

B. C. W. Groenendijk, B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo,” Circ. Res. 96, 1291-1298 (2005).
[CrossRef] [PubMed]

Guo, S.

L. Wang, Y. Wang, S. Guo, J. Zhang, M. Bachman, G. P. Li, and Z. Chen, “Frequency domain phase-resolved optical Doppler and Doppler variance tomography,” Opt. Commun. 242, 345-350 (2004).
[CrossRef]

Hamburger, V.

V. Hamburger and H. L. Hamilton, “A series of normal stages in the development of the chick embryo,” J. Morphol. 88, 49-92 (1951).
[CrossRef]

Hamilton, H. L.

V. Hamburger and H. L. Hamilton, “A series of normal stages in the development of the chick embryo,” J. Morphol. 88, 49-92 (1951).
[CrossRef]

Hammer, D. X.

Harasiewicz, K. A.

F. S. Foster, M. Y. Zhang, Y. Q. Zhou, G. Liu, J. Mehi, E. Cherin, K. A. Harasiewicz, B. G. Starkoski, L. Zan, D. A. Knapik, and S. L. Adamson, “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound Med. Biol. 28, 1165-1172 (2002).
[CrossRef] [PubMed]

Hedlund, L. W.

C. T. Badea, B. Fubara, L. W. Hedlund, and G. A. Johnson, 4-D micro-CT of the mouse heart,” Mol. Imaging 4, 110-116 (2005).
[PubMed]

Hee, M. R.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Hickerson, A.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

Hierck, B. P.

P. Vennemann, K. T. Kiger, R. Lindken, B. C. W. Groenendijk, S. Stekelenburg-de Vos, T. L. M. ten Hugen, N. T. C. Ursem, R. E. Poelmann, J. Westerweel, and B. P. Hierck, “In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart,” J. Biomech. 39, 1191-1200 (2006).
[CrossRef]

B. C. W. Groenendijk, B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo,” Circ. Res. 96, 1291-1298 (2005).
[CrossRef] [PubMed]

Hitzenberger, C. K.

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]

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

Hoeks, A. P.

R. S. Reneman, T. Arts, and A. P. Hoeks, “Wall shear stress--an important determinant of endothelial cell function and structure--in the arterial system in vivo. Discrepancies with theory,” J. Vasc. Res. 43, 251-269 (2006).
[CrossRef] [PubMed]

Hogers, B.

B. Hogers, M. C. De Ruiter, A. C. Gittenberger-de Goot, and R. E. Poelmann, “Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal,” Cardiovasc. Res. 41, 87-99 (1999).
[CrossRef] [PubMed]

Holdsworth, D. W.

D. W. Holdsworth, M. Drangova, and A. Fenster, “A high-resolution XRII-based quantitative volume CT scanner,” Med. Phys. 20, 449-462 (1993).
[CrossRef] [PubMed]

Hove, J. R.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751-753 (2006).
[CrossRef] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevando-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172-177 (2003).
[CrossRef] [PubMed]

Hu, N.

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
[CrossRef] [PubMed]

N. Hu and E. B. Clark, “Hemodynamics of the stage 12 to stage 29 chick embryo,” Circ. Res. 65, 1665-1670 (1989).
[PubMed]

Hu, Z.

Huang, D.

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12, 041215 (2007).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254, 1178-1181 (1991).
[CrossRef] [PubMed]

Huber, R.

Hunsicker, P. R.

M. J. Paulus, S. S. Gleason, S. J. Kennel, P. R. Hunsicker, and D. K. Johnson, “High resolution x-ray computed tomography: an emerging tool for small animal cancer research,” Neoplasia 2, 62-70 (2000).
[CrossRef] [PubMed]

Iftimia, N. V.

Izatt, J.

Izatt, J. A.

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12, 041215 (2007).
[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).
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Westerweel, J.

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[CrossRef]

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S. Radhakrishnan, A. M. Rollins, J. E. Roth, S. Yazdanfar, V. Westphal, D. S. Bardenstein, and J. A. Izatt, “Real-time optical coherence tomography of the anterior segment at 1310 nm,” Arch. Ophthalmol. (Chicago) 119, 1179-1185 (2001).

Wilson, D. L.

Wladimiroff, J. W.

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
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T. M. Yelbuz, X. Zhang, M. A. Choma, H. A. Stadt, M. Zdlanowicz, G. A. Johnson, and M. L. Kirby, “Approaching cardiac development in three dimensions by magnetic resonance microscopy,” Circulation 108, e154-e155 (2003).
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Arch. Ophthalmol. (Chicago)

S. Radhakrishnan, A. M. Rollins, J. E. Roth, S. Yazdanfar, V. Westphal, D. S. Bardenstein, and J. A. Izatt, “Real-time optical coherence tomography of the anterior segment at 1310 nm,” Arch. Ophthalmol. (Chicago) 119, 1179-1185 (2001).

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Dev. Dyn.

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[CrossRef] [PubMed]

J. Manner, L. Thrane, K. Norozi, and T. M. Yelbuz, “High-resolution in vivo imaging of the cross-sectional deformations of contracting embryonic heart loops using optical coherence tomography,” Dev. Dyn. 237, 953-961 (2008).
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P. Vennemann, K. T. Kiger, R. Lindken, B. C. W. Groenendijk, S. Stekelenburg-de Vos, T. L. M. ten Hugen, N. T. C. Ursem, R. E. Poelmann, J. Westerweel, and B. P. Hierck, “In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart,” J. Biomech. 39, 1191-1200 (2006).
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J. Biomech. Eng.

