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Original Contribution| Volume 49, ISSUE 5, P1238-1247, May 2023

Backscatter tensor imaging and 3D speckle tracking for simultaneous ex vivo structure and deformation measurement of myocardium

  • John M. Cormack
    Correspondence
    Corresponding author at 3550 Terrace Street, Pittsburgh, PA 15261.
    Affiliations
    Center for Ultrasound Molecular Imaging and Therapeutics, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15261-1909, USA

    Division of Cardiology, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA
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  • Marc A. Simon
    Affiliations
    Division of Cardiology, Department of Medicine, University of California San Francisco, San Francisco, California 94143, USA
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  • Kang Kim
    Affiliations
    Center for Ultrasound Molecular Imaging and Therapeutics, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15261-1909, USA

    Division of Cardiology, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA

    Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, 15213, USA
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      Abstract

      Objective: Biaxial mechanical testing is a common method for elucidation of mechanical properties of excised ventricular myocardium, especially in the context of structural remodeling that accompanies heart disease. Current imaging strategies in biaxial testing are based on optical camera imaging of the tissue surface, thus providing no information about the tissue microstructure and limiting strain measurements to two dimensions. Here, these limitations are overcome by replacing the camera with ultrasound imaging in order to measure both transmural fiber orientation and 3D tissue deformation during biaxial testing. Methods: Quasi-static biaxial mechanical testing is applied to four samples of excised porcine ventricular myocardium (two left- and two right-ventricular tissues). During testing, a rotational scan of an ultrasound linear array provides data for both backscatter tensor imaging and 3D speckle tracking, from which transmural fiber orientation and tissue deformation are computed, respectively. Ultrasound-derived fiber orientation and tissue strain are validated against histology and camera surface imaging, respectively. Discussion: Ultrasound-derived fiber angle and tissue strain exhibit good accuracy, with root-mean-square errors of 9.9° and 1.2% strain, respectively. Further investigation into the optimization of backscatter tensor imaging is warranted. Replacing the rotational scan of a linear array with volume imaging with a matrix array will improve the technique. Conclusion: Ultrasound imaging can replace the optical camera measurement during biaxial mechanical testing of ventricular myocardium in order to accurately provide measurements of transmural fiber orientation and tissue strain. In situ knowledge of transmural fiber structure and tissue deformation can enhance the inverse problem used to determine tissue mechanical properties from biaxial testing.

