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Published in: European Radiology 10/2018

Open Access 01-10-2018 | Cardiac

Disturbed left and right ventricular kinetic energy in patients with repaired tetralogy of Fallot: pathophysiological insights using 4D-flow MRI

Authors: Pia Sjöberg, Sebastian Bidhult, Jelena Bock, Einar Heiberg, Håkan Arheden, Ronny Gustafsson, Shahab Nozohoor, Marcus Carlsson

Published in: European Radiology | Issue 10/2018

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Abstract

Objectives

Indications for pulmonary valve replacement (PVR) in patients with pulmonary regurgitation (PR) after repaired tetralogy of Fallot (rToF) are debated. We aimed to compare right (RV) and left ventricular (LV) kinetic energy (KE) measured by 4D-flow magnetic resonance imaging (MRI) in patients to controls, to further understand the pathophysiological effects of PR.

Methods

Fifteen patients with rToF with PR > 20% and 14 controls underwent MRI. Ventricular volumes and KE were quantified from cine MRI and 4D-flow, respectively. Lagrangian coherent structures were used to discriminate KE in the PR. Restrictive RV physiology was defined as end-diastolic forward flow.

Results

LV systolic peak KE was lower in rToF, 2.8 ± 1.1 mJ, compared to healthy volunteers, 4.8 ± 1.1 mJ, p < 0.0001. RV diastolic peak KE was higher in rToF (7.7 ± 4.3 mJ vs 3.1 ± 1.3 mJ, p = 0.0001) and the difference most pronounced in patients with non-restrictive RV physiology. KE was primarily located in the PR volume at the time of diastolic peak KE, 64 ± 17%.

Conclusion

This is the first study showing disturbed KE in patients with rToF and PR, in both the RV and LV. The role of KE as a potential early marker of ventricular dysfunction to guide intervention needs to be addressed in future studies.

