Construction of 3D MR image-based computer models of pathologic hearts, augmented with histology and optical fluorescence imaging to characterize action potential propagation

Medical Image Analysis

Volumn 16, Issue 2, 2012, Pages 505-523

  Pop, Mihaela ^a   Sermesant, Maxime ^b   Liu, Garry ^a   Relan, Jatin ^b   Mansi, Tommaso ^c   Soong, Alan ^a   Peyrat, Jean Marc ^d   Truong, Michael V ^e   Fefer, Paul ^a   McVeigh, Elliot R ^f   Delingette, Herve ^b   Dick, Alexander J ^g   Ayache, Nicholas ^b   Wright, Graham A ^a  

^a Sunnybrook Health Sciences Centre   (Canada)

^b INRIA   (France)

^c SIEMENS CORPORATE RESEARCH   (United States)

^d SIEMENS AG   (Germany)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Cardiac computer models; Electrophysiology; MRI; Optical imaging

Indexed keywords

ABSOLUTE ERROR; ACTION POTENTIAL PROPAGATION; ACTION POTENTIALS; ACTIVATION TIME; CLINICAL APPLICATION; COMPUTER MODELS; CONDUCTION VELOCITY; ELECTROPHYSIOLOGICAL MODELS; EPICARDIAL SURFACES; EXCITATION WAVES; EXPERIMENTAL CONDITIONS; FIBER DIRECTION; IMAGE-BASED; ISOCHRONES; MODEL PARAMETERS; MODEL PREDICTION; MR IMAGES; MYOCARDIAL TISSUE; NORMAL ZONE; OPTICAL FLUORESCENCE; OPTICAL IMAGE; OPTICAL IMAGING; RADIO FREQUENCIES; REACTION DIFFUSION; VELOCITY RATIO; VOLTAGE SENSITIVE DYES;

DEPOLARIZATION; ELECTROPHYSIOLOGY; GEOMETRICAL OPTICS; HEART; HISTOLOGY; MAGNETIC RESONANCE IMAGING; NEUROLOGY; PATHOLOGY; THREE DIMENSIONAL COMPUTER GRAPHICS; TISSUE;

THREE DIMENSIONAL;

ABLATION THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DATA ANALYSIS; DIFFUSION; ELECTROPHYSIOLOGY; EPICARDIUM; FLUORESCENCE IMAGING; HEART DEPOLARIZATION; HEART INFARCTION; HEART MUSCLE POTENTIAL; HEART PACING; HISTOPATHOLOGY; HUMAN; INSTRUMENT VALIDATION; MEDICAL RECORD; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREDICTION; PRIORITY JOURNAL; RADIOFREQUENCY; SCAR; SENSITIVITY ANALYSIS; THREE DIMENSIONAL IMAGING; VOLTAGE SENSITIVE DYE IMAGING; VOLUMETRY;

ALGORITHMS; BODY SURFACE POTENTIAL MAPPING; HEART CONDUCTION SYSTEM; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING, CINE; MICROSCOPY, FLUORESCENCE; MODELS, ANATOMIC; MODELS, CARDIOVASCULAR; PATTERN RECOGNITION, AUTOMATED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SUBTRACTION TECHNIQUE; VOLTAGE-SENSITIVE DYE IMAGING;

EID: 84856209117     PISSN: 13618415     EISSN: 13618423     Source Type: Journal    
DOI: 10.1016/j.media.2011.11.007     Document Type: Article

References (81)

