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

          M. Khan, Dudley J Pennell, A Maceira … (2005)
          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.
          Article 0 comments Cited 137 times – based on 0 reviews     Review now
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            4D flow CMR in assessment of valve-related ascending aortic disease.

            Michael D Hope, Thomas A. Hope, Stephen Crook … (2011)
            Blood flow imaging with 3-dimensional time-resolved, phase-contrast cardiac magnetic resonance (4-dimensional [4D] Flow) is an innovative and visually appealing method for studying cardiovascular disease that allows quantification of important secondary vascular parameters including wall shear stress. The hypothesis of this pilot study is that 4D Flow will become a powerful tool for characterizing the relationship of aortic valve-related flow dynamics, especially with bicuspid aortic valve (BAV), and progression of ascending aortic (AsAo) dilation. We identified 46 patients previously studied with 4D Flow: tricuspid aortic valve patients without valvular disease (n = 20), and BAV patients with either normal flow (n = 7) or eccentric systolic jets resulting in abnormal right-handed helical AsAo flow (n = 19). The subgroup of patients with BAV and eccentric systolic AsAo blood flow was found to have significantly and asymmetrically elevated wall shear stress. This increased hemodynamic burden may place them at risk for AsAo aneurysm. Copyright © 2011 American College of Cardiology Foundation. Published by Elsevier Inc. All rights reserved.
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              Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy

              Jonatan Eriksson, Ann F. Bolger, Tino Ebbers … (2012)
              Aims Patients with mild heart failure (HF) who are clinically compensated may have normal left ventricular (LV) stroke volume (SV). Despite this, altered intra-ventricular flow patterns have been recognized in these subjects. We hypothesized that, compared with normal LVs, flow in myopathic LVs would demonstrate a smaller proportion of inflow volume passing directly to ejection and diminished the end-diastolic preservation of the inflow kinetic energy (KE). Methods and results In 10 patients with dilated cardiomyopathy (DCM) (49 ± 14 years, six females) and 10 healthy subjects (44 ± 17 years, four females), four-dimensional MRI velocity and morphological data were acquired. A previously validated method was used to separate the LV end-diastolic volume (EDV) into four flow components based on the blood's locations at the beginning and end of the cardiac cycle. KE was calculated over the cardiac cycle for each component. The EDV was larger (P = 0.021) and the ejection fraction smaller (P < 0.001) in DCM compared with healthy subjects; the SV was equivalent (DCM: 77 ± 19, healthy: 79 ± 16 mL). The proportion of the total LV inflow that passed directly to ejection was smaller in DCM (P = 0.000), but the end-diastolic KE/mL of the direct flow was not different in the two groups (NS). Conclusion Despite equivalent LVSVs, HF patients with mild LV remodelling demonstrate altered diastolic flow routes through the LV and impaired preservation of inflow KE at pre-systole compared with healthy subjects. These unique flow-specific changes in the flow route and energetics are detectable despite clinical compensation, and may prove useful as subclinical markers of LV dysfunction.
              Article 0 comments Cited 62 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Alberto Aliseda: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 17 August 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 8
                Electronic Location Identifier: e0161391
                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.

                Author information
                http://orcid.org/0000-0003-3776-0671
                Article
                Publisher ID: PONE-D-16-06705
                DOI: 10.1371/journal.pone.0161391
                PMC ID: 4988651
                PubMed ID: 27532640
                SO-VID: 0efb57b3-45ea-46b6-b292-30f1b4cad495
                Copyright © © 2016 Svalbring et al
                License:

                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
                Date received : 16 February 2016
                Date accepted : 4 August 2016
                Page count
                Figures: 3, Tables: 4, Pages: 12
                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.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Computer and Information Sciences
                Subject: Data Acquisition
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Heart
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Heart
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Heart
                Subject: Cardiac Ventricles
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Heart
                Subject: Cardiac Ventricles
                Subject: Physical Sciences
                Subject: Chemistry
                Subject: Chemical Elements
                Subject: Gadolinium
                Subject: Physical Sciences
                Subject: Physics
                Subject: Classical Mechanics
                Subject: Motion
                Subject: Velocity
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Flow
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Flow
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Flow
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Flow
                Subject: Medicine and Health Sciences
                Subject: Hematology
                Subject: Blood
                Subject: Blood Flow
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Coronary Heart Disease
                Subject: Medicine and Health Sciences
                Subject: Cardiology
                Subject: Coronary Heart Disease
                Custom metadata
                Data Availability 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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