Key Points

• Kinetic energy (KE) reflects ventricular performance
• KE is a potential marker of ventricular dysfunction in Fallot patients
• KE is disturbed in both ventricles in patients with tetralogy of Fallot
• KE contributes to the understanding of the pathophysiology of pulmonary regurgitation
• Lagrangian coherent structures enable differentiation of ventricular inflows
Appendix
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Literature
1.
go back to reference Stephensen S, Steding-Ehrenborg K, Munkhammar P et al (2014) The relationship between longitudinal, lateral, and septal contribution to stroke volume in patients with pulmonary regurgitation and healthy volunteers. Am J Physiol Heart Circ Physiol 306:H895–H903CrossRef Stephensen S, Steding-Ehrenborg K, Munkhammar P et al (2014) The relationship between longitudinal, lateral, and septal contribution to stroke volume in patients with pulmonary regurgitation and healthy volunteers. Am J Physiol Heart Circ Physiol 306:H895–H903CrossRef
2.
go back to reference Kempny A, Dimopoulos K, Uebing A et al (2012) Reference values for exercise limitations among adults with congenital heart disease. Relation to activities of daily life–single centre experience and review of published data. Eur Heart J 33:1386–1396CrossRef Kempny A, Dimopoulos K, Uebing A et al (2012) Reference values for exercise limitations among adults with congenital heart disease. Relation to activities of daily life–single centre experience and review of published data. Eur Heart J 33:1386–1396CrossRef
3.
go back to reference Harrison DA, Harris L, Siu SC et al (1997) Sustained ventricular tachycardia in adult patients late after repair of tetralogy of Fallot. J Am Coll Cardiol 30:1368–1373CrossRef Harrison DA, Harris L, Siu SC et al (1997) Sustained ventricular tachycardia in adult patients late after repair of tetralogy of Fallot. J Am Coll Cardiol 30:1368–1373CrossRef
4.
go back to reference Bokma JP, Winter MM, Oosterhof T et al (2015) Preoperative thresholds for mid-to-late haemodynamic and clinical outcomes after pulmonary valve replacement in tetralogy of Fallot. Eur Heart J 37:1–7 Bokma JP, Winter MM, Oosterhof T et al (2015) Preoperative thresholds for mid-to-late haemodynamic and clinical outcomes after pulmonary valve replacement in tetralogy of Fallot. Eur Heart J 37:1–7
5.
go back to reference Alvarez-Fuente M, Garrido-Lestache E, Fernandez-Pineda L et al (2016) Timing of pulmonary valve replacement: how much can the right ventricle dilate before it looses its remodeling potential? Pediatr Cardiol 37:601–605CrossRef Alvarez-Fuente M, Garrido-Lestache E, Fernandez-Pineda L et al (2016) Timing of pulmonary valve replacement: how much can the right ventricle dilate before it looses its remodeling potential? Pediatr Cardiol 37:601–605CrossRef
6.
go back to reference Shin YR, Jung JW, Kim NK et al (2016) Factors associated with progression of right ventricular enlargement and dysfunction after repair of tetralogy of Fallot based on serial cardiac magnetic resonance imaging. Eur J Cardiothorac Surg 50:464–469CrossRef Shin YR, Jung JW, Kim NK et al (2016) Factors associated with progression of right ventricular enlargement and dysfunction after repair of tetralogy of Fallot based on serial cardiac magnetic resonance imaging. Eur J Cardiothorac Surg 50:464–469CrossRef
7.
go back to reference Greutmann M (2016) Tetralogy of Fallot, pulmonary valve replacement, and right ventricular volumes: are we chasing the right target? Eur Heart J 37:836–839CrossRef Greutmann M (2016) Tetralogy of Fallot, pulmonary valve replacement, and right ventricular volumes: are we chasing the right target? Eur Heart J 37:836–839CrossRef
8.
go back to reference Bokma JP, de Wilde KC, Vliegen HW et al (2017) Value of cardiovascular magnetic resonance imaging in noninvasive risk stratification in tetralogy of Fallot. JAMA Cardiol 119:1370–1377 Bokma JP, de Wilde KC, Vliegen HW et al (2017) Value of cardiovascular magnetic resonance imaging in noninvasive risk stratification in tetralogy of Fallot. JAMA Cardiol 119:1370–1377
9.
go back to reference Lee N, Taylor MD, Banerjee RK (2015) Right ventricle-pulmonary circulation dysfunction: a review of energy-based approach. Biomed Eng Online 14:S8CrossRef Lee N, Taylor MD, Banerjee RK (2015) Right ventricle-pulmonary circulation dysfunction: a review of energy-based approach. Biomed Eng Online 14:S8CrossRef
10.
go back to reference Hirtler D, Garcia J, Barker AJ, Geiger J (2016) 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 26:3598–3607CrossRef Hirtler D, Garcia J, Barker AJ, Geiger J (2016) 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 26:3598–3607CrossRef
11.
