Abstract

Accurate imaging and measurement of hemodynamic forces is vital for investigating how physical forces acting on the embryonic heart are transduced and influence developmental pathways. Of particular importance is blood flow-induced shear stress, which influences gene expression by endothelial cells and potentially leads to congenital heart defects through abnormal heart looping, septation, and valvulogenesis. However no imaging tool has been available to measure shear stress on the endocardium volumetrically and dynamically. Using 4D structural and Doppler OCT imaging, we are able to accurately measure the blood flow in the heart tube in vivo and to map endocardial shear stress throughout the heart cycle under physiological conditions for the first time. These measurements of the shear stress patterns will enable precise titration of experimental perturbations and accurate correlation of shear with the expression of molecules critical to heart development.

© 2012 OSA

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    [CrossRef] [PubMed]
  3. J. Vermot, A. S. Forouhar, M. Liebling, D. Wu, D. Plummer, M. Gharib, and S. E. Fraser, “Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart,” PLoS Biol.7(11), e1000246 (2009).
    [CrossRef] [PubMed]
  4. R. E. Poelmann, A. C. Gittenberger-de Groot, and B. P. Hierck, “The development of the heart and microcirculation: role of shear stress,” Med. Biol. Eng. Comput.46(5), 479–484 (2008).
    [CrossRef] [PubMed]
  5. N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  26. M. Gargesha, M. W. Jenkins, D. L. Wilson, and A. M. Rollins, “High temporal resolution OCT using image-based retrospective gating,” Opt. Express17(13), 10786–10799 (2009).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]

2012 (2)

P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012).
[CrossRef]

M. Jenkins, M. Watanabe, and A. Rollins, “Longitudinal Imaging of Heart Development with Optical Coherence Tomography,” IEEE J. Sel. Top. Quantum Electron.18(3), 1166–1175 (2012).
[CrossRef]

2011 (4)

B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
[CrossRef] [PubMed]

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

C. M. Happel, L. Thrane, J. Thommes, J. Männer, and T. M. Yelbuz, ““Integration of an optical coherence tomography (OCT) system into an examination incubator to facilitate in vivo imaging of cardiovascular development in higher vertebrate embryos under stable physiological conditions” Annals of Anatomy -,” Anat. Anz.193(5), 425–435 (2011).
[CrossRef]

C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
[CrossRef] [PubMed]

2010 (3)

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
[CrossRef] [PubMed]

C. Poelma, K. Van der Heiden, B. P. Hierck, R. E. Poelmann, and J. Westerweel, “Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart,” J. R. Soc. Interface7(42), 91–103 (2010).
[CrossRef] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
[CrossRef] [PubMed]

2009 (7)

J. Vermot, A. S. Forouhar, M. Liebling, D. Wu, D. Plummer, M. Gharib, and S. E. Fraser, “Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart,” PLoS Biol.7(11), e1000246 (2009).
[CrossRef] [PubMed]

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt.14(4), 044020 (2009).
[CrossRef] [PubMed]

A. Davis, J. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (Hoboken)292(3), 311–319 (2009).
[CrossRef] [PubMed]

M. Gargesha, M. W. Jenkins, D. L. Wilson, and A. M. Rollins, “High temporal resolution OCT using image-based retrospective gating,” Opt. Express17(13), 10786–10799 (2009).
[CrossRef] [PubMed]

I. V. Larina, S. Ivers, S. Syed, M. E. Dickinson, and K. V. Larin, “Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT,” Opt. Lett.34(7), 986–988 (2009).
[CrossRef] [PubMed]

J. Ã. Männer, L. Thrane, K. Norozi, and T. M. Yelbuz, “In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function,” Dev. Dyn.238(12), 3273–3284 (2009).
[CrossRef] [PubMed]

2008 (5)

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. A25(12), 3134–3143 (2008).
[CrossRef] [PubMed]