1. Aliev R.R., Panfilov A.V. Modeling of heart excitation patterns caused by a local inhomogeneity. J. Theoret. Biol. 1996, 181:33-40.
2. Aliev R.R., Panfilov A.V. A simple two-variable model of cardiac excitation chaos. Solitons Fract. 1996, 7:293-301.
3. Ashikaga H., Sasano T., Dong J., et al. Magnetic resonance-based anatomical analysis of scar-related ventricular tachycardia: implications for catheter ablation. Circul. Res. 2007, 101(9):939-947.
4. Austin T., Trew M., Pullan A. Solving the cardiac bidomain equations for discontinuous conductivities. IEEE Trans. Biomed. Eng. 2006, 53(7):1265-1272.
5. Banville I., Gray R.A. Effect of action potential duration and conduction velocity restitution and their spatial dispersion on alternans and the stability of arrhythmias. J. Cardiovasc. Electrophysiol. 2002, 13:1141-1149.
6. Bayly P.V., KenKnight B.H., Rogers J.M., Hillsley R.E., Ideker R.E., Smith W.M. Estimation of conduction velocity vector fields from epicardial mapping data. IEEE Trans. Biomed. Eng. 1998, 45:563-571.
7. Bishop M., Plank G., Burton R.A.B., Schneider J.E., Gavaghan D.J., Grau V., Kohl P. Development of an anatomically detailed MRI-derived rabbit ventricular model and assessment of its impact on simulations of electrophysiological function. Am. J. Physiol. Heart Circ. Physiol. 2009, 298:H699-H718.
8. Caldwell B.J., Legrice I.J., Hooks D.A., Tai D.C.-S., Pullan A.J., Smaill B.H. Intramural measurement of transmembrane potential in the isolated pig heart: validation of a novel technique. J. Cardio. Electrophys. 2005, 16(9):1001-1010.
9. Camara O., Sermesant M., Lamata P., Wang L., Pop M., Relan J., De Craene M., Delingette H., Liu H., Niederer S., Plank G., Pashaei A., Romero D., Sebastian R., Wong K.C.L., Zhang H., Ayache N., Frangi A., Shi P., Smith N.P., Wright G.A. Inter-model consistency and complementarities: learning from ex-vivo imaging and electrophysiological data towards an integrated understanding of cardiac physiology. Prog. Biophys. Molec. Biol. 2011, 107:122-133.
10. Cerqueira M.D., Weissman N.J., Dilsizian V., Jacobs A.K., Kaul S., Laskey W.K., Pennell D.J., Rumberger J.A., Ryan T., Verani M.S. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart: a statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 2002, 105:539-542.
11. Chinchapatnam P., Rhode K.S., Ginks M., Rinaldi C.A., Lambiase P., Razavi R., Arridge S., Sermesant M. Model-based imaging of cardiac apparent conductivity and local conduction velocity for diagnosis and planning of therapy. IEEE Trans. Med. Imag. 2008, 27(11):1631-1642.
12. Chung, D., Pop, M., Sermesant, M., Wright, G.A., 2006. Stereo reconstruction of the epicardium for optical fluorescence imaging. In: Esboll, B.J., Jorgensen, T.M. (Eds.), MICCAI Workshop on Biophotonics for diagnosis and treatment, pp. 33-40.
13. Clarke G.M., Eidt S., Sun L., Mawdsley G., Zubovits J.T., Yaffee M.J. Whole-specimen histopathology: a method to produce whole-mount breast serial sections for 3-D digital histopathology imaging. Histopathology 2007, 50(2):232-242.
14. Clayton R.H. Computational models of normal and abnormal action potential propagation in cardiac tissue: linking experimental and clinical cardiology. Physiol. Meas. 2001, 22:R15-R34.
15. Clayton R.H., Panfilov A.V. A guide to modelling cardiac electrical activity in anatomically detailed ventricles. Prog. Biophys. Mol. Biol. 2008, 96(1-3):19-43.
