Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart.

Four-dimensional (4-D) imaging of the embryonic heart allows study of cardiac morphology and function in vivo during development. However, 4-D imaging of the embryonic heart using current techniques, including optical coherence tomography (OCT), is limited by the rate of image acquisition. Here, we present a nongated 4-D imaging strategy combined with an efficient postacquisition synchronization procedure that circumvents limitations on acquisition rate. The 4-D imaging strategy acquires a time series of images in B mode at several different locations along the heart, rendering out-of-phase image sequences. Then, our synchronization procedure uses similarity of local structures to find the phase shift between neighboring image sequences, employing M-mode images (extracted from the acquired B-mode images) to achieve computational efficiency. Furthermore, our procedure corrects the phase shifts by considering the phase lags introduced by peristaltic-like contractions of the embryonic heart wall. We applied the 4-D imaging strategy and synchronization procedure to reconstruct the cardiac outflow tract (OFT) of a chick embryo, imaged with OCT at early stages of development (Hamburger-Hamilton stage 18). We showed that the proposed synchronization procedure achieves efficiency without sacrificing accuracy and that the reconstructed 4-D images properly captured the dynamics of the OFT wall motion.

[1]  M. Fishman,et al.  Fashioning the vertebrate heart: earliest embryonic decisions. , 1997, Development.

[2]  Ruikang K. Wang,et al.  Theory, developments and applications of optical coherence tomography , 2005 .

[3]  Stephen A. Boppart,et al.  Optical coherence tomography: Principles applications and advances , 2004 .

[4]  Gabriel Acevedo-Bolton,et al.  Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis , 2003, Nature.

[5]  Reiner Horst,et al.  Introduction to Global Optimization (Nonconvex Optimization and Its Applications) , 2002 .

[6]  T. Bartman,et al.  Mechanics and function in heart morphogenesis , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[8]  M. Dworetsky A period-finding method for sparse randomly spaced observations or “How long is a piece of string?” , 1983 .

[9]  M. DeRuiter,et al.  Basics of Cardiac Development for the Understanding of Congenital Heart Malformations , 2005, Pediatric Research.

[10]  A. Moorman,et al.  Cardiac chamber formation: development, genes, and evolution. , 2003, Physiological reviews.

[11]  Michael Liebling,et al.  Rapid three‐dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[12]  Michael Liebling,et al.  Wavelet-based synchronization of nongated confocal microscopy data for 4D imaging of the embryonic heart , 2005, SPIE Optics + Photonics.

[13]  Michael Unser,et al.  Splines: a perfect fit for signal and image processing , 1999, IEEE Signal Process. Mag..

[14]  Jörg Männer,et al.  High‐resolution in vivo imaging of the cross‐sectional deformations of contracting embryonic heart loops using optical coherence tomography , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[15]  Ruikang K. Wang,et al.  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 , 2008, Physics in medicine and biology.

[16]  Anna I Hickerson,et al.  The Embryonic Vertebrate Heart Tube Is a Dynamic Suction Pump , 2006, Science.

[17]  Michael Liebling,et al.  Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences. , 2005, Journal of biomedical optics.

[18]  Colin K. L. Phoon,et al.  Imaging Tools for the Developmental Biologist: Ultrasound Biomicroscopy of Mouse Embryonic Development , 2006, Pediatric Research.

[19]  Max A. Viergever,et al.  Quantitative evaluation of convolution-based methods for medical image interpolation , 2001, Medical Image Anal..

[20]  Daniel L Marks,et al.  Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system. , 2006, Journal of biomedical optics.

[21]  Michael W. Jenkins,et al.  4D embryonic cardiography using gated optical coherence tomography. , 2006, Optics express.

[22]  M. Turiel,et al.  Power Spectral Analysis of Heart Rate and Arterial Pressure Variabilities as a Marker of Sympatho‐Vagal Interaction in Man and Conscious Dog , 1986, Circulation research.

[23]  M. Jenkins,et al.  In vivo gated 4D imaging of the embryonic heart using optical coherence tomography. , 2007, Journal of biomedical optics.

[24]  J. Fujimoto Optical coherence tomography for ultrahigh resolution in vivo imaging , 2003, Nature Biotechnology.

[25]  S A Boppart,et al.  Optical coherence tomography imaging in developmental biology. , 2000, Methods in molecular biology.

[26]  E. Olson A decade of discoveries in cardiac biology , 2004, Nature Medicine.

[27]  Renato Perucchio,et al.  Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube. , 2007, Journal of biomechanical engineering.

[28]  Joseph M. Schmitt,et al.  Optical coherence tomography (OCT): a review , 1999 .

[29]  E. Clark,et al.  Spectrum of cardiovascular anomalies following cardiac loop constriction in the chick embryo. , 1978, Birth defects original article series.

[30]  R. Stellingwerf Period determination using phase dispersion minimization , 1978 .

[31]  J. Fujimoto,et al.  Optical Coherence Tomography Principles, Instrumentation, and Biological Applicatons , 1996 .

[32]  S. Carerj,et al.  Anatomical M‐Mode: An Old–New Technique , 2003, Echocardiography.

[33]  Michael W. Jenkins,et al.  Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier Domain Mode Locked laser. , 2007, Optics express.

[34]  Adrian Mariampillai,et al.  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. , 2007, Optics express.

[35]  Joseph A. Izatt,et al.  Optical Coherence Tomography: A New High-Resolution Imaging Technology to Study Cardiac Development in Chick Embryos , 2002, Circulation.

[36]  W G O'Dell,et al.  Imaging three-dimensional cardiac function. , 2000, Annual review of biomedical engineering.

[37]  Benjamin J Vakoc,et al.  Multimodality optical imaging of embryonic heart microstructure. , 2007, Journal of biomedical optics.

[38]  C. Blanco,et al.  The chicken embryo in developmental physiology of the cardiovascular system: a traditional model with new possibilities. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[39]  Panos M. Pardalos,et al.  Introduction to Global Optimization , 2000, Introduction to Global Optimization.

[40]  Jörg Männer,et al.  Cardiac looping in the chick embryo: A morphological review with special reference to terminological and biomechanical aspects of the looping process , 2000, The Anatomical record.

[41]  W H Lamers,et al.  Persisting zones of slow impulse conduction in developing chicken hearts. , 1992, Circulation research.

[42]  J. Izatt,et al.  Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography. , 2008, Journal of biomedical optics.

[43]  D. Stainier,et al.  Early Myocardial Function Affects Endocardial Cushion Development in Zebrafish , 2004, PLoS biology.

[44]  Bradley B Keller,et al.  Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[45]  N. Hu,et al.  Hemodynamics of the Stage 12 to Stage 29 Chick Embryo , 1989, Circulation research.

[46]  D. H. Roberts,et al.  Time Series Analysis with Clean - Part One - Derivation of a Spectrum , 1987 .