L. A. Taber, J. Zhang, and R. Perucchio, “Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube,” J. Biomech. Eng. 129, 441-449 (2007).
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[CrossRef] [PubMed]

J. Exp. Biol.

N. T. Ursem, C. S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark, “Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction,” J. Exp. Biol. 207, 1487-1490 (2004).
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X. Zhang, T. M. Yelbuz, G. P. Kofer, M. A. Choma, M. L. Kirby, and G. A. Johnson, “Improved preparation of chick embryonic samples for magnetic resonance microscopy,” Magn. Reson. Med. 49, 1192-1195 (2003).
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[PubMed]

Nature

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Neoplasia

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[CrossRef]

Opt. Express

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, 3116-3121 (2003).
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Figures (6)

Fig. 1
Fig. 1

SDOCT microscope system for small animal imaging. (a) Chicken embryo preparation, (b) SDOCT system setup. A low-coherence light source ( λ = 1310 nm ) was used in a fiber-based Michelson interferometer design where the optical power was split using a 50 50 coupler into reference and sample arms. The interferogram was measured using a custom-made spectrometer containing a 512 element InGaAs CCD detector (Sensors Unlimited). Two-axis scanning of the SDOCT beam across the sample was performed using an adapted Zeiss stereo zoom microscope. (c) SDOCT signal falloff as a function of depth. 12 dB signal falloff was measured at 1.5 mm imaging depth. SLD, superluminescent diode (InPhenix); L, lens; M, mirror; M2, dual-axis scanning mirror (Optics in Motion); G, grating (Wasatch).

Fig. 2
Fig. 2

SDV measurement and volume rendering of chicken embryo vessel. (a) Doppler OCT image (blue) superimposed on a SDOCT intensity image of a cross section of a vessel. The vertical dashed line indicates the location where SDV measurements were acquired. (b) 3D surface rendering of the vessel. The surface rendering was used to measure the angle of blood flow (green) relative to the SDOCT scanning beam. Here two orthogonal OCT planes are displayed for which the x y plane corresponds to the image shown in (a). Scale bar = 200 μ m .

Fig. 3
Fig. 3

Detectable flow velocity range. Plot of the theoretical minimum and maximum detectable velocities, as per Eq. (1) using our 19 kHz , 1310 nm , SDOCT system. Higher velocities than the maximum plotted here are detectable but result in phase-wrapping artifacts.

Fig. 4
Fig. 4

Volume images of chicken embryo heart development from HH 9 to HH 15. Top row, SDOCT cross sections in x y and y z planes, volume reconstruction, and surface rendering of the fusing heart tube at HH 9 (View 1). Middle row, SDOCT cross sections in the x y and y z planes, volume reconstruction, and surface rendering of the fused heart tube at HH 12 (View 2). Bottom row, SDOCT cross sections in the x y and y z planes, volume reconstruction, and surface rendering of the looping heart tube at HH 15 (View 3). Light purple represents the heart tube wall consisting of the myocardium, cardiac jelly, and endocardium layers. Dark purple represents the heart tube lumen. The microscope images the in the third column were taken from representative embryos at or near the same stage of development. Cross sections and volume reconstructions were made using the VolView OSA visualization platform, currently called OSA ISP. nt, neural tube; ht, heart tube; s, somites; a, atrial buds; v, primitive ventricle; oft, outflow tract. Scale bar = 500 μ m .

Fig. 5
Fig. 5

Time series of Doppler SDOCT images of blood flow through the outflow tract. A series of Doppler B-mode images (red–blue) are overlaid on SDOCT images of the primitive ventricle and outflow tract at HH 11 (top) and HH 14 (bottom), respectively. At HH 14, the primitive ventricle increased in diameter and the endocardial cushion (ec) is clearly visible at 80 and 560 ms . All images were acquired at 12   frames s . 0 ms was set at diastole, or when the outflow tract was most contracted. Dotted arrows show the direction of flow. e, endocardium layer; m, myocardium layer; cj, cardiac jelly. Scale bar = 250 μ m .

Fig. 6
Fig. 6

SDV measurements at HH 11 and HH 14. Surface renderings and volume reconstructions of the heart tube at (a) HH 11 (View 4) and (d) HH 14 (View 5). Insets show Doppler OCT images of blood flow out of the outflow tract (out of the plane). SDV measurements were acquired along the yellow dashed line. The heart tube is in the midst of looping at HH 14 as evidenced by the U-shaped rendering and appearance of the inflow tract in (d). Blood flow velocity dynamics from (b) HH 11 and (e) HH 14. (c), (f) M-mode images where the vertical axis is depth and the horizontal is time. These M-mode images are acquired simultaneously with the velocity measurement, enabling correlation of heart tube contractions. SDV measurements were taken along the green dotted line in (c) and (f). oft, outflow tract; ift, inflow tract. Scale bar = 250 μ m .

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Tables (1)

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Table 1 Milestones of Early Heart Development in Different Species a

Equations (1)

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V ( z , t ) = Δ ϕ ( z , t ) 2 π T λ 2 n cos θ ,

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