16. Conn, A.R., Gould, N.I.M., Toint, Ph.L., 2000. Trust Region Methods, MPS-SIAM Series on Optimization 1, SIAM, Philadelphia, USA. ISBN-13: 978-0-898714-60-9.
17. De Bakker J.M.T., Van Capelle F.J.L., Janse M.J., Wilde A.A.M., Coronel R., Becker A.E., Dingemans K.P., Van Hemel N.M., Hauer R.N.W. Reentry as a cause of VT in patients with chronic ischemic heart disease: electrophysiologic and anatomic correlation. Circulation 1988, 77(3):589-606.
18. Dukkipati S., Mallozi R., et al. Electroanatomic mapping of the left ventricle in a porcine model of chronic myocardial infarction with magnetic resonance-based catheter tracking. Circulation 2008, 118(8):853-862.
19. Efimov I.R., Huang T.D., Rendt J.M., Salama G. Optical mapping of repolarization and refractoriness from intact heart. Circul. Res. 1994, 90:1469-1480.
20. Efimov I.R., Nikolski V.P., Salama G. Optical imaging of the heart. Circul. Res. 2004, 95:21-33.
21. Elharrar V., Surawicz B. Cycle length effect on restitution of action potential duration in dog cardiac fibers. Am. J. Physiol. 1983, 244:H782-H792.
22. Gavaghan D., Garny A., Maini P.K., Kohl P. Mathematical models in physiology. Philos. Trans. A Math. Phys. Eng. Sci. 2006, 364(1842):1099-1106.
23. Girouard S.D., Rosenbaum D.S. Role of wavelength adaptation in the initiation, maintenance, and pharmacologic suppression of reentry. J. Cardiovasc. Electrophysiol. 2001, 12(6):697-707.
24. Hao S.C., Christini D.J., Stein K.M., Jordan P.N., Iwai S., Bramwell O., Markowitz S.M., Mittal S., Lerman B.B. Effect of beta-adrenergic blockade on dynamic electrical restitution in vivo. Am. J. Physiol. 2004, 287:H390-H394.
25. Helm P.A., Tseng H.J., Younes L., McVeigh E.R., Winslow R.L. Ex vivo 3D diffusion tensor imaging and quantification of cardiac laminar structure. Magn. Reson. Med. 2005, 54:850-859.
26. Hillman E.M.C., Bernus O., Pease E., Bouchard M.B., Pertsov A. Depth-resolved optical imaging of transmural electrical propagation in perfused heart. Opt. Exp. 2007, 15:17827-17841.
27. Horn B.K.P. Closed-form solution of absolute orientation using unit quaternions. J. Opt. Soc. Am. A 1987, 4:629-642.
28. Hunter P.J., Nielsen P.M. A strategy for computational integrative physiology. Physiology 2005, 20:316-325.
29. Hunter P.J., Crampin E.J., Nielsen P.M. Bioinformatics, multiscale modeling and the IUPS Physiome Project. Brief Bioinform. 2008, 9(4):333-343.
30. Hyatt C.J., Mironov S.F., Vetter F.J., Zemlin C.W., Pertsov A.M. Optical action potential upstroke morphology reveals near-surface transmural propagation direction. Circul. Res. 2005, 97:277-284.
31. Hyatt C.J., Mironov S.F., Vetter F.J., Zemlin C.W., Pertsov A.M. Optical action potential upstroke morphology reveals near-surface transmural propagation direction. Circul. Res. 2005, 97:277-284.
32. Janse M.J., Wit A.L. Electrophysiological mechanisms of ventricular arrhythmias resulting from myocardial ischemia and infarction. Physiol. Rev. 1989, 69(4):1049-1169.
33. Kadish A., Shinnar M., Moore E.N., Levine J.H., Balke C.W., Spear J.F. Interaction of fiber orientation and direction of impulse propagation with anatomic barriers in anisotropic canine myocardium. Circulation 1988, 78:1478-1494.
34. Kawara T., Derksen R., de Groot J.R., Coronel R., Tasseron S., Linnenbank A.C., Hauer R.N., Kirkels H., Janse M.J., de Bakker J.M.T. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 2001, 104:3069-3074.