S. Rugonyi, C. Shaut, A. Liu, K. Thornburg, and R. K. Wang, “Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation,” Phys. Med. Biol.53(18), 5077–5091 (2008).
[CrossRef] [PubMed]

R. E. Poelmann, A. C. Gittenberger-de Groot, and B. P. Hierck, “The development of the heart and microcirculation: role of shear stress,” Med. Biol. Eng. Comput.46(5), 479–484 (2008).
[CrossRef] [PubMed]

B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
[CrossRef] [PubMed]

R. M. Werkmeister, N. Dragostinoff, M. Pircher, E. Götzinger, C. K. Hitzenberger, R. A. Leitgeb, and L. Schmetterer, “Bidirectional Doppler Fourier-domain optical coherence tomography for measurement of absolute flow velocities in human retinal vessels,” Opt. Lett.33(24), 2967–2969 (2008).
[CrossRef] [PubMed]

2007 (5)

C. J. Pedersen, D. Huang, M. A. Shure, and A. M. Rollins, “Measurement of absolute flow velocity vector using dual-angle, delay-encoded Doppler optical coherence tomography,” Opt. Lett.32(5), 506–508 (2007).
[CrossRef] [PubMed]

G. B. Atkins and M. K. Jain, “Role of Krüppel-like transcription factors in endothelial biology,” Circ. Res.100(12), 1686–1695 (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. Express15(10), 6251–6267 (2007).
[CrossRef] [PubMed]

K. Yashiro, H. Shiratori, and H. Hamada, “Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch,” Nature450(7167), 285–288 (2007).
[CrossRef] [PubMed]

B. C. Groenendijk, K. Van der Heiden, B. P. Hierck, and R. E. Poelmann, “The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model,” Physiology (Bethesda)22(6), 380–389 (2007).
[CrossRef] [PubMed]

2006 (2)

J. P. Huddleson, N. Ahmad, and J. B. Lingrel, “Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin,” J. Biol. Chem.281(22), 15121–15128 (2006).
[CrossRef] [PubMed]

P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

2005 (2)

P. Basu, P. E. Morris, J. L. Haar, M. A. Wani, J. B. Lingrel, K. M. L. Gaensler, and J. A. Lloyd, “KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo,” Blood106(7), 2566–2571 (2005).
[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(12), 1291–1298 (2005).
[CrossRef] [PubMed]

2003 (2)

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature421(6919), 172–177 (2003).
[CrossRef] [PubMed]

M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
[CrossRef] [PubMed]

2002 (2)

C. K. L. Phoon, O. Aristizábal, 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(3), H908–H916 (2002).
[PubMed]

R. J. Dekker, S. van Soest, R. D. Fontijn, S. Salamanca, P. G. de Groot, E. VanBavel, H. Pannekoek, and A. J. G. Horrevoets, “Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2),” Blood100(5), 1689–1698 (2002).
[CrossRef] [PubMed]

2000 (2)

N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
[CrossRef] [PubMed]

C. K. L. 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(8), 1275–1283 (2000).
[CrossRef] [PubMed]

1999 (3)

M. L. A. Broekhuizen, B. Hogers, M. C. DeRuiter, R. E. Poelmann, A. C. Gittenberger-de Groot, and J. W. Wladimiroff, “Altered hemodynamics in chick embryos after extraembryonic venous obstruction,” Ultrasound Obstet. Gynecol.13(6), 437–445 (1999).
[CrossRef] [PubMed]

B. Hogers, M. C. DeRuiter, A. C. Gittenberger-de Groot, and R. E. Poelmann, “Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal,” Cardiovasc. Res.41(1), 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(22), 1584–1586 (1999).
[CrossRef] [PubMed]

1988 (1)

R. M. Goldstein, H. A. Zebker, and C. L. Werner, “Satellite radar interferometry: Two-dimensional phase unwrapping,” Radio Sci.23(4), 713–720 (1988).
[CrossRef]

1974 (1)

B. E. Dunn, “Technique of shell-less culture of the 72-hour avian embryo,” Poult. Sci.53(1), 409–412 (1974).
[CrossRef] [PubMed]

Acevedo-Bolton, G.

