Multiscale cardiac imaging spanning the whole heart and its internal cellular architecture in a small animal model

Rykiel, Graham; López, Clàudia; Riesterer, Jessica L.; Fries, Ian; Deosthali, Sanika; Courchaine, Katherine; Maloyan, Alina; Thornburg, Kent L.; Rugonyi, Sandra

doi:10.7554/elife.58138

Cited by 15 publications

(12 citation statements)

References 75 publications

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“…Nevertheless, since the valve is only explanted when heart valve replacement is performed, studies at earlier stages of the disease are still lacking to obtain more information about the onset of aortic stenosis. As described in the section dedicated to whole-heart imaging, heart valves could be identified on whole-heart images obtained with both CE-CT and PC-CT, and their integrities have been evaluated [31,46,[56][57][58]64,67,71,80]. However, the resolution of these images remains relatively low compared to the sizes of the valves, and the valve positioning could not be described accurately.…”

Section: Measurement Of the Calcifications In Heart Valves And Assessmentioning

confidence: 99%

“…The integrity of the septum and the valves, the position of the chambers and the connection of the main vessels of the heart have been evaluated using both CE-CT [ 40 , 55 , 57 , 69 , 71 ] and PC-CT [ 31 , 80 ] to investigate cardiac diseases or malformations. Anatomical defects associated with complex cardiac diseases, such as intrauterine growth restriction and tetralogy of Fallot, were revealed in animal models.…”

Section: The Heartmentioning

confidence: 99%

“…With CE-CT, Stephenson et al reported that the cardiac conduction system could be distinguished from the myocardium itself based on differential staining of Lugol’s iodine in the conduction system and in the contractile myocardium [ 63 ]. Finally, when optimizing the preparation protocols, several research groups mentioned the importance of imaging such a complex organ with a multiscale approach, either by focusing on a region of interest (ROI) [ 31 , 88 , 89 , 90 ] or by combining several imaging modalities [ 71 ].…”

Section: The Heartmentioning

confidence: 99%

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A Review of Ex Vivo X-ray Microfocus Computed Tomography-Based Characterization of the Cardiovascular System

Leyssens

Pestiaux

Kerckhofs

2021

IJMS

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Cardiovascular malformations and diseases are common but complex and often not yet fully understood. To better understand the effects of structural and microstructural changes of the heart and the vasculature on their proper functioning, a detailed characterization of the microstructure is crucial. In vivo imaging approaches are noninvasive and allow visualizing the heart and the vasculature in 3D. However, their spatial image resolution is often too limited for microstructural analyses, and hence, ex vivo imaging is preferred for this purpose. Ex vivo X-ray microfocus computed tomography (microCT) is a rapidly emerging high-resolution 3D structural imaging technique often used for the assessment of calcified tissues. Contrast-enhanced microCT (CE-CT) or phase-contrast microCT (PC-CT) improve this technique by additionally allowing the distinction of different low X-ray-absorbing soft tissues. In this review, we present the strengths of ex vivo microCT, CE-CT and PC-CT for quantitative 3D imaging of the structure and/or microstructure of the heart, the vasculature and their substructures in healthy and diseased state. We also discuss their current limitations, mainly with regard to the contrasting methods and the tissue preparation.

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Section: Measurement Of the Calcifications In Heart Valves And Assessmentioning

confidence: 99%

Section: The Heartmentioning

confidence: 99%

Section: The Heartmentioning

confidence: 99%

See 1 more Smart Citation

A Review of Ex Vivo X-ray Microfocus Computed Tomography-Based Characterization of the Cardiovascular System

Leyssens

Pestiaux

Kerckhofs

2021

IJMS

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“…Moreover, collagen deposition or different biological structures as nerves or vessels may impact the cytoarchitecture analysis (Greiner et al, 2018 ). Recently, Phase-Contrast micro-CT was combined with high-resolution imaging techniques such as Serial-Block-Face Scanning Electron Microscopy (SBF-SEM) or Focused Ion Beam-Scanning Electron Microscopy (FIB-SEM) to perform multi-scale investigations on the heart organization (Rykiel et al, 2020 ), and accurate analysis of the 3D organization of contractile units (Pinali et al, 2015 ; Willingham et al, 2020 ), although limiting 3D reconstruction with nanometric resolution at micrometers-sized volumes.…”

