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Journal of Cardiovascular Magnetic Resonance
Published in: Journal of Cardiovascular Magnetic Resonance 1/2021

Open Access 01-12-2021 | Pulmonary Valve Replacement | Research

Moving beyond size: vorticity and energy loss are correlated with right ventricular dysfunction and exercise intolerance in repaired Tetralogy of Fallot

Authors: Yue-Hin Loke, Francesco Capuano, Vincent Cleveland, Jason G. Mandell, Elias Balaras, Laura J. Olivieri

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2021

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Abstract

Background

The global effect of chronic pulmonary regurgitation (PR) on right ventricular (RV) dilation and dysfunction in repaired Tetralogy of Fallot (rTOF) patients is well studied by cardiovascular magnetic resonance (CMR). However, the links between PR in the RV outflow tract (RVOT), RV dysfunction and exercise intolerance are not clarified by conventional measurements. Not all patients with RV dilation share the same intracardiac flow characteristics, now measurable by time resolved three-dimensional phase contrast imaging (4D flow). In our study, we quantified regional vorticity and energy loss in rTOF patients and correlated these parameters with RV dysfunction and exercise capacity.

Methods

rTOF patients with 4D flow datasets were retrospectively analyzed, including those with transannular/infundibular repair and conduit repair. Normal controls and RV dilation patients with atrial-level shunts (Qp:Qs > 1.2:1) were included for comparison. 4D flow was post-processed using IT Flow (Cardioflow, Japan). Systolic/diastolic vorticity (ω, 1/s) and viscous energy loss (VEL, mW) in the RVOT and RV inflow were measured. To characterize the relative influence of diastolic vorticity in the two regions, an RV Diastolic Vorticity Quotient (ωRVOT-Diastole/ωRV Inflow-Diastole, RV-DVQ) was calculated. Additionally, RVOT Vorticity Quotient (ωRVOT-Diastole/ωRVOT-Systole, RVOT-VQ) and RVOT Energy Quotient (VELRVOT-Diastole/VELRVOT-Systole, RVOT-EQ) was calculated. In rTOF, measurements were correlated against conventional CMR and exercise stress test results.

Results

58 rTOF patients, 28 RV dilation patients and 12 controls were included. RV-DVQ, RVOT-VQ, and RVOT-EQ were highest in rTOF patients with severe PR compared to rTOF patients with non-severe PR, RV dilation and controls (p < 0.001). RV-DVQ positively correlated with RV end-diastolic volume (0.683, p < 0.001), PR fraction (0.774, p < 0.001) and negatively with RV ejection fraction (− 0.521, p = 0.003). Both RVOT-VQ, RVOT-EQ negatively correlated with VO2-max (− 0.587, p = 0.008 and − 0.617, p = 0.005) and % predicted VO2-max (− 0.678, p = 0.016 and − 0.690, p = 0.001).