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature421(6919), 172–177 (2003).
[CrossRef] [PubMed]

Adler, D. C.

Ahmad, N.

J. P. Huddleson, N. Ahmad, and J. B. Lingrel, “Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin,” J. Biol. Chem.281(22), 15121–15128 (2006).
[CrossRef] [PubMed]

Akasaka, N.

N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
[CrossRef] [PubMed]

Aristizabal, O.

C. K. L. 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(8), 1275–1283 (2000).
[CrossRef] [PubMed]

Aristizábal, O.

C. K. L. Phoon, O. Aristizábal, 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(3), H908–H916 (2002).
[PubMed]

Atkins, G. B.

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J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature421(6919), 172–177 (2003).
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A. Davis, J. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (Hoboken)292(3), 311–319 (2009).
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M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
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B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
[CrossRef] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
[CrossRef] [PubMed]

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
[CrossRef] [PubMed]

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[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. Express15(10), 6251–6267 (2007).
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N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
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I. V. Larina, S. Ivers, S. Syed, M. E. Dickinson, and K. V. Larin, “Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT,” Opt. Lett.34(7), 986–988 (2009).
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I. V. Larina, S. Ivers, S. Syed, M. E. Dickinson, and K. V. Larin, “Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT,” Opt. Lett.34(7), 986–988 (2009).
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J. Vermot, A. S. Forouhar, M. Liebling, D. Wu, D. Plummer, M. Gharib, and S. E. Fraser, “Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart,” PLoS Biol.7(11), e1000246 (2009).
[CrossRef] [PubMed]

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B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
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[CrossRef] [PubMed]

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J. P. Huddleson, N. Ahmad, and J. B. Lingrel, “Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin,” J. Biol. Chem.281(22), 15121–15128 (2006).
[CrossRef] [PubMed]

P. Basu, P. E. Morris, J. L. Haar, M. A. Wani, J. B. Lingrel, K. M. L. Gaensler, and J. A. Lloyd, “KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo,” Blood106(7), 2566–2571 (2005).
[CrossRef] [PubMed]

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A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt.14(4), 044020 (2009).
[CrossRef] [PubMed]

S. Rugonyi, C. Shaut, A. Liu, K. Thornburg, and R. K. Wang, “Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation,” Phys. Med. Biol.53(18), 5077–5091 (2008).
[CrossRef] [PubMed]

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P. Basu, P. E. Morris, J. L. Haar, M. A. Wani, J. B. Lingrel, K. M. L. Gaensler, and J. A. Lloyd, “KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo,” Blood106(7), 2566–2571 (2005).
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C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
[CrossRef] [PubMed]

C. M. Happel, L. Thrane, J. Thommes, J. Männer, and T. M. Yelbuz, ““Integration of an optical coherence tomography (OCT) system into an examination incubator to facilitate in vivo imaging of cardiovascular development in higher vertebrate embryos under stable physiological conditions” Annals of Anatomy -,” Anat. Anz.193(5), 425–435 (2011).
[CrossRef]

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J. Ã. Männer, L. Thrane, K. Norozi, and T. M. Yelbuz, “In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function,” Dev. Dyn.238(12), 3273–3284 (2009).
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P. Basu, P. E. Morris, J. L. Haar, M. A. Wani, J. B. Lingrel, K. M. L. Gaensler, and J. A. Lloyd, “KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo,” Blood106(7), 2566–2571 (2005).
[CrossRef] [PubMed]

Nickerson, A.

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

Norozi, K.

J. Ã. Männer, L. Thrane, K. Norozi, and T. M. Yelbuz, “In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function,” Dev. Dyn.238(12), 3273–3284 (2009).
[CrossRef] [PubMed]

Ortmaier, T.