      Keywords

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      References

        • Streeter D.D.
        • Bassett D.L.
        An engineering analysis of myocardial fiber orientation in pig’s left ventricle in systole.
        Anat. Rec. 1996; 155: 503-512
        • Avazmohammadi R.
        • Soares J.S.
        • Li D.S.
        • Eperjesi T.
        • Pilla J.
        • Gorman R.C.
        • Sacks M.S.
        On the in vivo systolic compressibility of left ventricular free wall myocardium in the normal and infarcted heart.
        J. Biomech. 2020; 107: 109767
        • Chen J.
        • S-K S.
        • Liu W.
        • McLean M.
        • Allen J.S.
        • Tan J.
        • Wickline S.A.
        • Yu X.
        Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI.
        Am. J. Physiol. Heart Circ. Physiol. 2003; 285: H946-H954
        • Chen X.
        • Xie H.
        • Kim K.
        • Jia C.
        • Rubin J.M.
        • O’Donnell M.
        3-D correlation-based speckle tracking.
        Ultrasonic Imaging. 2005; 27: 27-36
        • Cormack J.M.
        • Simon M.A.
        • Kim K.
        Refraction-corrected backscatter tensor imaging of excised porcine ventricular myocardium.
        JASA Express Lett. 2022; 2: 092001
        • Derode A.
        • Fink M.
        Partial coherence of transient ultrasonic fields in anisotropic random media: Application to coherent echo detection.
        J. Acoust. Soc. Am. 1997; 101: 690-704
        • Fixsen L.S.
        • RGP L.
        Ultrasound-based estimation of fibre-directional strain: a simulation study.
        Ultrasound Med. Biol. 2022; 48: 1785-1796
        • Hayabuchi Y.
        • Homma Y.
        • Kagami S.
        Right ventricular myocardial stiffness and relaxation components by kinematic model-based transtricuspid flow analysis in children and adolescents with pulmonary arterial hypertension.
        Ultrasound Med. Biol. 2019; 45: 1999-2009
        • Hill M.R.
        • Simon M.A.
        • Valdez-Jasso D.
        • Zhang W.
        • Champion H.C.
        • Sacks M.S.
        Structural and mechanical adaptations of right ventricle free wall myocardium to pressure overload.
        Ann. Biomed. Eng. 2014; 42: 2451-2465
        • Hooks D.A.
        • Trew M.L.
        • Caldwell B.J.
        • Sands G.B.
        • LeGrice I.J.
        • Smaill B.H.
        Laminar arrangement of ventricular myocytes influences electrical behavior of the heart.
        Circ. Res. 2007; 101: e103-e112
        • Mallart R.
        • Fink M.
        Adaptive focusing in scattering media through sound-speed inhomogeneities: The van Cittert Zernike approach and focusing criterion.
        J. Acoust. Soc. Am. 1994; 96: 3721-3732
        • McEnvoy E.
        • . Holzapfel G.A.
        • McGarry P.
        Compressibility and anisotropy of the ventricular myocardium: Experimental analysis and microstructural modeling.
        J. Biomech. Eng. 2018; 140: 081004
        • Nemavhola F.
        Study of biaxial mechanical properties of the passive pig heart: Material characterization and categorization of regional differences.
        Int. J. Mech. Mater. Eng. 2021; 16: 14
        • Noordegraaf A.V.
        • Groeneveldt J.A.
        • . Bogaard H.J.
        Pulmonary hypertension.
        Eur. Respir. Rev. 2016; 25: 4-11
        • Papadacci C.
        • Finel V.
        • Provost J.
        • Villemain O.
        • Bruneval P.
        • J-L G.
        • Tanter M.
        • Fink M.
        • Pernot M.
        Imaging the dynamics of cardiac fiber orientation in vivo using 3D ultrasound backscatter tensor imaging.
        Sci. Rep. 2017; 7: 830
        • Papadacci C.
        • Tanter M.
        • Pernot M.
        • Fink M.
        Ultrasound backscatter tensor imaging (BTI): Analysis of the spatial coherence of ultrasonic speckle in anisotropic tissues.
        IEEE Trans. Ult. Ferr. and Freq. Cont. 2014; 61: 968-996
        • Park D.W.
        • Sebastiani A.
        • Yap C.H.
        • Simon M.A.
        • Kim K.
        Quantification of coupled stiffness and fiber orientation remodeling in hypertensive rat right-ventricular myocardium using 3D ultrasound speckle tracking with biaxial testing.
        PLoS ONE. 2016; 11: e1065320
        • Püspoki Z.
        • Storath M.
        • Sage D.
        • Unser M.
        Transforms and operators for directional bioimage analysis: a survey.
        Adv. Anat. Embryol. Cell Biol. 2016; 219: 69-93
        • Ramalli A.
        • Santos P.
        • D’hooge J.
        Ultrasound imaging of cardiac fiber orientation: What are we looking at? Proc.
        IEEE Int Ultrason Symp. 2018; : 1-9
        • Ryo K.
        • Goda A.
        • Onishi T.
        • Delgado-Montero A.
        • Tayal B.
        • Champion H.C.
        • Simon M.A.
        • . Mathier M.A.
        • Gladwin M.T.
        • Gorcsan III, J.
        Characterization of right ventricular remodeling in pulmonary hypertension associated with patient outcomes by 3-dimensional wall motion tracking echocardiography.
        Circ. Cardiovascular Imag. 2015; 8: e003176
        • Sacks M.S.
        A method for planar biaxial mechanical testing that includes in-plane shear.
        J. Biomech. Eng. 1999; 121: 551-555
        • Sharifi Kia D.
        • Benza E.
        • Bachman T.N.
        • Tushak C.
        • Kim K.
        • Simon M.A.
        Angiotensin receptor-neprilysin inhibition attenuates right ventricular remodeling in pulmonary hypertension.
        J. Am. Heart. Assoc. 2020; 9: e015708
        • Sharifi Kia D.
        • Fortunato R.
        • . Maiti S.
        • Simon M.A.
        • Kim K.
        An exploratory assessment of stretch-induced transmural myocardial fiber kinematics in right ventricular pressure overload.
        Sci. Rep. 2021; 11: 3587
        • Sharifi Kia D.
        • Shen Y.
        • Bachman T.N.
        • Goncharova E.A.
        • Kim K.
        • Simon M.A.
        The effects of healthy aging on right ventricular structure and biomechanical properties: A pilot study.
        Front. Med. 2022; 8: 751338
        • Sommer G.
        • . Schriefl A.J.
        • Andrä M.
        • Sacherer M.
        • Viertler C.
        • Wolinski H.
        • Holzapfel G.A.
        Biomechanical properties and microstructure of human ventricular myocardium.
        Acta Biomat. 2015; 24: 172-192
        • Sommer G.
        • DCh H.
        • Andrä M.
        • Sacherer M.
        • Viertler C.
        • Regitnig P.
        • Holzapfel G.A.
        Quantification of shear deformations and corresponding stresses in the biaxially tested human myocardium.
        Annals of Biomed. Eng. 2015; 43: 2334-2348
        • 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. Research. 2005; 96: 244-251
        • Yap C.H.
        • Park D.W.
        • Dutta D.
        • Simon M.
        • Kim K.
        Methods for using 3-D ultrasound speckle tracking in biaxial mechanical testing of biological tissue samples.
        Ultrasound Med. Biol. 2015; 41: 1029-1042