Conclusions

In rTOF patients, vorticity and energy loss dominate the RVOT compared to tricuspid inflow, correlating with RV dysfunction and exercise intolerance. These 4D flow-based measurements may be sensitive biomarkers to guide surgical management of rTOF patients.
Literature
1.
Bhatt AB, Foster E, Kuehl K, Alpert J, Brabeck S, Crumb S, et al. Congenital heart disease in the older adult: a scientific statement from the American Heart Association. Circulation. 2015;131(21):1884–931.PubMedCrossRef
2.
Stout KK, Daniels CJ, Aboulhosn JA, Bozkurt B, Broberg CS, Colman JM, et al. 2018 AHA/ACC guideline for the management of adults with congenital heart disease: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines. Circulation. 2019;139:14. https://​doi.​org/​10.​1161/​CIR.​0000000000000603​.CrossRef
3.
4.
Wald RM, Valente AM, Gauvreau K, Babu-Narayan SV, Assenza GE, Schreier J, et al. Cardiac magnetic resonance markers of progressive RV dilation and dysfunction after tetralogy of Fallot repair. Heart. 2015;101(21):1724–30.PubMedCrossRef
5.
Zaidi SJ, Cossor W, Singh A, Maffesanti F, Kawaji K, Woo J, et al. Three-dimensional analysis of regional right ventricular shape and function in repaired tetralogy of Fallot using cardiovascular magnetic resonance. Clin Imaging. 2018;52:106–12.PubMedPubMedCentralCrossRef
6.
Heng EL, Gatzoulis MA, Uebing A, Sethia B, Uemura H, Smith GC, et al. Immediate and midterm cardiac remodeling after surgical pulmonary valve replacement in adults with repaired Tetralogy of Fallot: a prospective cardiovascular magnetic resonance and clinical study. Circulation. 2017;136(18):1703–13.PubMedPubMedCentralCrossRef
7.
Shen W-C, Chen C-A, Chang C-I, Chen Y-S, Huang S-C, Wu M-H, et al. Outflow tract geometries are associated with adverse outcome indicators in repaired tetralogy of Fallot. J Thoracic Cardiovasc Surg. 2020;225:6702.
8.
Avesani M, Borrelli N, Krupickova S, Sabatino J, Donne GD, Ibrahim A, et al. Echocardiography and cardiac magnetic resonance in children with repaired tetralogy of Fallot: new insights in cardiac mechanics and exercise capacity. Int J Cardiol. 2020;321:144–9.PubMedCrossRef
9.
Ta HT, Critser PJ, Alsaied T, Germann J, Powell AW, Redington AN, et al. Modified ventricular global function index correlates with exercise capacity in repaired Tetralogy of Fallot. J Am Heart Assoc. 2020;9(14):e016308.PubMedPubMedCentralCrossRef
10.
Lumens J, Fan CS, Walmsley J, Yim D, Manlhiot C, Dragulescu A, et al. Relative impact of right ventricular electromechanical dyssynchrony versus pulmonary regurgitation on right ventricular dysfunction and exercise intolerance in patients after repair of Tetralogy of Fallot. J Am Heart Assoc. 2019;8:2. https://​doi.​org/​10.​1161/​JAHA.​118.​010903.CrossRef
11.
Rashid I, Mahmood A, Ismail TF, O’Meagher S, Kutty S, Celermajer D, et al. Right ventricular systolic dysfunction but not dilatation correlates with prognostically significant reductions in exercise capacity in repaired Tetralogy of Fallot. Eur Heart J Cardiovasc Imag. 2020;21(8):906–13.CrossRef
12.
Hirtler D, Garcia J, Barker AJ, Geiger J. Assessment of intracardiac flow and vorticity in the right heart of patients after repair of tetralogy of Fallot by flow-sensitive 4D MRI. Eur Radiol. 2016;26(10):3598–607.PubMedPubMedCentralCrossRef
13.
Francois CJ, Srinivasan S, Schiebler ML, Reeder SB, Niespodzany E, Landgraf BR, et al. 4D cardiovascular magnetic resonance velocity mapping of alterations of right heart flow patterns and main pulmonary artery hemodynamics in tetralogy of Fallot. J Cardiovasc Magn Reson. 2012;14(1):16.PubMedPubMedCentralCrossRef