C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
[CrossRef] [PubMed]

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R. J. Dekker, S. van Soest, R. D. Fontijn, S. Salamanca, P. G. de Groot, E. VanBavel, H. Pannekoek, and A. J. G. Horrevoets, “Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2),” Blood100(5), 1689–1698 (2002).
[CrossRef] [PubMed]

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C. J. Pedersen, D. Huang, M. A. Shure, and A. M. Rollins, “Measurement of absolute flow velocity vector using dual-angle, delay-encoded Doppler optical coherence tomography,” Opt. Lett.32(5), 506–508 (2007).
[CrossRef] [PubMed]

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M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
[CrossRef] [PubMed]

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C. K. L. Phoon, O. Aristizábal, 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(3), H908–H916 (2002).
[PubMed]

C. K. L. 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(8), 1275–1283 (2000).
[CrossRef] [PubMed]

Pircher, M.

Plummer, D.

J. Vermot, A. S. Forouhar, M. Liebling, D. Wu, D. Plummer, M. Gharib, and S. E. Fraser, “Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart,” PLoS Biol.7(11), e1000246 (2009).
[CrossRef] [PubMed]

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C. Poelma, K. Van der Heiden, B. P. Hierck, R. E. Poelmann, and J. Westerweel, “Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart,” J. R. Soc. Interface7(42), 91–103 (2010).
[CrossRef] [PubMed]

B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
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Poelmann, R. E.

C. Poelma, K. Van der Heiden, B. P. Hierck, R. E. Poelmann, and J. Westerweel, “Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart,” J. R. Soc. Interface7(42), 91–103 (2010).
[CrossRef] [PubMed]

B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
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R. E. Poelmann, A. C. Gittenberger-de Groot, and B. P. Hierck, “The development of the heart and microcirculation: role of shear stress,” Med. Biol. Eng. Comput.46(5), 479–484 (2008).
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B. C. Groenendijk, K. Van der Heiden, B. P. Hierck, and R. E. Poelmann, “The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model,” Physiology (Bethesda)22(6), 380–389 (2007).
[CrossRef] [PubMed]

P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
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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(12), 1291–1298 (2005).
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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(12), 1291–1298 (2005).
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M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
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M. Jenkins, M. Watanabe, and A. Rollins, “Longitudinal Imaging of Heart Development with Optical Coherence Tomography,” IEEE J. Sel. Top. Quantum Electron.18(3), 1166–1175 (2012).
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Rollins, A. M.

B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
[CrossRef] [PubMed]

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
[CrossRef] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
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M. Gargesha, M. W. Jenkins, D. L. Wilson, and A. M. Rollins, “High temporal resolution OCT using image-based retrospective gating,” Opt. Express17(13), 10786–10799 (2009).
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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. Express15(10), 6251–6267 (2007).
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C. J. Pedersen, D. Huang, M. A. Shure, and A. M. Rollins, “Measurement of absolute flow velocity vector using dual-angle, delay-encoded Doppler optical coherence tomography,” Opt. Lett.32(5), 506–508 (2007).
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M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
[CrossRef] [PubMed]

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Rothenberg, F. G.

Rugonyi, S.

P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012).
[CrossRef]

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt.14(4), 044020 (2009).
[CrossRef] [PubMed]

S. Rugonyi, C. Shaut, A. Liu, K. Thornburg, and R. K. Wang, “Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation,” Phys. Med. Biol.53(18), 5077–5091 (2008).
[CrossRef] [PubMed]

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R. J. Dekker, S. van Soest, R. D. Fontijn, S. Salamanca, P. G. de Groot, E. VanBavel, H. Pannekoek, and A. J. G. Horrevoets, “Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2),” Blood100(5), 1689–1698 (2002).
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N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
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Sedmera, D.

M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
[CrossRef] [PubMed]

Shaut, C.

