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      Why SIT Works: Normal Function Despite Typical Myofiber Pattern in Situs Inversus Totalis (SIT) Hearts Derived by Shear-induced Myofiber Reorientation

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          Abstract

          The left ventricle (LV) of mammals with Situs Solitus (SS, normal organ arrangement) displays hardly any interindividual variation in myofiber pattern and experimentally determined torsion. SS LV myofiber pattern has been suggested to result from adaptive myofiber reorientation, in turn leading to efficient pump and myofiber function. Limited data from the Situs Inversus Totalis (SIT, a complete mirror image of organ anatomy and position) LV demonstrated an essential different myofiber pattern, being normal at the apex but mirrored at the base. Considerable differences in torsion patterns in between human SIT LVs even suggest variation in myofiber pattern among SIT LVs themselves. We addressed whether different myofiber patterns in the SIT LV can be predicted by adaptive myofiber reorientation and whether they yield similar pump and myofiber function as in the SS LV. With a mathematical model of LV mechanics including shear induced myofiber reorientation, we predicted myofiber patterns of one SS and three different SIT LVs. Initial conditions for SIT were based on scarce information on the helix angle. The transverse angle was set to zero. During reorientation, a non-zero transverse angle developed, pump function increased, and myofiber function increased and became more homogeneous. Three continuous SIT structures emerged with a different location of transition between normal and mirrored myofiber orientation pattern. Predicted SIT torsion patterns matched experimentally determined ones. Pump and myofiber function in SIT and SS LVs are similar, despite essential differences in myocardial structure. SS and SIT LV structure and function may originate from same processes of adaptive myofiber reorientation.

          Author Summary

          Deciphering the structure-function relation in healthy hearts is important to understand cardiac pathologies. In the structure-function relation, the myofiber orientation patterns play a central role. Between people with normal organ arrangement (Situs Solitus, SS) this pattern is strikingly similar. Such consistency in myocardial structure might be the result of an adaptation process to accommodate for homogeneous distribution of myofiber strain across the wall and for optimal pump function. The heart of people with a mirror-imaged position of their organs (Situs Inversus Totalis, SIT) has a modified myofiber orientation pattern with respect to SS: normal at the LV apex, but mirrored at the base. Hence, studying SIT hearts provides a unique possibility 1) for understanding adaptation mechanisms related to myofiber orientation and mechanical load, and 2) to gain additional insights into the structure-function relations of the LV. Through mathematical modeling of LV mechanics, we have found that myofiber orientation pattern in both SS and SIT may originate from same processes of adaptive myofiber reorientation. After reorientation, pump and local myofiber function were found to be similar between SS and SIT as well: a remarkable finding when considering the large difference in myofiber orientation pattern.

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          Most cited references33

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          Characterization of the normal cardiac myofiber field in goat measured with MR-diffusion tensor imaging.

          Cardiac myofiber orientation is a crucial determinant of the distribution of myocardial wall stress. Myofiber orientation is commonly quantified by helix and transverse angles. Accuracy of reported helix angles is limited. Reported transverse angle data are incomplete. We measured cardiac myofiber orientation postmortem in five healthy goat hearts using magnetic resonance-diffusion tensor imaging. A novel local wall-bound coordinate system was derived from the characteristics of the fiber field. The transmural course of the helix angle corresponded to data reported in literature. The mean midwall transverse angle ranged from -12 +/- 4 degrees near the apex to +9.0 +/- 4 degrees near the base of the left ventricle, which is in agreement with the course predicted by Rijcken et al. (18) using a uniform load hypothesis. The divergence of the myofiber field was computed, which is a measure for the extent to which wall stress is transmitted through the myofiber alone. It appeared to be <0.07 mm(-1) throughout the myocardial walls except for the fusion sites between the left and right ventricles and the insertion sites of the papillary muscles.
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            Noninvasive measurement of shortening in the fiber and cross-fiber directions in the normal human left ventricle and in idiopathic dilated cardiomyopathy.

