Abstract
For treatment of complex congenital heart disease, computer simulation using a three-dimensional heart model may help to improve outcomes by enabling detailed preoperative evaluations. However, no highly integrated model that accurately reproduces a patient’s pathophysiology, which is required for this simulation has been reported. We modelled a case of complex congenital heart disease, double outlet right ventricle with ventricular septal defect and atrial septal defect. From preoperative computed tomography images, finite element meshes of the heart and torso were created, and cell model of cardiac electrophysiology and sarcomere dynamics was implemented. The parameter values of the heart model were adjusted to reproduce the patient’s electrocardiogram and haemodynamics recorded preoperatively. Two options of in silico surgery were performed using this heart model, and the resulting changes in performance were examined. Preoperative and postoperative simulations showed good agreement with clinical records including haemodynamics and measured oxyhaemoglobin saturations. The use of a detailed sarcomere model also enabled comparison of energetic efficiency between the two surgical options. A novel in silico model of congenital heart disease that integrates molecular models of cardiac function successfully reproduces the observed pathophysiology. The simulation of postoperative state by in silico surgeries can help guide clinical decision-making.
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Bahlmann, E., E. Gerdts, D. Cramariuc, C. Gohlke-Baerwolf, C. A. Nienaber, K. Wachtell, R. Seifert, J. B. Chambers, K. H. Kuck, and S. Ray. Prognostic value of energy loss index in asymptomatic aortic stenosis. Circulation 1247:1149–1156, 2013.
Baretta, A., C. Corsini, W. Yang, I. E. Vignon-Clementel, A. L. Marsden, J. A. Feinstein, T. Y. Hsia, G. Dubini, F. Migliavacca, and G. Pennati. Virtual surgeries in patients with congenital heart disease: a multi-scale modelling test case. Philos. Trans. R. Soc. Lond. Ser. A 369:4316–4330, 2011.
Corsini, C., D. Cosentino, G. Pennati, G. Dubini, T.-H. Hsia, and F. Migliavacca. Multiscale models of the hybridpalliation for hypoplastic left heart syndrome. J. Biomech. 44:767–770, 2011.
Courtemanche, M., R. J. Ramirez, and S. Nattel. Ionic mechanisms underlying human atrial action potential properites: insights from a mathematical model. Am. J. Physiol. 275:H301–321, 1998.
Escande, D., D. Loisance, C. Planche, and E. Coraboeuf. Age-related changes of action potential plateau shape in isolated human atrial fibers. Am. J. Physiol. 249:H843–850, 1985.
Haggerty, C. M., K. R. Kanter, M. Restrepo, D. A. de Zelicourt, W. J. Parks, J. Rossignac, M. A. Fogel, and A. P. Yoganathan. Simulating hemodynamics of the Fontan Y-graft based on patient-specific in vivo connections. J. Thorac. Cardiovasc. Surg. 145:663–670, 2013.
Helm P., R. Winslow and E. McVeigh. DTMRI data sets http://gforge.icm.jhu.edu/gf/project/dtmri_data_sets. Accessed 12 Jan 14, 2004.
Hoffman, J. I. Congenital heart disease: incidence and inheritance. Pediatric Clin. N. Am. 37:25–43, 1990.
Katayama, S., N. Umetani, T. Hisada, and S. Sugiura. Bicuspid aortic valves undergo excessive strain during its opening - a simulation study. J. Thorac. Cardiovasc. Surg. 145:1570–1576, 2013.
Kerckhoffs, R. C. P., M. L. Neal, Q. Gu, J. B. Bassingthwaighte, J. H. Omens, and A. D. McCulloch. Coupling of a 3D finite element model of cardiac ventricular mechanics to lumped systems models of the systemic and pulmonic circulation. Ann. Biomed. Eng. 35:1–18, 2007.
Nichols, W. W., C. J. Pepine, E. A. Geiser, and R. Conti. Vascular load defined by the aortic input impedance spectrum. Fed. Proc. 39:196–201, 1980.
O’Hara, T., L. Virag, A. Varro, and Y. Rudy. Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput. Biol. 7:e1002061, 2011.
Okada, J., T. Sasaki, T. Washio, H. Yamashita, T. Kariya, Y. Imai, M. Nakagawa, Y. Kadooka, R. Nagai, T. Hisada, and S. Sugiura. Patient specific simulation of body surface ECG using the finite element method. Pacing Clin. Electrophysiol. 36:309–321, 2013.
Okada, J., T. Washio, A. Maehara, S. Momomura, S. Sugiura, and T. Hisada. Transmural and apicobasal gradients in repolarization contribute to T-wave genesis in human surface ECG. Am. J. Physiol. 301:H200–208, 2011.
Okada, J.-I., T. Washio, M. Nakagawa, M. Watanabe, Y. Kadooka, T. Kariya, H. Yamashita, Y. Yamada, S.-I. Momomura, R. Nagai, T. Hisada, and S. Sugiura. Multi-scale, tailor-made heart simulation can predict the effect of cardiac resynchronization therapy. J. Mol. Cell Cardiol. 108:17–23, 2017.
Quail, M., and A. M. Taylor. Computer modeling to tailor therapy for congenital heart disease. Curr. Cardiol. Rep. 154:395–401, 2013.
Quarteroni, A., T. Lassila, S. Rossi, and R. Ruiz-Baier. Integrated Heart—Coupling multiscale and multiphysics models for the simulation of the cardiac function. Comput. Methods Appl. Mech. Eng. 314:345–407, 2017.