S. Rugonyi, C. Shaut, A. Liu, K. Thornburg, and R. K. Wang, “Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation,” Phys. Med. Biol.53(18), 5077–5091 (2008).
[CrossRef] [PubMed]

Shepherd, N.

Shi, L.

P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012).
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K. Yashiro, H. Shiratori, and H. Hamada, “Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch,” Nature450(7167), 285–288 (2007).
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C. J. Pedersen, D. Huang, M. A. Shure, and A. M. Rollins, “Measurement of absolute flow velocity vector using dual-angle, delay-encoded Doppler optical coherence tomography,” Opt. Lett.32(5), 506–508 (2007).
[CrossRef] [PubMed]

Stanley, C. P.

M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
[CrossRef] [PubMed]

Stekelenburg-de Vos, S.

P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

Sumpio, B. E.

N. Azuma, S. A. Duzgun, M. Ikeda, H. Kito, N. Akasaka, T. Sasajima, and B. E. Sumpio, “Endothelial cell response to different mechanical forces,” J. Vasc. Surg.32(4), 789–794 (2000).
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I. V. Larina, S. Ivers, S. Syed, M. E. Dickinson, and K. V. Larin, “Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT,” Opt. Lett.34(7), 986–988 (2009).
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P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

Thommes, J.

C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
[CrossRef] [PubMed]

C. M. Happel, L. Thrane, J. Thommes, J. Männer, and T. M. Yelbuz, ““Integration of an optical coherence tomography (OCT) system into an examination incubator to facilitate in vivo imaging of cardiovascular development in higher vertebrate embryos under stable physiological conditions” Annals of Anatomy -,” Anat. Anz.193(5), 425–435 (2011).
[CrossRef]

Thompson, R. P.

M. Reckova, C. Rosengarten, A. deAlmeida, C. P. Stanley, A. Wessels, R. G. Gourdie, R. P. Thompson, and D. Sedmera, “Hemodynamics is a key epigenetic factor in development of the cardiac conduction system,” Circ. Res.93(1), 77–85 (2003).
[CrossRef] [PubMed]

Thornburg, K.

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

S. Rugonyi, C. Shaut, A. Liu, K. Thornburg, and R. K. Wang, “Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation,” Phys. Med. Biol.53(18), 5077–5091 (2008).
[CrossRef] [PubMed]

Thornburg, K. L.

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt.14(4), 044020 (2009).
[CrossRef] [PubMed]

Thrane, L.

C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
[CrossRef] [PubMed]

C. M. Happel, L. Thrane, J. Thommes, J. Männer, and T. M. Yelbuz, ““Integration of an optical coherence tomography (OCT) system into an examination incubator to facilitate in vivo imaging of cardiovascular development in higher vertebrate embryos under stable physiological conditions” Annals of Anatomy -,” Anat. Anz.193(5), 425–435 (2011).
[CrossRef]

J. Ã. Männer, L. Thrane, K. Norozi, and T. M. Yelbuz, “In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function,” Dev. Dyn.238(12), 3273–3284 (2009).
[CrossRef] [PubMed]

Troyer, A.

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

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C. K. L. Phoon, O. Aristizábal, 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(3), H908–H916 (2002).
[PubMed]

C. K. L. 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(8), 1275–1283 (2000).
[CrossRef] [PubMed]

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P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

Van der Heiden, K.

C. Poelma, K. Van der Heiden, B. P. Hierck, R. E. Poelmann, and J. Westerweel, “Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart,” J. R. Soc. Interface7(42), 91–103 (2010).
[CrossRef] [PubMed]

B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
[CrossRef] [PubMed]

B. C. Groenendijk, K. Van der Heiden, B. P. Hierck, and R. E. Poelmann, “The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model,” Physiology (Bethesda)22(6), 380–389 (2007).
[CrossRef] [PubMed]

van Leeuwen, T. G.

van Soest, S.