35. Kay M.W., Amison P.M., Rogers J.M. Three-dimensional surface reconstruction and panoramic optical mapping of large hearts. IEEE Trans. Biomed. Eng. 2004, 51:1219-1229.
36. Keener J.P., Sneyd J. Mathematical Physiology 1998, Springer.
37. Kim B.S., Kim Y.H., Hwang G.S., Pak H.N., Lee S.C., Shim W.J., Oh D.J., Ro Y.M. Action potential duration restitution kinetics in human atrial fibrillation. J. Am. College Cardiol. 2002, 39:1329-1336.
38. Kleber A.G., Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol. Rev. 2004, 84:431-488.
39. Lepiller D., Sermesant M., Pop M., Delingette H., Wright G.A., Ayache N. Cardiac electrophysiology model adjustment using the fusion of MR and optical imaging. Lecture Notes in Computer Science 2008, vol. 5241:678-685. Springer.
40. Li L., Nikolski V., Wallick D., Efimov I., Cheng Y. Redistribution of Cx43 expression in the endocardial infarction border zone is associated with increased arrhythmogenesis in the rabbit heart. Circulation 2003, 108:IV-189.
41. Martinez-Rubio A., Bayes-Genis A., Guindo J., Bayes de Luna A. Sudden cardiac death. Contrib. Sci. 1999, 1:147-157.
42. Mills W.R., Mal N., Forudi F., Popovic Z.B., Penn M.S., Laurita K.R. Optical mapping of late myocardial infarctions in rats. Am. J. Heart Circ. Physiol. 2005, (290):H1298-H1306.
43. Moreau-Villeger V., Delingette H., Sermesant M., Ashikaga H., McVeigh E., Ayache N. Building maps of local apparent conductivity of the epicardium with a 2-D electrophysiological model of the heart. IEEE Trans. Bio-med. Eng. 2006, 53:1457-1466.
44. Muzikant A.L., Henriquez C.S. Validation of three-dimensional conduction models using experimental mapping: are we getting closer?. Prog. Biophys. Mol. Biol. 1998, 69(2-3):205-223.
45. Nanthakumar K., Jalife J., Masse S., Downar E., Pop M., Asta J., Ross H., Rao V., Mironov S., Sevaptsidis E., Rogers J., Wright G., Dhopeshwarkar R. Optical mapping of Langendorff-perfused human hearts: establishing a model for the study of ventricular fibrillation in humans. Am. J. Physiol. Heart Circul. Physiol. 2007, 293:H875-H880.
46. Nash M.P., Panfilov A.V. Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias. Prog. Biophys. Mol. Biol. 2004, 85:501-522.
47. Niederer S., Kerfoot E., Benson A.P., Barnabeu M.O., Bernus O., Bradley C., Cherry E.M., Clayton R., Fenton F.H., Garny A., Heidenreich E., Land S., Maleckar M., Pathmanathan P., Plank G., Rodriguez J.F., Roy I., Sachse F.B., Seemann G., Skavhaug O., Smith N.P. Verification of cardiac tissue electro-physiology simulators using an N-version benchmark. Philos. Trans. Roy. Soc. 2011, 369:4331-4351.
48. Pastore J.M., Rosenbaum D.S. Role of structural barriers in the mechanism of alternans-induced reentry. Circul. Res. 2000, 87:1157-1163.
49. Pop, M., Sermesant, M., Chung, D., Liu, G., McVeigh, E.R., Crystal, E., Wright, G.A., 2007. An experimental framework to validate 3D models of cardiac electrophysiology via optical imaging and MRI. In: Proceedings of Functional Imaging and Modeling of the Heart 2007 (FIMH'07), LNCS, vol. 4466, 7-9 June, pp. 100-109.
50. Pop M., Sermesant M., Lepiller D., Truong M.V., McVeigh E.R., Crystal E., Dick A.J., Delingete H., Ayache N., Wright G.A. Fusion of optical imaging and MRI for the evaluation and adjustment of macroscopic models of cardiac electrophysiology: a feasibility study. Med. Image Anal. 2009, 13(2):370-380.
