Abstract
Description of the cardiac myofiber architecture in pathological or even physiological conditions is essential for image-based modeling in electrophysiology or mechanical studies. While diffusion tensor imaging (DTI) is one of the best modalities to capture myofiber orientation of large mammalian hearts, validations of putative myofiber’s main orientation from DTI in whole hearts of large mammals is limited. First we design an experimental protocol for sheep (N = 1) and human (N = 1) whole hearts that combine a standardized sample preparation with high-resolution diffusion MRI at 600 µm3 using low angular resolution (6 directions) followed by a tissue air-drying approach coupled with X-ray imaging at 42 µm3. Secondly, we propose a standardized post-processing pipeline for symmetric multimodal mapping allowing the comparison of myofiber orientation computed from DTI and structure tensor imaging (STI), respectively. We then identified region-of-interest (ROI) exhibiting small or sharp spatial variations in myofiber orientation and compared the putative myofiber orientation for both methods. In conclusion, we show a good correspondence of structural features between the two imaging modalities and identify new unexpected and complex cardiomyocytes organization such as oscillating patterns or clear separation of opposing fiber-bundles.
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References
Cohn, J.N., Ferrari, R., Sharpe, N.: Cardiac remodeling—concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. JACC 35(3), 569–582 (2000)
Chen, J., Song, S.K., Liu, W., McLean, M., et al.: Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI. AJP 285(3), H946–H954 (2003)
Eder, R.A., et al.: Exercise-induced CITED4 expression is necessary for regional remodeling of cardiac microstructural tissue helicity. Commun. Biol. 5, 656 (2022)
Carruth, E.D., Teh, I., Schneider, J.E., et al.: Regional variations in ex-vivo diffusion tensor anisotropy are associated with cardiomyocyte remodeling in rats after left ventricular pressure overload. JCMR 22, 21 (2020)
Planinc, I., et al.: Comprehensive assessment of myocardial remodeling in ischemic heart disease by synchrotron propagation based X-ray phase contrast imaging. Sci. Rep. 11, 14020 (2021)
Milani-Nejad, N., Janssen, P.M.L.: Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol. Ther. 141(3), 235–249 (2014)
Sands, G.B., et al.: Automated imaging of extended tissue volumes using confocal microscopy. Microsc. Res. Tech. 67(5), 227–239 (2005)
Gonzalez-Tendero, A., et al.: Whole heart detailed and quantitative anatomy, myofibre structure and vasculature from X-ray phase-contrast synchrotron radiation-based micro computed tomography. Eur. Heart J. – Cardiovasc. Imaging 18(7), 732–741 (2017)
Sosnovik, D.E., Wang, R., Dai, G., et al.: Diffusion MR tractography of the heart. J. Cardiovasc. Magn. Reson. 11, 47 (2009)
Lombaert, H., Peyrat, J.M., Croisille, P., et al.: Human atlas of the cardiac fiber architecture: study on a healthy population. IEEE Trans. Med. Imaging 31(7), 1436–1447 (2012)
Pashakhanloo, F., et al.: Myofiber architecture of the human atria as revealed by submillimeter diffusion tensor imaging. Circ.: Arrhythm. Electrophysiol. 9(4), e004133 (2016)
Yang, F., et al.: Quantitative comparison of human myocardial fiber orientations derived from DTI and polarized light imaging. Phys. Med. Biol. 63(21), 215003 (2018)
Pallares-Lupon, N., et al.: Optimizing large organ scale micro computed tomography imaging in pig and human hearts using a novel air-drying technique. Arch. Cardiovasc. Dis. Suppl. 12, 268–269 (2021)
Magat, J., et al.: A groupwise registration and tractography framework for cardiac myofiber architecture description by diffusion MRI: An application to the ventricular junctions. PLoS One 17(7), e0271279 (2022)
Magat, J., et al.: 3D MRI of explanted sheep hearts with submillimeter isotropic spatial resolution: comparison between diffusion tensor and structure tensor imaging. Magn. Reson. Mater. Phys., Biol. Med. 34(5), 741–755 (2021)
Rodríguez-Padilla, J., et al.: Impact of intraventricular septal fiber orientation on cardiac electromechanical function. AJP 322(6), H936–H952 (2022)
Tournier, J.D., Calamante, F., Connelly, A.: Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35(4), 1459–1472 (2007)
Garcia-Canadilla, P., et al.: Myoarchitectural disarray of hypertrophic cardiomyopathy begins pre-birth. J. Anat. 235(5), 962–976 (2019)
Avants, B.B., Tustison, N., et al.: A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3), 2033–2044 (2011)
Hasdemir, C.A.N., Aktas, S., et al.: Demonstration of ventricular myocardial extensions into the pulmonary artery and aorta beyond the ventriculo-arterial junction. Pacing Clin. Electrophysiol. 30(4), 534–539 (2007)
Burton, R.A., Lee, P., et al.: Three-dimensional histology: tools and application to quantitative assessment of cell-type distribution in rabbit heart. Europace 16(suppl_4), iv86–iv95 (2014)
Lee, S.E., et al.: Three-dimensional cardiomyocytes structure revealed by diffusion tensor imaging and its validation using a tissue-clearing technique. Sci. Rep. 8(1), 1–11 (2018)
Teh, I., McClymont, D., et al.: Validation of diffusion tensor MRI measurements of cardiac microstructure with structure tensor synchrotron radiation imaging. J. Cardiovasc. Magn. Reson. 19(1), 1–14 (2017)
McClymont, D., et al.: The impact of signal-to-noise ratio, diffusion-weighted directions and image resolution in cardiac diffusion tensor imaging – insights from the ex-vivo rat heart. J. Cardiovasc. Magn. Reson. 19, 90 (2017)
Acknowledgements and Funding
All staff from LIRYC and CHU Bordeaux involved in the Human donor program CADENCE and HARMONICA project are gratefully acknowledged for their valuable contributions. This work received financial support from the French National Investments for the Future Programs: ANR-10-IAHU-04. HD figures are available at: https://github.com/valeryozenne/Cardiac-Structure-Database/tree/master/Article-4.
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Ozenne, V. et al. (2023). Symmetric Multimodal Mapping of Ex Vivo Cardiac Microstructure of Large Mammalian Whole Hearts for Volumetric Comparison of Myofiber Orientation Estimated from Diffusion MRI and MicroCT. In: Bernard, O., Clarysse, P., Duchateau, N., Ohayon, J., Viallon, M. (eds) Functional Imaging and Modeling of the Heart. FIMH 2023. Lecture Notes in Computer Science, vol 13958. Springer, Cham. https://doi.org/10.1007/978-3-031-35302-4_5
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