R. J. Dekker, S. van Soest, R. D. Fontijn, S. Salamanca, P. G. de Groot, E. VanBavel, H. Pannekoek, and A. J. G. Horrevoets, “Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2),” Blood100(5), 1689–1698 (2002).
[CrossRef] [PubMed]

Vanauker, M.

B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
[CrossRef] [PubMed]

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R. J. Dekker, S. van Soest, R. D. Fontijn, S. Salamanca, P. G. de Groot, E. VanBavel, H. Pannekoek, and A. J. G. Horrevoets, “Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2),” Blood100(5), 1689–1698 (2002).
[CrossRef] [PubMed]

Vennemann, P.

P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

Vermot, J.

J. Vermot, A. S. Forouhar, M. Liebling, D. Wu, D. Plummer, M. Gharib, and S. E. Fraser, “Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart,” PLoS Biol.7(11), e1000246 (2009).
[CrossRef] [PubMed]

Vrolijk, J.

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(12), 1291–1298 (2005).
[CrossRef] [PubMed]

Wang, R.

A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
[CrossRef] [PubMed]

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt.14(4), 044020 (2009).
[CrossRef] [PubMed]

Wang, R. K.

P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012).
[CrossRef]

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

Watanabe, M.

M. Jenkins, M. Watanabe, and A. Rollins, “Longitudinal Imaging of Heart Development with Optical Coherence Tomography,” IEEE J. Sel. Top. Quantum Electron.18(3), 1166–1175 (2012).
[CrossRef]

B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
[CrossRef] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
[CrossRef] [PubMed]

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
[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. Express15(10), 6251–6267 (2007).
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[CrossRef] [PubMed]

B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
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P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
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[CrossRef]

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B. Garita, M. W. Jenkins, M. Han, C. Zhou, M. Vanauker, A. M. Rollins, M. Watanabe, J. G. Fujimoto, and K. K. Linask, “Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping,” Am. J. Physiol. Heart Circ. Physiol.300(3), H879–H891 (2011).
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[CrossRef] [PubMed]

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A. Liu, A. Nickerson, A. Troyer, X. Yin, R. Cary, K. Thornburg, R. Wang, and S. Rugonyi, “Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts,” Comput. Struc.89(11-12), 855–867 (2011).
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Dev. Dyn. (1)

J. Ã. Männer, L. Thrane, K. Norozi, and T. M. Yelbuz, “In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function,” Dev. Dyn.238(12), 3273–3284 (2009).
[CrossRef] [PubMed]

Eng. Comput. (1)

A. Liu, R. K. Wang, K. L. Thornburg, and S. Rugonyi, “Dynamic variation of hemodynamic shear stress on the walls of developing chick hearts: computational models of the heart outflow tract,” Eng. Comput.25(1), 73–86 (2009).
[CrossRef]

IEEE J. Sel. Top. Quantum Electron. (1)

M. Jenkins, M. Watanabe, and A. Rollins, “Longitudinal Imaging of Heart Development with Optical Coherence Tomography,” IEEE J. Sel. Top. Quantum Electron.18(3), 1166–1175 (2012).
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J. Biomed. Opt. (1)

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt.15(6), 066022 (2010).
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P. Vennemann, K. T. Kiger, R. Lindken, B. C. Groenendijk, S. Stekelenburg-de Vos, T. L. ten Hagen, N. T. 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(7), 1191–1200 (2006).
[CrossRef] [PubMed]

J. Biomed. Opt. (3)

P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012).
[CrossRef]

C. M. Happel, J. Thommes, L. Thrane, J. Männer, T. Ortmaier, B. Heimann, and T. M. Yelbuz, “Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan,” J. Biomed. Opt.16(9), 096007 (2011).
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J. Opt. Soc. Am. A (1)

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Nat. Photonics (1)

M. W. Jenkins, A. R. Duke, S. Gu, Y. Doughman, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics4(9), 623–626 (2010).
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Nature (2)

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Opt. Lett. (2)

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Physiology (Bethesda) (1)