Section: Introductionmentioning

confidence: 99%

Quantification of Myocyte Disarray in Human Cardiac Tissue

et al. 2021

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Proper three-dimensional (3D)-cardiomyocyte orientation is important for an effective tension production in cardiac muscle. Cardiac diseases can cause severe remodeling processes in the heart, such as cellular misalignment, that can affect both the electrical and mechanical functions of the organ. To date, a proven methodology to map and quantify myocytes disarray in massive samples is missing. In this study, we present an experimental pipeline to reconstruct and analyze the 3D cardiomyocyte architecture in massive samples. We employed tissue clearing, staining, and advanced microscopy techniques to detect sarcomeres in relatively large human myocardial strips with micrometric resolution. Z-bands periodicity was exploited in a frequency analysis approach to extract the 3D myofilament orientation, providing an orientation map used to characterize the tissue organization at different spatial scales. As a proof-of-principle, we applied the proposed method to healthy and pathologically remodeled human cardiac tissue strips. Preliminary results suggest the reliability of the method: strips from a healthy donor are characterized by a well-organized tissue, where the local disarray is log-normally distributed and slightly depends on the spatial scale of analysis; on the contrary, pathological strips show pronounced tissue disorganization, characterized by local disarray significantly dependent on the spatial scale of analysis. A virtual sample generator is developed to link this multi-scale disarray analysis with the underlying cellular architecture. This approach allowed us to quantitatively assess tissue organization in terms of 3D myocyte angular dispersion and may pave the way for developing novel predictive models based on structural data at cellular resolution.

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“…Several cardiovascular imaging techniques such as micro-computed tomography (μCT) [7,8] and phase-contrast CT [9][10][11][12] combined with structure tensor image (STI) analysis have demonstrated their ability to map the cardiac fiber organization with a spatial resolution close to 10 µm isotropic [13].…”

Section: Introductionmentioning

confidence: 99%

A groupwise registration and tractography framework for cardiac myofiber architecture description by diffusion MRI: an application to the ventricular junctions

Magat

Yon

Bihan-Poudec

et al. 2021

Preprint

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Background: Knowledge of the normal myocardial-myocyte orientation could theoretically allow the definition of relevant quantitative biomarkers in clinical routine to diagnose heart pathologies. A whole heart diffusion tensor template representative of the global myofiber organization over species is therefore crucial for comparisons across populations. In this study, we developed a template-based and tractography framework to resolve the global myofiber arrangement of large mammalian hearts. To demonstrate the potential application of the proposed method, a novel description of sub-regions in the intraventricular septum is presented. Methods: Three explanted sheep (ovine) hearts (size ~12×8×6 cm3 , heart weight ~ 150 g ) were perfused with contrast agent and fixative and imaged in a 9.4T magnet. A group-wise registration of high-resolution anatomical and diffusion-weighted images were performed to generated anatomical and diffusion tensor templates. Diffusion tensor metrics (eigenvalues, eigenvectors, fractional anisotropy...) were computed to provide a quantitative and spatially-resolved analysis of cardiac microstructure. Then tractography was performed using deterministic and probabilistic algorithms and used for different purposes: i) Visualization of myofiber architecture, ii) Segmentation of sub-area depicting the same fiber organization, iii) Seeding and Tract Editing. Finally, dissection was performed to confirm the existence of macroscopic structures identified in the diffusion tensor template. Results: The template creation takes advantage of high-resolution anatomical and diffusion-weighted images obtained at an isotropic resolution of 150 μm and 600 μm respectively, covering ventricles and atria and providing information on the normal myocardial architecture. The diffusion metric distributions from the template were found close to the one of the individual samples validating the registration procedure. Small new sub-regions exhibiting spatially sharp variations in fiber orientation close to the junctions of the septum and ventricles were identified. Each substructure was defined and represented using streamlines. The existence of a bundle of fibers in the posterior junction was validated by anatomical dissection. A complex structural organization of the anterior junction in comparison to the posterior junction was evidenced by the high-resolution acquisition. Conclusions: A new framework combining cardiac template generation and tractography was applied on the whole sheep heart. The framework can be used for anatomical investigation, characterization of microstructure and visualization of myofiber orientation across samples. Finally, a novel description of the ventricular junction in large mammalian hearts was proposed.

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Multiscale cardiac imaging spanning the whole heart and its internal cellular architecture in a small animal model

Cited by 15 publications

References 75 publications

A Review of Ex Vivo X-ray Microfocus Computed Tomography-Based Characterization of the Cardiovascular System

A Review of Ex Vivo X-ray Microfocus Computed Tomography-Based Characterization of the Cardiovascular System

Quantification of Myocyte Disarray in Human Cardiac Tissue

A groupwise registration and tractography framework for cardiac myofiber architecture description by diffusion MRI: an application to the ventricular junctions

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