go back to reference Arvidsson PM, Töger J, Heiberg E et al (2013) Quantification of left and right atrial kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. J Appl Physiol 114:1472–1481CrossRef Arvidsson PM, Töger J, Heiberg E et al (2013) Quantification of left and right atrial kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. J Appl Physiol 114:1472–1481CrossRef
12.
go back to reference Eriksson J, Bolger AF, Ebbers T, Carlhäll C-JJ (2013) Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy. Eur Heart J Cardiovasc Imaging 14:417–424CrossRef Eriksson J, Bolger AF, Ebbers T, Carlhäll C-JJ (2013) Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy. Eur Heart J Cardiovasc Imaging 14:417–424CrossRef
13.
go back to reference Al-Wakeel N, Fernandes JF, Amiri A et al (2015) Hemodynamic and energetic aspects of the left ventricle in patients with mitral regurgitation before and after mitral valve surgery. J Magn Reson Imaging 42:1705–1712CrossRef Al-Wakeel N, Fernandes JF, Amiri A et al (2015) Hemodynamic and energetic aspects of the left ventricle in patients with mitral regurgitation before and after mitral valve surgery. J Magn Reson Imaging 42:1705–1712CrossRef
14.
go back to reference Kanski M, Arvidsson PM, Töger J et al (2015) Left ventricular fluid kinetic energy time curves in heart failure from cardiovascular magnetic resonance 4D flow data. J Cardiovasc Magn Reson 17:111CrossRef Kanski M, Arvidsson PM, Töger J et al (2015) Left ventricular fluid kinetic energy time curves in heart failure from cardiovascular magnetic resonance 4D flow data. J Cardiovasc Magn Reson 17:111CrossRef
15.
go back to reference Sjöberg P, Heiberg E, Wingren P et al (2017) Decreased diastolic ventricular kinetic energy in young patients with Fontan circulation demonstrated by four-dimensional cardiac magnetic resonance imaging. Pediatr Cardiol 38:669–680CrossRef Sjöberg P, Heiberg E, Wingren P et al (2017) Decreased diastolic ventricular kinetic energy in young patients with Fontan circulation demonstrated by four-dimensional cardiac magnetic resonance imaging. Pediatr Cardiol 38:669–680CrossRef
16.
go back to reference Jeong D, Anagnostopoulos PV, Roldan-Alzate A et al (2014) Ventricular kinetic energy may provide a novel noninvasive way to assess ventricular performance in patients with repaired tetralogy of Fallot. J Thorac Cardiovasc Surg 149:1339–1347CrossRef Jeong D, Anagnostopoulos PV, Roldan-Alzate A et al (2014) Ventricular kinetic energy may provide a novel noninvasive way to assess ventricular performance in patients with repaired tetralogy of Fallot. J Thorac Cardiovasc Surg 149:1339–1347CrossRef
17.
go back to reference Töger J, Kanski M, Carlsson M et al (2012) Vortex ring formation in the left ventricle of the heart: analysis by 4D flow MRI and Lagrangian coherent structures. Ann Biomed Eng 40:1–11CrossRef Töger J, Kanski M, Carlsson M et al (2012) Vortex ring formation in the left ventricle of the heart: analysis by 4D flow MRI and Lagrangian coherent structures. Ann Biomed Eng 40:1–11CrossRef
19.
go back to reference Gläser S, Koch B, Ittermann T et al (2010) Influence of age, sex, body size, smoking, and β blockade on key gas exchange exercise parameters in an adult population. Eur J Cardiovasc Prev Rehabil 17:469–476CrossRef Gläser S, Koch B, Ittermann T et al (2010) Influence of age, sex, body size, smoking, and β blockade on key gas exchange exercise parameters in an adult population. Eur J Cardiovasc Prev Rehabil 17:469–476CrossRef
20.
go back to reference Munkhammar P, Carlsson M, Arheden H, Pesonen E (2013) Restrictive right ventricular physiology after tetralogy of Fallot repair is associated with fibrosis of the right ventricular outflow tract visualized on cardiac magnetic resonance imaging. Eur Heart J Cardiovasc Imaging 14:978–985CrossRef Munkhammar P, Carlsson M, Arheden H, Pesonen E (2013) Restrictive right ventricular physiology after tetralogy of Fallot repair is associated with fibrosis of the right ventricular outflow tract visualized on cardiac magnetic resonance imaging. Eur Heart J Cardiovasc Imaging 14:978–985CrossRef
21.
go back to reference Lee W, Yoo S-J, Roche SL et al (2013) Determinants and functional impact of restrictive physiology after repair of tetralogy of Fallot: new insights from magnetic resonance imaging. Int J Cardiol 167:1347–1353CrossRef Lee W, Yoo S-J, Roche SL et al (2013) Determinants and functional impact of restrictive physiology after repair of tetralogy of Fallot: new insights from magnetic resonance imaging. Int J Cardiol 167:1347–1353CrossRef
22.
go back to reference Kanski M, Töger J, Steding-Ehrenborg K et al (2015) Whole-heart four-dimensional flow can be acquired with preserved quality without respiratory gating, facilitating clinical use: a head-to-head comparison. BMC Med Imaging 15:20CrossRef Kanski M, Töger J, Steding-Ehrenborg K et al (2015) Whole-heart four-dimensional flow can be acquired with preserved quality without respiratory gating, facilitating clinical use: a head-to-head comparison. BMC Med Imaging 15:20CrossRef