51. Pop, M., Sermesant, M., Mansi, T., Crystal, E., Detsky, J.S., Yang, Y., Fefer, P., McVeigh, E.R., Dick, A.J., Ayache, N., Wright, G.A. (2009b). Characterization of porcine infarcts heart: insights from experiments and theoretical modelling. In: Proceedings of the FIMH, June 3-5, 2009, Nice - LNCS, vol. 5528, Springer-Verlag, Berlin, Heidelberg, pp. 1-10.
52. Potse M., Dube B., Richer J., Vinet A., Gulrajani R.M. A comparison of monodomain and bidomain reaction-diffusion models for action potential propagation in human heart. IEEE Trans. Biomed. Eng. 2006, 53:2425-2435.
53. Prassl A.J., Kickinger F., Ahammer H., Grau V., Schneider J.E., Hofer E., Vigmond E.J., Trayanova N.A., Plank G. Automatically generated, anatomically accurate meshes for cardiac electrophysiology problems. IEEE Trans. Biomed. Eng. 2009, 56(5):1318-1330.
54. Qin H., Kay M.W., Chattipakon N., Redden D.T., Ideker R.E., Rogers J.M. Effects of heart isolation, voltage-sensitive dye, and electromechanical uncoupling agents on ventricular fibrillation. Am. J. Physiol. Heart Circ. Physiol. 2003, 284:H1818-H1826.
55. Qu F., Nikolski V., Efimov I., Deng C. Fluorescent real-time monitoring of HIFU cardiac focal ablation. J. Acoust. Soc. Am. 2004, 115(5):2448.
56. Relan J., Sermesant M., Delingette PopM, Sorine M., Wright G.A., Ayache N. Parameter estimation of a 3D cardiac electrophysiology model including the restitution curve using optical and MR data. IFMBE Proceedings, Munich, Germany 2009, vol. 25/IV:1716-1719. Springer.
57. Relan, J., Sermesant, M., Pop, M., Delingette, H., Sorine, M., Wright, G.A., Ayache, N., 2009b. Volumetric prediction of cardiac electrophysiology using a heart model personalised to surface data. In: MICCAI Workshop on Cardiovascular Interventional Imaging and Biophysical Modelling - CI2BM09, London, UK, pp. 19-27.
58. Relan J., Pop M., Delingette H., Wright G.A., Ayache N., Sermesant M. Personalisation of a cardiac electrophysiology model using optical mapping and MRI for prediction of changes with pacing. IEEE Trans. Biomed. Eng. 2011, 58(12):3339-3349.
59. Schmidt A., Azevedo C.F., Cheng A., et al. Infarct tissue heterogeneity by magnetic resonance imaging identifies enhanced cardiac arrhythmia susceptibility in patients with left ventricular dysfunction. Circulation 2007, 115(15):2006-2014.
60. Schmitt C., Zrenner B., Schneider M., Karch M., Ndrepepa G., Deisenhofer I., Weyerbrock S., Schreieck J., Schomig A. Clinical experience with a novel multielectrode basket catheter in right atrial tachycardias. Circulation 1999, 99(18):2414-2422.
61. Sermesant M., Faris O., Evans F., McVeigh E.R., Coudiere Y., Delingette H., Ayache N. " Preliminary Validation Using in vivo Measures of a Macroscopic Electrical Model of the Heart" in Surgery Simulation and soft Tissue Modelling 2003, Springer, Berlin/Heidelberg.
62. Sermesant M., Rhode K., Sanchez-Ortiz G.I., Camara O., Andriantsimiavona R., Hegde S., Rueckert D., Lambiase P., Bucknall C., Rosenthal E., Delingette H., Hill D.L., Ayache N., Razavi R. Simulation of cardiac pathologies using an electromechanical biventricular model and XMR interventional imaging. Med. Image Anal. 2005, 9:467-480.
63. Sermesant M., Delingette H., Ayache N. An electromechanical model of the heart for image analysis and simulation. IEEE Trans. Med. Imag. 2006, 25:612-625.