14.
Fredriksson A, Trzebiatowska-Krzynska A, Dyverfeldt P, Engvall J, Ebbers T, Carlhäll C-J. Turbulent kinetic energy in the right ventricle: Potential MR marker for risk stratification of adults with repaired Tetralogy of Fallot. J Magn Reson Imaging. 2018;47(4):1043–53.PubMedCrossRef
15.
Robinson JD, Rose MJ, Joh M, Jarvis K, Schnell S, Barker AJ, et al. 4-D flow magnetic-resonance-imaging-derived energetic biomarkers are abnormal in children with repaired tetralogy of Fallot and associated with disease severity. Pediatr Radiol. 2019;49(3):308–17.PubMedCrossRef
16.
Mikhail A, Labbio GD, Darwish A, Kadem L. How pulmonary valve regurgitation after tetralogy of fallot repair changes the flow dynamics in the right ventricle: An in vitro study. Med Eng Phys. 2020;83:48–55.PubMedCrossRef
17.
Moceri P, Duchateau N, Gillon S, Jaunay L, Baudouy D, Squara F, et al. Three-dimensional right ventricular shape and strain in congenital heart disease patients with right ventricular chronic volume loading. Eur Heart J. 2020;5:jeaa189.
18.
Capuano F, Loke YH, Olivieri L, Balaras E. Computational modeling of right ventricle flow dynamics in congenital heart disease. In: García-Villalba M, Kuerten H, Salvetti MV, editors. Direct and large eddy simulation XII. Cham: Springer; 2020. p. 477–83.CrossRef
19.
Capuano F, Romano L, Loke YH, Dellegrottaglie S, Notorio M, Cocchia R, et al. P1449 CMR-driven computational modeling of right ventricular flow dynamics. Eur Heart J. 2020;21(1):jez319.877.
20.
21.
Loke YH, Krieger A, Sable C, Olivieri L. Novel uses for three-dimensional printing in congenital heart disease. Curr Pediatr Rep. 2016;4(2):28–34.CrossRef
22.
23.
Wald RM, Haber I, Wald R, Valente AM, Powell AJ, Geva T. Effects of regional dysfunction and late gadolinium enhancement on global right ventricular function and exercise capacity in patients with repaired tetralogy of Fallot. Circulation. 2009;119(10):1370–7.PubMedPubMedCentralCrossRef
24.
Nakaji K, Itatani K, Tamaki N, Morichi H, Nakanishi N, Takigami M, et al. Assessment of biventricular hemodynamics and energy dynamics using lumen-tracking 4D flow MRI without contrast medium. J Cardiol. 2021;914:508.
25.
Cibis M, Jarvis K, Markl M, Rose M, Rigsby C, Barker AJ, et al. The effect of resolution on viscous dissipation measured with 4D flow MRI in patients with Fontan circulation: evaluation using computational fluid dynamics. J Biomech. 2015;48(12):2984–9.PubMedPubMedCentralCrossRef
26.
Mercer-Rosa L, Yang W, Kutty S, Rychik J, Fogel M, Goldmuntz E. Quantifying pulmonary regurgitation and right ventricular function in surgically repaired Tetralogy Of Fallot: a comparative analysis of echocardiography and magnetic resonance imaging. Circ Cardiovasc Imaging. 2012;5(5):637–43.PubMedPubMedCentralCrossRef
27.
Bhat M, Goldmuntz E, Fogel MA, Rychik J, Mercer-Rosa L. Longitudinal validation of the diastolic to systolic time-velocity integral ratio as a Doppler-derived measure of pulmonary regurgitation in patients with repaired Tetralogy of Fallot. Pediatr Cardiol. 2017;38(2):240–6.PubMedCrossRef
28.
Mukaka MM. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 2012;24(3):69–71.PubMedPubMedCentral
29.
Waldmann V, Bouzeman A, Duthoit G, Koutbi L, Bessiere F, Labombarda F, et al. Long-term follow-up of patients with Tetralogy of Fallot and implantable cardioverter defibrillator: The DAI-T4F nationwide registry. Circulation. 2020;142(17):1612–22.PubMedCrossRef
30.
