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Erschienen in: International Journal of Computer Assisted Radiology and Surgery 1/2019

19.09.2018 | Original Article

Influence of fiber connectivity in simulations of cardiac biomechanics

verfasst von: D Gil, R Aris, A Borras, E Ramirez, R Sebastian, M Vazquez

Erschienen in: International Journal of Computer Assisted Radiology and Surgery | Ausgabe 1/2019

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Abstract

Purpose

Personalized computational simulations of the heart could open up new improved approaches to diagnosis and surgery assistance systems. While it is fully recognized that myocardial fiber orientation is central for the construction of realistic computational models of cardiac electromechanics, the role of its overall architecture and connectivity remains unclear. Morphological studies show that the distribution of cardiac muscular fibers at the basal ring connects epicardium and endocardium. However, computational models simplify their distribution and disregard the basal loop. This work explores the influence in computational simulations of fiber distribution at different short-axis cuts.

Methods

We have used a highly parallelized computational solver to test different fiber models of ventricular muscular connectivity. We have considered two rule-based mathematical models and an own-designed method preserving basal connectivity as observed in experimental data. Simulated cardiac functional scores (rotation, torsion and longitudinal shortening) were compared to experimental healthy ranges using generalized models (rotation) and Mahalanobis distances (shortening, torsion).

Results

The probability of rotation was significantly lower for ruled-based models [95% CI (0.13, 0.20)] in comparison with experimental data [95% CI (0.23, 0.31)]. The Mahalanobis distance for experimental data was in the edge of the region enclosing 99% of the healthy population.