            Studies in anesthetized dogs have shown that myocardial fibers shorten approximately 8%. However, in the endocardium, shortening occurs to a much greater extent at 90 degrees to the fiber orientation ("cross-fiber shortening") than it does along the fiber direction. The purpose of this study was to estimate the extent of fiber and cross-fiber shortening in the normal human left ventricle and in patients with idiopathic dilated cardiomyopathy (IDC). Ten normal subjects and nine patients with IDC were imaged with magnetic resonance tissue tagging. Finite strain analysis was used to calculate endocardial and epicardial shortening in the fiber and cross-fiber directions using anatomic fiber angles from representative autopsy specimens as references. Anatomic fiber angles were not different between normal subjects and IDC patients. Epicardial fiber strain was -0.14+/-0.01 in normal subjects and -0.08+/-0.01 in IDC patients (P<.0001 versus normal subjects). Epicardial cross-fiber strain was -0.08+/-0.01 in normal subjects and -0.06+/-0.01 in IDC patients (P=NS). Endocardial fiber strain was -0.16+/-0.01 in normal subjects and -0.09+/-0.01 in IDC patients (P<.0001), and endocardial cross-fiber strain was -0.26+/-0.01 in normal subjects and -0.15+/-0.01 in IDC patients (P<.0001). Cross-fiber shortening was greater than fiber shortening at the endocardium in both normal subjects (P<.0001) and IDC patients (P<.05). In normal humans, the direction of maximal deformation aligns with the fiber direction in the epicardium but is perpendicular to the fiber direction in the endocardium. When strain in a coordinate system aligned to the fibers is estimated, cross-fiber shortening is found to be the dominant shortening strain at the endocardium. Normal fiber shortening is 15%, and this is markedly reduced in IDC. The normal transition in fiber orientation through the wall is not altered in IDC, and cross-fiber shortening is still the dominant strain at the endocardium, suggesting that interactions between myocardial layers persist in these patients.
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              Myocardial material parameter estimation: a non-homogeneous finite element study from simple shear tests.

              The passive material properties of myocardium play a major role in diastolic performance of the heart. In particular, the shear behaviour is thought to play an important mechanical role due to the laminar architecture of myocardium. We have previously compared a number of myocardial constitutive relations with the aim to extract their suitability for inverse material parameter estimation. The previous study assumed a homogeneous deformation. In the present study we relaxed the homogeneous assumption by implementing these laws into a finite element environment in order to obtain more realistic measures for the suitability of these laws in both their ability to fit a given set of experimental data, as well as their stability in the finite element environment. In particular, we examined five constitutive laws and compare them on the basis of (i) "goodness of fit": how well they fit a set of six shear deformation tests, (ii) "determinability": how well determined the objective function is at the optimal parameter fit, and (iii) "variability": how well determined the material parameters are over the range of experiments. Furthermore, we compared the FE results with those from the previous study.It was found that the same material law as in the previous study, the orthotropic Fung-type "Costa-Law", was the most suitable for inverse material parameter estimation for myocardium in simple shear.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                July 2012
                July 2012
                26 July 2012
                : 8
                : 7
                : e1002611
                Affiliations
                [1 ]Department of Biomedical Engineering/Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, The Netherlands
                [2 ]Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, The Netherlands
                University of California San Diego, United States of America
                Author notes

                Conceived and designed the experiments: ACR TD. Performed the experiments: ACR TD. Analyzed the data: MP WK PHMB TD. Contributed reagents/materials/analysis tools: WK PHMB. Wrote the paper: MP TD PHMB WK ACR.

                Article
                PCOMPBIOL-D-12-00251
                10.1371/journal.pcbi.1002611
                3406011
                22844239
                4e2abc92-c6f0-4720-af27-b0937be15f83
                Pluijmert et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 14 February 2012
                : 28 May 2012
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Computational Biology
                Biophysic Al Simulations
                Medicine
                Anatomy and Physiology
                Cardiovascular System

                Quantitative & Systems biology
                Quantitative & Systems biology

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