Balasubramanian S, Harrild DM, Kerur B, Marcus E, del Nido P, Geva T, et al. Impact of surgical pulmonary valve replacement on ventricular strain and synchrony in patients with repaired tetralogy of Fallot: a cardiovascular magnetic resonance feature tracking study. J Cardiovasc Magn Reson. 2018;20(1):37.PubMedPubMedCentralCrossRef
31.
O’Byrne ML, Glatz AC, Mercer-Rosa L, Gillespie MJ, Dori Y, Goldmuntz E, et al. Trends in pulmonary valve replacement in children and adults with tetralogy of fallot. Am J Cardiol. 2015;115(1):118–24.PubMedCrossRef
32.
Preoperative Predictors of Death and Sustained Ventricular Tachycardia After Pulmonary Valve Replacement in Patients With Repaired Tetralogy of Fallot Enrolled in the INDICATOR Cohort. 10.
33.
Ferraz Cavalcanti PE, Sá MPBO, Santos CA, Esmeraldo IM, de Escobar RR, de Menezes AM, et al. Pulmonary valve replacement after operative repair of Tetralogy of Fallot. J Am Coll Cardiol. 2013;62(23):2227–43.PubMedCrossRef
34.
Ghonim S, Ernst S, Keegan J, Giannakidis A, Spadotto V, Voges I, et al. Three-dimensional late gadolinium enhancement cardiovascular magnetic resonance predicts inducibility of ventricular tachycardia in adults with repaired Tetralogy of Fallot. Circ Arrhythm Electrophysiol. 2020;13:11. https://​doi.​org/​10.​1161/​CIRCEP.​119.​008321.CrossRef
35.
Pasipoularides A, Shu M, Shah A, Womack MS, Glower DD. Diastolic right ventricular filling vortex in normal and volume overload states. Am J Physiol Heart Circ Physiol. 2003;284(4):H1064–72.PubMedCrossRef
36.
Pasipoularides A. Evaluation of right and left ventricular diastolic filling. J of Cardiovasc Trans Res. 2013;6(4):623–39.CrossRef
37.
Mangual JO, Domenichini F, Pedrizzetti G. Describing the highly three dimensional right ventricle flow. Ann Biomed Eng. 2012;40(8):1790–801.PubMedCrossRef
38.
Fredriksson AG, Zajac J, Eriksson J, Dyverfeldt P, Bolger AF, Ebbers T, et al. 4-D blood flow in the human right ventricle. Am J Physiol Heart Circ Physiol. 2011;301(6):H2344–50.PubMedCrossRef
39.
Mangual JO, Domenichini F, Pedrizzetti G. Three dimensional numerical assessment of the right ventricular flow using 4D echocardiography boundary data. Eur J Mech B Fluids. 2012;35:25–30.CrossRef
40.
Stugaard M, Koriyama H, Katsuki K, Masuda K, Asanuma T, Takeda Y, et al. Energy loss in the left ventricle obtained by vector flow mapping as a new quantitative measure of severity of aortic regurgitation: a combined experimental and clinical study. Eur Heart J Cardiovasc Imag. 2015;16(7):723–30.CrossRef
41.
Pedrizzetti G, Sengupta PP. Vortex imaging: new information gain from tracking cardiac energy loss. European Heart Journal. 2015;16(7):719–20.
42.
Okafor I, Raghav V, Condado JF, Midha PA, Kumar G, Yoganathan AP. Aortic regurgitation generates a kinematic obstruction which hinders left ventricular filling. Ann Biomed Eng. 2017;45(5):1305–14.PubMedCrossRef
43.
Ye XT, Buratto E, Konstantinov IE, d’Udekem Y. Does transatrial-transpulmonary approach improve outcomes compared with transventricular approach in non-neonatal patients undergoing tetralogy of Fallot repair? Interact Cardiovasc Thorac Surg. 2019;29(6):960–6.PubMedCrossRef
44.
Zdradzinski MJ, Qureshi AM, Stewart R, Pettersson G, Krasuski RA. Comparison of long-term postoperative sequelae in patients with tetralogy of Fallot versus isolated pulmonic stenosis. Am J Cardiol. 2014;114(2):300–4.PubMedPubMedCentralCrossRef
45.
Sjöberg P, Töger J, Hedström E, Arvidsson P, Heiberg E, Arheden H, et al. Altered biventricular hemodynamic forces in patients with repaired tetralogy of Fallot and right ventricular volume overload because of pulmonary regurgitation. Am J Physiol Heart Circ Physiol. 2018;315(6):H1691–702.PubMedCrossRef
46.