Conclusions

Cardiac electromechanical simulations of the heart with fibers extracted from experimental data produce functional scores closer to healthy ranges than rule-based models disregarding architecture connectivity.
Literatur
1.
Zurück zum Zitat Bishop M, Hales P, Plank G, Gavaghan DJ, Scheider J, Grau V (2009) Comparison of rule-based and dtmri-derived fibre architecture in a whole rat ventricular computational model. In: Functional imaging and modeling of the heart, pp 87–96 Bishop M, Hales P, Plank G, Gavaghan DJ, Scheider J, Grau V (2009) Comparison of rule-based and dtmri-derived fibre architecture in a whole rat ventricular computational model. In: Functional imaging and modeling of the heart, pp 87–96
3.
Zurück zum Zitat Carreras F, Garcia J, Gil D, Pujadas S, Li CH, Suarez-Arias R, Leta R, Alomar X, Ballester M, Pons-Llado G (2012) Left ventricular torsion and longitudinal shortening: two fundamental components of myocardial mechanics assessed by tagged cine-mri in normal subjects. Int J Cardiovasc Imaging 28(2):273–84CrossRefPubMed Carreras F, Garcia J, Gil D, Pujadas S, Li CH, Suarez-Arias R, Leta R, Alomar X, Ballester M, Pons-Llado G (2012) Left ventricular torsion and longitudinal shortening: two fundamental components of myocardial mechanics assessed by tagged cine-mri in normal subjects. Int J Cardiovasc Imaging 28(2):273–84CrossRefPubMed
4.
Zurück zum Zitat Casero R, Burton R.A, Quinn T.A, Bollensdorff C, Hales P, Schneider J, Kohl P, Grau V (2010) Cardiac valve annulus manual segmentation using computer assisted visual feedback in three-dimensional image data. In: EMBC, pp 738–741 Casero R, Burton R.A, Quinn T.A, Bollensdorff C, Hales P, Schneider J, Kohl P, Grau V (2010) Cardiac valve annulus manual segmentation using computer assisted visual feedback in three-dimensional image data. In: EMBC, pp 738–741
5.
Zurück zum Zitat Ferreira PF, Kilner PJ, McGill LA, Nielles-Vallespin S, Scott AD, Ho SY, McCarthy KP, Haba M, Ismail T, Gatehouse P, Silva R, Lyon A, Prasad S, Firmin D (2014) In vivo cardiovascular magnetic resonance diffusion tensor imaging shows evidence of abnormal myocardial laminar orientations and mobility in hypertrophic cardiomyopathy. J Cardiovasc Mag Res 16(87):1–16 Ferreira PF, Kilner PJ, McGill LA, Nielles-Vallespin S, Scott AD, Ho SY, McCarthy KP, Haba M, Ismail T, Gatehouse P, Silva R, Lyon A, Prasad S, Firmin D (2014) In vivo cardiovascular magnetic resonance diffusion tensor imaging shows evidence of abnormal myocardial laminar orientations and mobility in hypertrophic cardiomyopathy. J Cardiovasc Mag Res 16(87):1–16
6.
Zurück zum Zitat Fritz T, Wieners C, Seemann G (2014) Simulation of the contraction of the ventricles in a human heart model including atria and pericardium. Biomech Model Mechanobiol 13:627–641CrossRefPubMed Fritz T, Wieners C, Seemann G (2014) Simulation of the contraction of the ventricles in a human heart model including atria and pericardium. Biomech Model Mechanobiol 13:627–641CrossRefPubMed
7.
Zurück zum Zitat Gil D, Borras A, Aris R, Vazquez M, Lafortune P, Houzeaux G, Aguado J, Ballester M, Li CH, Carreras F (2012) What a difference in biomechanics cardiac fiber makes. In: STACOM Gil D, Borras A, Aris R, Vazquez M, Lafortune P, Houzeaux G, Aguado J, Ballester M, Li CH, Carreras F (2012) What a difference in biomechanics cardiac fiber makes. In: STACOM
8.
Zurück zum Zitat Gonzalez Tendero A, Zhang C, Balicevic V, Cardenes R, Loncaric S, Butakoff C, Paun B, Bonnin A, Garcia-Canadilla P, Munoz-Moreno E, Gratacos E, Crispi F, Bijnens (2017) Whole heart detailed and quantitative anatomy, myofibre structure and vasculature from x-ray phase-contrast synchrotron radiation-based micro computed tomography. EHJ Cardiovasc Imaging 18:732–41CrossRef Gonzalez Tendero A, Zhang C, Balicevic V, Cardenes R, Loncaric S, Butakoff C, Paun B, Bonnin A, Garcia-Canadilla P, Munoz-Moreno E, Gratacos E, Crispi F, Bijnens (2017) Whole heart detailed and quantitative anatomy, myofibre structure and vasculature from x-ray phase-contrast synchrotron radiation-based micro computed tomography. EHJ Cardiovasc Imaging 18:732–41CrossRef
9.
Zurück zum Zitat Gurev V, Lee T, Constantino J, Arevalo H, Trayanova NA (2011) Models of cardiac electromechanics based on individual hearts imaging data. Biomech Model Mechanobiol 10(3):295–306CrossRefPubMed Gurev V, Lee T, Constantino J, Arevalo H, Trayanova NA (2011) Models of cardiac electromechanics based on individual hearts imaging data. Biomech Model Mechanobiol 10(3):295–306CrossRefPubMed
10.
Zurück zum Zitat Helm PA, Younes L, Beg MF, Ennis DB, Leclercq C, Faris OP, McVeigh E, Kass D, Miller MI, Winslow RL (2006) Evidence of structural remodeling in the dyssynchronous failing heart. Circ Res 98(1):125–132CrossRefPubMed Helm PA, Younes L, Beg MF, Ennis DB, Leclercq C, Faris OP, McVeigh E, Kass D, Miller MI, Winslow RL (2006) Evidence of structural remodeling in the dyssynchronous failing heart. Circ Res 98(1):125–132CrossRefPubMed
11.
Zurück zum Zitat Humphrey J (2001) Cardiovascular solid mechanics. Cells, tissues, and organs. Springer, Berlin Humphrey J (2001) Cardiovascular solid mechanics. Cells, tissues, and organs. Springer, Berlin
12.
Zurück zum Zitat Hunter PJ, McCulloch AD, ter Keurs HE (1998) Modelling the mechanical properties of cardiac muscle. Prog Biophys Mol Biol 69(2–3):289–331CrossRefPubMed Hunter PJ, McCulloch AD, ter Keurs HE (1998) Modelling the mechanical properties of cardiac muscle. Prog Biophys Mol Biol 69(2–3):289–331CrossRefPubMed
13.
Zurück zum Zitat Lafortune P, Arís R, Vázquez M, Houzeaux G (2012) Coupled electromechanical model of the heart: Parallel finite element formulation. Int J Numer Methods Biomed Eng 28:72–86CrossRef Lafortune P, Arís R, Vázquez M, Houzeaux G (2012) Coupled electromechanical model of the heart: Parallel finite element formulation. Int J Numer Methods Biomed Eng 28:72–86CrossRef