23.
go back to reference Carlsson M, Bock J, Bidhult S et al (2017) Multi-vendor whole-heart 4D flow validation study with and without respiratory gating. In: 20th Annu SCMR Sci Sess. Abstr Suppl p P327 Carlsson M, Bock J, Bidhult S et al (2017) Multi-vendor whole-heart 4D flow validation study with and without respiratory gating. In: 20th Annu SCMR Sci Sess. Abstr Suppl p P327
24.
go back to reference Heiberg E, Sjögren J, Ugander M et al (2010) Design and validation of Segment—freely available software for cardiovascular image analysis. BMC Med Imaging 10:1CrossRef Heiberg E, Sjögren J, Ugander M et al (2010) Design and validation of Segment—freely available software for cardiovascular image analysis. BMC Med Imaging 10:1CrossRef
25.
go back to reference Busch J, Giese D, Kozerke S (2017) Image-based background phase error correction in 4D flow MRI revisited. J Magn Reson Imaging 1–10 Busch J, Giese D, Kozerke S (2017) Image-based background phase error correction in 4D flow MRI revisited. J Magn Reson Imaging 1–10
26.
go back to reference Ordovas KG, Carlsson M, Lease KE et al (2012) Impaired regional left ventricular strain after repair of tetralogy of Fallot. J Magn Reson Imaging 35:79–85CrossRef Ordovas KG, Carlsson M, Lease KE et al (2012) Impaired regional left ventricular strain after repair of tetralogy of Fallot. J Magn Reson Imaging 35:79–85CrossRef
27.
go back to reference Chang M-C, Wu M-T, Weng K-P et al (2018) Left ventricular regional myocardial motion and twist function in repaired tetralogy of Fallot evaluated by magnetic resonance tissue phase mapping. Eur Radiol 28:104–114CrossRef Chang M-C, Wu M-T, Weng K-P et al (2018) Left ventricular regional myocardial motion and twist function in repaired tetralogy of Fallot evaluated by magnetic resonance tissue phase mapping. Eur Radiol 28:104–114CrossRef
28.
go back to reference Diller G-PP, Kempny A, Liodakis E et al (2012) Left ventricular longitudinal function predicts life-threatening ventricular arrhythmia and death in adults with repaired tetralogy of Fallot. Circulation 125:2440–2446CrossRef Diller G-PP, Kempny A, Liodakis E et al (2012) Left ventricular longitudinal function predicts life-threatening ventricular arrhythmia and death in adults with repaired tetralogy of Fallot. Circulation 125:2440–2446CrossRef
29.
go back to reference Kopic S, Stephensen SS, Heiberg E et al (2017) Isolated pulmonary regurgitation causes decreased right ventricular longitudinal function and compensatory increased septal pumping in a porcine model. Acta Physiol 221:163–173CrossRef Kopic S, Stephensen SS, Heiberg E et al (2017) Isolated pulmonary regurgitation causes decreased right ventricular longitudinal function and compensatory increased septal pumping in a porcine model. Acta Physiol 221:163–173CrossRef
30.
go back to reference Rao PS, Awa S, Linde LM et al (1973) Role of kinetic energy in pulmonary valvar pressure gradients. Circulation 48:65–73CrossRef Rao PS, Awa S, Linde LM et al (1973) Role of kinetic energy in pulmonary valvar pressure gradients. Circulation 48:65–73CrossRef
31.
go back to reference Carlsson M, Heiberg E, Toger J, Arheden H (2012) Quantification of left and right ventricular kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. Am J Physiol Heart Circ Physiol 302:H893–H900CrossRef Carlsson M, Heiberg E, Toger J, Arheden H (2012) Quantification of left and right ventricular kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. Am J Physiol Heart Circ Physiol 302:H893–H900CrossRef
32.
go back to reference Prec O, Katz N, Sennet L et al (1949) Determination of kinetic energy of the heart in man. Am J Physiol 159:483–491PubMed Prec O, Katz N, Sennet L et al (1949) Determination of kinetic energy of the heart in man. Am J Physiol 159:483–491PubMed
33.
go back to reference Barber NJ, Ako EO, Kowalik GT et al (2016) Magnetic resonance-augmented cardiopulmonary exercise testing. Circ Cardiovasc Imaging 9:e005282CrossRef Barber NJ, Ako EO, Kowalik GT et al (2016) Magnetic resonance-augmented cardiopulmonary exercise testing. Circ Cardiovasc Imaging 9:e005282CrossRef
Metadata
Title
Disturbed left and right ventricular kinetic energy in patients with repaired tetralogy of Fallot: pathophysiological insights using 4D-flow MRI
Authors
Pia Sjöberg
Sebastian Bidhult
Jelena Bock
Einar Heiberg
Håkan Arheden
Ronny Gustafsson
Shahab Nozohoor
Marcus Carlsson
Publication date
01-10-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5385-3

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