Riesenkampff, E., U. Rietdorf, I. Wolf, B. Schnackenburg, P. Ewert, M. Huebler, V. Alexi-Meskishvili, R. H. Anderson, N. Engel, H.-P. Meinzer, R. Hetzer, F. Berger, and T. Kuehne. The practical clinical value of three-dimensional models of complex congenitally malformed hearts. J. Thorac. Cardiovasc. Surg. 138:571–580, 2009.
Sanchez-Quintana, D., R. H. Anderson, and S. Y. Ho. Ventricular myoarchitecture in tetralogy of Fallot. Heart 76:280–286, 1996.
Santiago, A., J. Aguado-Sierra, M. Zavala-Aké, R. Doste-Beltran, S. Gómez, R. Arís, J. C. Cajas, E. Casoni, and M. Vázquez. Fully coupled fluid-electro-mechanical model of the human heart for supercomputers. Int. J. Numer. Methods Biomed. Eng. 34:e3140, 2018.
Shin’oka, T., H. Kurosawa, Y. Imai, M. Aoki, M. Ishiyama, T. Sakamoto, S. Miyamoto, K. Hobo, and Y. Ichihara. Outcomes of definitive surgical repair for congenitally corrected transposition of the great arteries or double outlet right ventricle with discordant atrioventricular connections: Risk analyses in 189 patients. J. Thorac. Cardiovasc. Surg. 133:1318–1328, 2007.
Shiraishi, I., M. Yamagishi, K. Hamaoka, M. Fukuzawa, and T. Yagihara. Simulative operation on congenital heart disease using rubber-like urethane stereolithographic biomodels based on 3D datasets of multislice computed tomography. Eur. J. Cardio-Thorac. Surg. 37:302–306, 2010.
Tobon-Gomez, C., N. Duchateau, R. Sebastian, S. Marchesseau, O. Camara, E. Donal, M. De Craene, A. Pashaei, J. Relan, M. Steghofer, P. Lamata, H. Delingette, S. Duckett, M. Garreau, A. Hernandez, K. S. Rhode, M. Sermesant, N. Ayache, C. Leclercq, R. Razavi, N. P. Smith, and A. F. Frangi. Understanding the mechanisms amenable to CRT response: from pre-operative multimodal image data to patient-specific computational models. Med. Biol. Eng. Comput. 51:1235–1250, 2013.
Washio, T., T. Hisada, H. Watanabe, and T. E. Tezduyar. A robust preconditioner for fluid-structure interaction problems. Comput. Methods Appl. Mech. Eng. 194:4027–4047, 2005.
Washio, T., J. Okada, and T. Hisada. A parallel multilevel technique for solving the bidomain equation on a human heart with Purkinje fibers and a torso model. SIAM Rev. 52:717–743, 2010.
Washio, T., J. Okada, S. Sugiura, and T. Hisada. Approximation for cooperative interactions of a spatially-detailed cardiac sarcomere model. Cell Mol. Bioeng. 5:113–126, 2011.
Washio, T., J.-I. Okada, A. Takahashi, K. Yoneda, Y. Kadooka, S. Sugiura, and T. Hisada. Multiscale heart simulation with cooperative stochastic cross-bridge dynamics and cellular structures. SIAM J. Multiscale Model. Simul. 11:965–999, 2013.
Washio, T., K. Yoneda, J. I. Okada, T. Kariya, S. Sugiura, and T. Hisada. Ventricular fiber optimization utilizing the branching structure. Int. J. Numer. Methods Biomed. Eng. 32:e02753, 2016.
Watanabe, H., S. Sugiura, H. Kafuku, and T. Hisada. Multiphysics simulation of left ventricular filling dynamics using fluid-structure interaction finite element method. Biophys. J. 87:2074–2085, 2004.
Yongxia, Q., and M. Boutjdir. Gene expression of SERCA2a and L- and T-type Ca channels during human heart devlopment. Pediatr. Res. 50:569–574, 2001.
Zhang, Q., and T. Hisada. Analysis of fluid-structure interaction problem with structural buckling and large domain change by ALE finite element method. Comput Methods Appl. Mech. Eng. 190:6341–6357, 2001.
Zhang, Q., and T. Hisada. Studies of the strong coupling and weak coupling methods in FSI analysis. Int. J. Numer. Methods Eng. 60:2013–2029, 2004.
Acknowledgments
We thank Richard Lipkin, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.
Conflict of interest
Dr. Okada, Dr. Washio, Dr. Hisada, and Dr. Sugiura have received Grant support from Fujitsu Ltd. The remaining authors have no disclosures.
Funding
This work was supported in part by MEXT as ‘Priority Issue on Post-K-computer’ (Integrated Computational Life Science to Support Personalized and Preventive Medicine, Project ID: hp160209 and hp150260), and by the Japan Society for the Promotion of Science (JSPS) through its ‘Funding Program for World-Leading Innovative R&D on Science and Technology (FIRST Program)’.
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Kariya, T., Washio, T., Okada, Ji. et al. Personalized Perioperative Multi-scale, Multi-physics Heart Simulation of Double Outlet Right Ventricle. Ann Biomed Eng 48, 1740–1750 (2020). https://doi.org/10.1007/s10439-020-02488-y
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DOI: https://doi.org/10.1007/s10439-020-02488-y