64. Stankovicova T., Szilard M., De Scheerder I., Sipido K.R. M cells and transmural heterogeneity of action potential configuration in myocytes from the left ventricular wall of the pig heart. Cardiovasc. Res. 2000, 45:952-960.
65. Sung D., Omens J.H., McCulloch A.D. Model-based analysis of optically mapped epicardial activation patterns and conduction velocity. Ann. Biomed. Eng. 2000, 28:1085-1092.
66. Taccardi B., Punske B.B., Macchi E., Macleod R.S., Ershler P.R. Epicardial and intramural excitation during ventricular pacing: effect of myocardial structure. Am. J. Physiol. Heart Circ. Physiol. 2008, 294(4):H1753-H1766.
67. Ten Tusscher K.H.W.J., Panfilov A.V. Influence of diffuse fibrosis on wave propagation in human ventricular tissue. Eurospace 2007, 9:38-45.
68. Trayanova N. Defibrillation of the heart: insights into mechanism from modelling studies. Exp. Physiol. 2006, 91:323-327.
69. Trayanova N. In the spotlight: cardiovascular engineering. IEEE Rev. Biomed. Eng. 2009, 17(2):12.
70. Ursell P.C., Gardner P.I., Albala A., Fenoglio J.J., Wit A.L. Structural and electrophysiological changes in the epicardial border zone of canine myocardial infarcts during infarct healing. Circul. Res. 1985, 56:436-451.
71. Vadakkumpadan F., Rantner L., Tice B., Boyle P., Prassl A., Vigmond E., Plank G., Trayanova N. Image-based models of cardiac structure with applications in arrhythmia and defibrillation studies. J. Electrocardiol. 2009, 42(2):157.
72. Vadakkumpadan F., Arevalo H., Prassl A.J., Chen J., Kickinger F., Kohl P., Plank G., Trayanova N.A. Image-based models of cardiac structure in health and disease Wiley Interdiscip. Rev. Syst. Biol. Med. 2010, 2(4):489-506.
73. Van Leemput K., Maes K., Vandermeulen F., Colchester A., Suetens P. Automated segmentation of multiple sclerosis lesions by model outlier detection. IEEE Trans. Med. Imag. 2001, 20(8):677-688.
74. Vetter F.J., Simons S.B., Mironov S., Hyatt C.J., Pertsov A.M. Epicardial fiber organization in swine right ventricle and its impact on propagation. Circ. Res. 2005, 96:244-251.
75. Vigmond E., Vadakkuumpadan D., Gurev V., Deo M., Plank G., Trayanova N. Towards predictive modelling of the electrophysiology of the heart. Exp. Physiol. 2009, 94:562-577.
76. Walton M.K., Fozzard H.A. The conducted action potential: models and comparison to experiments. Biophys. J. 1983, 44:9-26.
77. Wu M.T., Tseng W.Y.I., Su M.Y.M., Liu C.P., Chiou K.R., Wedeen V.J., Reese T.G., Yang C.F. Diffusion tensor magnetic resonance imaging mapping the fiber architecture remodeling in human myocardium after infarction - correlation with viability and wall motion. Circulation 2006, 114:1036-1045.
78. Wu E.X., Wu Y., Nicholls J.M., et al. MR diffusion tensor imaging study of postinfarct myocardium structural remodeling in a porcine model. Magn. Reson. Med. 2007, 58(4):687-695.
79. Xie F., Qu Z., Yang J., Baher A., Weiss J.N., Garfinkel A. A simulation study of the effects of cardiac anatomy in ventricular fibrillation. J. Clin. Invest. 2004, 113(5):686-693.
80. Yan A.T., Shayne A.J., Brown K.A., et al. Characterization of the peri-infarct zone by contrast-enhanced cardiac magnetic resonance imaging is a powerful predictor of post-myocardial infarction mortality. Circulation 2006, 114(1):32-39.
81. Yang Z., Zhang H., Kong S., Yue X.F., Jin Y.B., Jin J., Huang Y.C. Study for relevance of the acute myocardial ischemia to arrhythmia by the optical mapping method. Physiol. Measur. 2007, 28:481-488.