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      Altered Diastolic Flow Patterns and Kinetic Energy in Subtle Left Ventricular Remodeling and Dysfunction Detected by 4D Flow MRI

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          Abstract

          Aims

          4D flow magnetic resonance imaging (MRI) allows quantitative assessment of left ventricular (LV) function according to characteristics of the dynamic flow in the chamber. Marked abnormalities in flow components’ volume and kinetic energy (KE) have previously been demonstrated in moderately dilated and depressed LV’s compared to healthy subjects. We hypothesized that these 4D flow-based measures would detect even subtle LV dysfunction and remodeling.

          Methods and Results

          We acquired 4D flow and morphological MRI data from 26 patients with chronic ischemic heart disease with New York Heart Association (NYHA) class I and II and with no to mild LV systolic dysfunction and remodeling, and from 10 healthy controls. A previously validated method was used to separate the LV end-diastolic volume (LVEDV) into functional components: direct flow, which passes directly to ejection, and non-ejecting flow, which remains in the LV for at least 1 cycle. The direct flow and non-ejecting flow proportions of end-diastolic volume and KE were assessed. The proportions of direct flow volume and KE fell with increasing LVEDV-index (LVEDVI) and LVESV-index (LVESVI) (direct flow volume r = -0.64 and r = -0.74, both P<0.001; direct flow KE r = -0.48, P = 0.013, and r = -0.56, P = 0.003). The proportions of non-ejecting flow volume and KE rose with increasing LVEDVI and LVESVI (non-ejecting flow volume: r = 0.67 and r = 0.76, both P<0.001; non-ejecting flow KE: r = 0.53, P = 0.005 and r = 0.52, P = 0.006). The proportion of direct flow volume correlated moderately to LVEF (r = 0.68, P < 0.001) and was higher in a sub-group of patients with LVEDVI >74 ml/m 2 compared to patients with LVEDVI <74 ml/m 2 and controls (both P<0.05).

          Conclusion

          Direct flow volume and KE proportions diminish with increased LV volumes, while non-ejecting flow proportions increase. A decrease in direct flow volume and KE at end-diastole proposes that alterations in these novel 4D flow-specific markers may detect LV dysfunction even in subtle or subclinical LV remodeling.

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          Most cited references 20

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          Normalized left ventricular systolic and diastolic function by steady state free precession cardiovascular magnetic resonance.

          We used state of the art CMR to define ranges for normal left ventricular volumes and systolic/diastolic function normalized to the influence of gender, body surface area and age. New CMR normalized ranges were modeled and displayed in graphical form for clinical use, with normalization for body surface area, gender, and age. The determination of normality, or the severity of abnormality, depends on the use of the appropriate reference ranges normalized to all 3 variables. These novel data have particular importance for clinical practice and clinical trials using CMR.
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            Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance.

            The transit of blood through the beating heart is a basic aspect of cardiovascular physiology which remains incompletely studied. Quantification of the components of multidirectional flow in the normal left ventricle (LV) is lacking, making it difficult to put the changes observed with LV dysfunction and cardiac surgery into context. Three dimensional, three directional, time resolved magnetic resonance phase-contrast velocity mapping was performed at 1.5 Tesla in 17 normal subjects, 6 female, aged 44+/-14 years (mean+/-SD). We visualized and measured the relative volumes of LV flow components and the diastolic changes in inflowing kinetic energy (KE). Of total diastolic inflow volume, 44+/-11% followed a direct, albeit curved route to systolic ejection (videos 1 and 2), in contrast to 11% in a subject with mildly dilated cardiomyopathy (DCM), who was included for preliminary comparison (video 3). In normals, 16+/-8% of the KE of inflow was conserved to the end of diastole, compared with 5% in the DCM patient. Blood following the direct route lost or transferred less of its KE during diastole than blood that was retained until the next beat (1.6+/-1.0 millijoules vs 8.2+/-1.9 millijoules, p<0.05); whereas, in the DCM patient, the reduction in KE of retained inflow was 18-fold greater than that of the blood tracing the direct route. Multidimensional flow mapping can measure the paths, compartmentalization and kinetic energy changes of blood flowing into the LV, demonstrating differences of KE loss between compartments, and potentially between the flows in normal and dilated left ventricles.
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              Quantification of left and right ventricular kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements.

