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In vivo spectral domain optical coherence tomography volumetric imaging and spectral Doppler velocimetry of early stage embryonic chicken heart development
A. M. Davis, F. G. Rothenberg, N. Shepherd, and J. A. Izatt »View Author Affiliations
1Biomedical Engineering Department, Duke University, 136 Hudson Hall, 3000 Science Drive, Durham, North Carolina 27708, USA
2Division of Cardiovascular Diseases, University of Cincinnati, 231 Albert Sabin Way, ML 0542, Cincinnati, Ohio 45267, USA
3Department of Pediatrics/Neonatology Division, Duke University Medical Center, DUMC Box 3719, Durham, North Carolina 27710, USA
*Corresponding author: Anjul.Davis@gmail.com
JOSA A, Vol. 25, Issue 12, pp. 3134-3143 (2008)
http://dx.doi.org/10.1364/JOSAA.25.003134
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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
OCIS Codes
(110.4500) Imaging systems : Optical coherence tomography
(110.6880) Imaging systems : Three-dimensional image acquisition
(170.1420) Medical optics and biotechnology : Biology
(280.3340) Remote sensing and sensors : Laser Doppler velocimetry
ToC Category:
Imaging Systems
History
Original Manuscript: July 18, 2008
Revised Manuscript: October 19, 2008
Manuscript Accepted: October 20, 2008
Published: November 26, 2008
Virtual Issues
Vol. 4, Iss. 2 Virtual Journal for Biomedical Optics
Interactive Science Publishing (2008) Optics Express
Citation
A. M. Davis, F. G. Rothenberg, N. Shepherd, and J. A. Izatt, "In vivo spectral domain optical coherence tomography volumetric imaging and spectral Doppler velocimetry of early stage embryonic chicken heart development," J. Opt. Soc. Am. A 25, 3134-3143 (2008)
http://www.opticsinfobase.org/josaa/abstract.cfm?URI=josaa-25-12-3134
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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). [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, 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]
- 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]
- 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).
- 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. 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]
- 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]
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- 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]
- 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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- 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]
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- 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]
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- 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]
- 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).
- 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]
- 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]
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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). [CrossRef] [PubMed]
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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]
- 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]
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Am. J. Physiol. Heart Circ. Physiol.
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Anat. Rec.
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Arch. Ophthalmol. (Chicago)
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Cardiovasc. Res.
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Circ. Res.
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Circulation
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Dev. Dyn.
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Development
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J. Biomed. Opt.
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Magn. Reson. Med.
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Med. Phys.
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Neoplasia
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Opt. Commun.
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Opt. Express
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2008, Manner, Dev. Dyn.
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- 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]
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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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- 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]
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- 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]
- 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]
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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). [CrossRef] [PubMed]
- 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]
- 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]
- 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]
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- N. Hu and E. B. Clark, “Hemodynamics of the stage 12 to stage 29 chick embryo,” Circ. Res. 65, 1665-1670 (1989). [PubMed]
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