Pasipoularides A. Mechanotransduction mechanisms for intraventricular diastolic vortex forces and myocardial deformations: part 1. J of Cardiovasc Trans Res. 2015;8(1):76–87.CrossRef
47.
Pasipoularides A. Mechanotransduction Mechanisms for Intraventricular Diastolic Vortex Forces and Myocardial Deformations: Part 2. J Cardiovasc Trans Res. 2015;8(5):293–318.CrossRef
48.
49.
Jeong D, Anagnostopoulos PV, Roldan-Alzate A, Srinivasan S, Schiebler ML, Wieben O, et al. Ventricular kinetic energy may provide a novel noninvasive way to assess ventricular performance in patients with repaired tetralogy of Fallot. J Thorac Cardiovasc Surg. 2015;149(5):1339–47.PubMedCrossRef
50.
Fogel MA, Sundareswaran KS, de Zelicourt D, Dasi LP, Pawlowski T, Rome J, et al. Power loss and right ventricular efficiency in patients after Tetralogy of Fallot repair with pulmonary insufficiency: clinical implications. J Thorac Cardiovasc Surg. 2012;143(6):1279–85.PubMedCrossRef
51.
Meadows J, Powell AJ, Geva T, Dorfman A, Gauvreau K, Rhodes J. Cardiac magnetic resonance imaging correlates of exercise capacity in patients with surgically repaired Tetralogy of Fallot. Am J Cardiol. 2007;100(9):1446–50.PubMedCrossRef
52.
Macdonald JA, Beshish AG, Corrado PA, Barton GP, Goss KN, Eldridge MW, et al. Feasibility of cardiovascular four-dimensional flow MRI during exercise in healthy participants. Radiol Cardiothorac Imaging. 2020;2(3):e190033.PubMedPubMedCentralCrossRef
53.
Berganza FM, de Alba CG, Özcelik N, Adebo D. Cardiac magnetic resonance feature tracking biventricular two-dimensional and three-dimensional strains to evaluate ventricular function in children after repaired Tetralogy of Fallot as compared with healthy children. Pediatr Cardiol. 2017;38(3):566–74.PubMedCrossRef
54.
Leonardi B, Taylor AM, Mansi T, Voigt I, Sermesant M, Pennec X, et al. Computational modelling of the right ventricle in repaired tetralogy of Fallot: can it provide insight into patient treatment? Eur Heart J. 2013;14(4):381–6.
55.
Tang D, del Nido PJ, Yang C, Zuo H, Huang X, Rathod RH, et al. Patient-specific MRI-based right ventricle models using different zero-load diastole and systole geometries for better cardiac stress and strain calculations and pulmonary valve replacement surgical outcome predictions. PLoS ONE. 2016;11(9):e0162986.PubMedPubMedCentralCrossRef
56.
Bhat M, Mercer-Rosa L, Fogel MA, Harris MA, Paridon SM, McBride MG, et al. Longitudinal changes in adolescents with TOF: implications for care. Eur Heart J Cardiovasc Imaging. 2017;18(3):356–63.PubMedCrossRef
57.
Kipps AK, Graham DA, Harrild DM, Lewis E, Powell AJ, Rhodes J. Longitudinal exercise capacity of patients with repaired tetralogy of fallot. Am J Cardiol. 2011;108(1):99–105.PubMedPubMedCentralCrossRef
58.
Sacco F, Paun B, Lehmkuhl O, Iles TL, Iaizzo PA, Houzeaux G, et al. Evaluating the roles of detailed endocardial structures on right ventricular haemodynamics by means of CFD simulations. Int J Numer Method Biomed Eng. 2018;34(9):e3115.PubMedCrossRef
59.
Nyrnes SA, Fadnes S, Wigen MS, Mertens L, Lovstakken L. Blood speckle-tracking based on high-frame rate ultrasound imaging in pediatric cardiology. J Am Soc Echocardiogr. 2020;33(4):493-503.e5.PubMedCrossRef
Metadata
Title
Moving beyond size: vorticity and energy loss are correlated with right ventricular dysfunction and exercise intolerance in repaired Tetralogy of Fallot
Authors
Yue-Hin Loke
Francesco Capuano
Vincent Cleveland
Jason G. Mandell
Elias Balaras
Laura J. Olivieri
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2021
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-021-00789-2

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