              We aimed to quantify kinetic energy (KE) during the entire cardiac cycle of the left ventricle (LV) and right ventricle (RV) using four-dimensional phase-contrast magnetic resonance imaging (MRI). KE was quantified in healthy volunteers (n = 9) using an in-house developed software. Mean KE through the cardiac cycle of the LV and the RV were highly correlated (r(2) = 0.96). Mean KE was related to end-diastolic volume (r(2) = 0.66 for LV and r(2) = 0.74 for RV), end-systolic volume (r(2) = 0.59 and 0.68), and stroke volume (r(2) = 0.55 and 0.60), but not to ejection fraction (r(2) < 0.01, P = not significant for both). Three KE peaks were found in both ventricles, in systole, early diastole, and late diastole. In systole, peak KE in the LV was lower (4.9 ± 0.4 mJ, P = 0.004) compared with the RV (7.5 ± 0.8 mJ). In contrast, KE during early diastole was higher in the LV (6.0 ± 0.6 mJ, P = 0.004) compared with the RV (3.6 ± 0.4 mJ). The late diastolic peaks were smaller than the systolic and early diastolic peaks (1.3 ± 0.2 and 1.2 ± 0.2 mJ). Modeling estimated the proportion of KE to total external work, which comprised ∼0.3% of LV external work and 3% of RV energy at rest and 3 vs. 24% during peak exercise. The higher early diastolic KE in the LV indicates that LV filling is more dependent on ventricular suction compared with the RV. RV early diastolic filling, on the other hand, may be caused to a higher degree of the return of the atrioventricular plane toward the base of the heart. The difference in ventricular geometry with a longer outflow tract in the RV compared with the LV explains the higher systolic KE in the RV.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                17 August 2016
                2016
                : 11
                : 8
                Affiliations
                [1 ]Department of Medical and Health Sciences, Division of Cardiovascular Medicine, Linköping University, Linköping, Sweden
                [2 ]Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden
                [3 ]Department of Medicine, University of California San Francisco, San Francisco, California, United States of America
                [4 ]Department of Clinical Physiology, Department of Medical and Health Sciences, Linköping University, Linköping, Sweden
                University of Washington, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceived and designed the experiments: ES AFB CJC.

                • Performed the experiments: ES AF JE.

                • Analyzed the data: ES AF J. Eriksson CJC.

                • Contributed reagents/materials/analysis tools: J. Eriksson AF PD TE.

                • Wrote the paper: ES CJC AFB.

                • Recruited the subjects: J. Engvall. Performed statistical analysis: ES. Supervised the study: CJC. Critically revision of manuscript: J. Eriksson AF PD TE J. Engvall.

                Article
                PONE-D-16-06705
                10.1371/journal.pone.0161391
                4988651
                27532640
                © 2016 Svalbring 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.

                Page count
                Figures: 3, Tables: 4, Pages: 12
                Product
                Funding
                This work was funded by Swedish Heart Lung foundation (grant number: 20140398) [ https://www.hjart-lungfonden.se/HLF/Om-Hjart-lungfonden/About-HLF/], Receiver: CJC; Swedish Research Council (grant number: 2014-6191) [ http://www.vr.se], Receiver: TE; European Union FP7 (grant number: 223615) [ https://ec.europa.eu/research/fp7/index_en.cfm], Receiver: TE; Medical Research Council of Southeast Sweden (grant number: FORSS-35141, FORSS-88731, FORSS-157921) [ http://www.fou.nu/is/forss/], Receiver: JE; County Council of Ostergotland/Heart and Medicine Center (grant number: 20090120) [ http://www.regionostergotland.se/hmc/], Receiver: JE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Custom metadata
                All relevant data are within the paper and its Supporting Information files. The underlying MRI and Echocardiographic data sets are available from the Linköping University Hospital for researchers who meet the criteria for access to confidential data.
 Regarding the underlying data sets the IRB form states that the data obtained from the patients will be stored on secure computers within the Linköping University Hospital.

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