14.
Zurück zum Zitat Myerburg RJ, Nilsson K, Gelband H (1972) Physiology of canine intraventricular conduction and endocardial excitation. Circ Res 30(2):217–243CrossRefPubMed Myerburg RJ, Nilsson K, Gelband H (1972) Physiology of canine intraventricular conduction and endocardial excitation. Circ Res 30(2):217–243CrossRefPubMed
15.
Zurück zum Zitat O’Hara T, Virag L, Varro A, Rudy Y (2011) Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput Biol 7(5):e1002061CrossRefPubMedPubMedCentral O’Hara T, Virag L, Varro A, Rudy Y (2011) Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput Biol 7(5):e1002061CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Potse M, Dube B, Richer J, Vinet A, Gulrajani RM (2006) A comparison of monodomain and bidomain reaction–diffusion models for action potential propagation in the human heart. Trans Biomed Eng 53(12):2425–2435CrossRef Potse M, Dube B, Richer J, Vinet A, Gulrajani RM (2006) A comparison of monodomain and bidomain reaction–diffusion models for action potential propagation in the human heart. Trans Biomed Eng 53(12):2425–2435CrossRef
17.
Zurück zum Zitat Poveda F, Gil D, Marti E, Andaluz A, Ballester M, Carreras F (2013) Helical structure of the cardiac ventricular anatomy assessed by diffusion tensor magnetic resonance imaging multi-resolution tractography. Rev Esp Cardiaol 66(10):782–90CrossRef Poveda F, Gil D, Marti E, Andaluz A, Ballester M, Carreras F (2013) Helical structure of the cardiac ventricular anatomy assessed by diffusion tensor magnetic resonance imaging multi-resolution tractography. Rev Esp Cardiaol 66(10):782–90CrossRef
18.
Zurück zum Zitat Santiago A (2018) Fluid Electro Mechanical model of the human heart for supercomputers. Ph.D. Thesis. UPC, Barcelona, Spain Santiago A (2018) Fluid Electro Mechanical model of the human heart for supercomputers. Ph.D. Thesis. UPC, Barcelona, Spain
19.
Zurück zum Zitat Savadjieva P, Strijkers GJ, Bakermans AJ, Piuze E, Zucker S, Siddiqi K (2012) Heart wall myofibers are arranged in minimal surfaces to optimize organ function. PNAS 109(24):9248–9253CrossRef Savadjieva P, Strijkers GJ, Bakermans AJ, Piuze E, Zucker S, Siddiqi K (2012) Heart wall myofibers are arranged in minimal surfaces to optimize organ function. PNAS 109(24):9248–9253CrossRef
20.
Zurück zum Zitat Scollan D, Holmes A, Winslow R, Forder J (1998) Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol 275:2308–2318 Scollan D, Holmes A, Winslow R, Forder J (1998) Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol 275:2308–2318
21.
Zurück zum Zitat Sebastián R, Zimmerman V, Romero D, Sánchez-Quintana D, Frangi AF (2013) Characterization and modeling of the peripheral cardiac conduction system. IEEE Trans Med Imaging 32(1):45–55CrossRefPubMed Sebastián R, Zimmerman V, Romero D, Sánchez-Quintana D, Frangi AF (2013) Characterization and modeling of the peripheral cardiac conduction system. IEEE Trans Med Imaging 32(1):45–55CrossRefPubMed
22.
Zurück zum Zitat Streeter D, Spotnitz H, Patel D, Ross J, Sonnenblick E (1969) Fiber orientation in the canine left ventricle during diastole and systole. Circ Res 24:339–347CrossRefPubMed Streeter D, Spotnitz H, Patel D, Ross J, Sonnenblick E (1969) Fiber orientation in the canine left ventricle during diastole and systole. Circ Res 24:339–347CrossRefPubMed
23.
Zurück zum Zitat Teh I, McClymont D, Burton R, Maguire M, Whittington H, Lygate C, Kohl P, Schneider J (2016) Resolving fine cardiac structures in rats with high-resolution dti. Nat Sci Rep 6(30573):1–14 Teh I, McClymont D, Burton R, Maguire M, Whittington H, Lygate C, Kohl P, Schneider J (2016) Resolving fine cardiac structures in rats with high-resolution dti. Nat Sci Rep 6(30573):1–14
24.
Zurück zum Zitat Torrent Guasp F, Ballester M, Buckberg G, Carreras F, Flotats A, Carrio I, Ferreira A, Samuels L, Narula J (2001) Spatial orientation of the ventricular muscle band: physiologic contribution and surgical implications. J Thorac Cardiovasc Surg 122(2):389–92CrossRefPubMed Torrent Guasp F, Ballester M, Buckberg G, Carreras F, Flotats A, Carrio I, Ferreira A, Samuels L, Narula J (2001) Spatial orientation of the ventricular muscle band: physiologic contribution and surgical implications. J Thorac Cardiovasc Surg 122(2):389–92CrossRefPubMed
25.
Zurück zum Zitat Toussaint N, Stoeck C, Schaeffter T, Kozerke S, Sermesant M, Batchelor P (2013) In vivo human cardiac fibre architecture estimation using shape-based diffusion tensor processing. Med Image Anal 17:1243–1255CrossRefPubMed Toussaint N, Stoeck C, Schaeffter T, Kozerke S, Sermesant M, Batchelor P (2013) In vivo human cardiac fibre architecture estimation using shape-based diffusion tensor processing. Med Image Anal 17:1243–1255CrossRefPubMed
26.
Zurück zum Zitat Vázquez M, Arís R, Aguado-Sierra J, Houzeaux G, Santiago A, López M, Córdoba P, Rivero M, Cajas JC (2015) Alya red ccm: Hpc-based cardiac computational modeling. In: Selected topics of computational and experimental fluid mechanics pp 189–207 Vázquez M, Arís R, Aguado-Sierra J, Houzeaux G, Santiago A, López M, Córdoba P, Rivero M, Cajas JC (2015) Alya red ccm: Hpc-based cardiac computational modeling. In: Selected topics of computational and experimental fluid mechanics pp 189–207
Metadaten
Titel
Influence of fiber connectivity in simulations of cardiac biomechanics
verfasst von
D Gil
R Aris
A Borras
E Ramirez
R Sebastian
M Vazquez
Publikationsdatum
19.09.2018
Verlag
Springer International Publishing
Erschienen in
International Journal of Computer Assisted Radiology and Surgery / Ausgabe 1/2019
Print ISSN: 1861-6410
Elektronische ISSN: 1861-6429
DOI
https://doi.org/10.1007/s11548-018-1849-9

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