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B. P. Hierck, K. Van der Heiden, C. Poelma, J. Westerweel, and R. E. Poelmann, “Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane!” ScientificWorldJournal8, 212–222 (2008).
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M. W. Jenkins, D. C. Adler, M. Gargesha, R. Huber, O. Q. Chughtai, Y. Pan, L. M. Peterson, D. L. Wilson, M. Watanabe, J. G. Fujimoto, and A. M. Rollins, “An environmental chamber based OCT system for high-throughput longitudinal imaging of the embryonic heart,” presented at the SPIE BIOS Expo, San Jose, CA, Jan 19­24, 2008.

Supplementary Material (1)

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Figures (6)

Fig. 1
Fig. 1

Panel A shows a quail embryo imaged with a stereomicroscope at 12X magnification. This embryo was removed from the yolk and inverted using the New culture for clear visualization under the microscope. All other embryos imaged by OCT in this work were left on the yolk as described in detail in the Methods section. Panel B shows a cross sectional image of the quail embryo heart imaged by OCT. The cross section was recorded at approximately the location of the green dotted line in panel A. Imaging by OCT allows for the visualization of the myocardium, cardiac jelly, and endocardium in vivo in both the inflow and outflow region of the heart tube. Panels C and D show Doppler OCT data overlaid on a structural cross section of the outflow tract of the heart tube during diastole and systole respectively at the approximate location of the red dotted line in panel B. The increasing red color represents increasing blood velocity in the forward direction and the blue represents retrograde blood flow as represented by the color bar. Myo, myocardium; CJ, cardiac jelly; BL, blood; Endo, endocardium.

Fig. 2
Fig. 2

Panel A shows the centerline (pink curve) through the segmented endocardium of a representative heart tube during diastole. Tangents to the centerline were used to determine the Doppler angle for absolute velocity calculations. Panel B shows the surface mesh of a representative segmented endocardium of a heart tube cut at the location of the dotted line in panel A. The white arrows pointed inward along the surface mesh represent the normal vectors to the endocardium along the entire inner wall of the heart tube.

Fig. 3
Fig. 3

Shear stress on the endocardium. Shear stress is calculated using the velocity gradient normal to the wall of the heart tube and the viscosity of blood. Four evenly spaced time points during a heart cycle are represented and the shear stress values are displayed on the endocardium surface. The represented heartbeat lasted 367 ms. The gray region represents the area where valid Doppler OCT data were not obtained because the direction of the blood flow was nearly perpendicular to the OCT imaging beam. See also Media 1.

Fig. 4
Fig. 4

Shear stress on the inner and outer curvature of the outflow tract. Panel A shows the 3D shear stress map at the time of maximum shear stress in the outflow tract. Panel B and C show the shear stress map of the same heart cropped to show only the outflow tract. Panel B shows the shear stress map oriented to view the outer curvature of the heart tube and Panel C shows the shear stress map oriented to view the inner curvature of the heart. The viewing direction is represented in panel A by the two arrows.

Fig. 5
Fig. 5

Shear stress measured over time. Panels A-C shows the measured shear stress over time at three different locations in the same heart, namely the inner and outer curvatures of the outflow tract, and the inflow tract, respectively. The shear stress was calculated for the duration of one effective heart cycle and displayed three times for ready visualization. The locations represented by all three traces are indicated in the 3D surface mesh shown in panel D. P, pumping phase; F, filling phase.

Fig. 6
Fig. 6

Shear rate measurement verification. The x-axis represents the actual flow rate recorded from the syringe pump. The y-axis shows the shear rate values measured from the Doppler OCT data taken at each flow rate. These calculations were repeated for 7 experiments at each flow rate. The solid line represents the theoretical shear rate based on the measured flow rates. The dotted line represents the peak shear stress value measured in the embryonic heart.

Tables (1)

Tables Icon

Table 1 Maximal shear stress at the inflow and outflow regions of the heart (Pa)a

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