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4D flow MRI applications in congenital heart disease

  • Cardiac
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Abstract

Advances in the diagnosis and management of congenital heart disease (CHD) have resulted in a growing population of patients surviving well into adulthood and requiring lifelong follow-up. Flow quantification is a central component in the assessment of patients with CHD. 4D flow magnetic resonance imaging (MRI) has emerged as a tool that enables comprehensive study of flow. It involves the acquisition of a three-dimensional time-resolved volume with velocity encoding in all three spatial directions along the cardiac cycle. This allows flow quantification and visualization of blood flow patterns as well as the study of advanced hemodynamic parameters as kinetic energy and wall shear stress. 4D flow MRI-based study of flow has given insight into the altered hemodynamics in CHD particularly in bicuspid aortic valve disease and Fontan circulation. The aim of this review is to discuss the expanding clinical and research applications of 4D flow MRI in CHD as well its limitations.

Key Points

• Three-dimensional velocity encoding allows not only flow quantification but also the visualization of multidirectional flow patterns and the study of advanced hemodynamic parameters.

• 4D flow MRI has added insight into the abnormal hemodynamics involved in congenital heart disease in particular in bicuspid aortic valve and Fontan circulation.

• The main limitation of 4D flow MRI in congenital heart disease is the relatively long scan duration required for the complete coverage of the heart and great vessels with adequate spatiotemporal resolution.

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Abbreviations

2D:

Two-dimensional

4D:

Four-dimensional

AVSD:

Atrioventricular septal defect

BAV:

Bicuspid aortic valve

BLAST:

Broad linear speed-up technique

CHD:

Congenital heart disease

ECG:

Electrocardiography

EL:

Energy loss

GRAPPA:

Generalized Autocalibrating Partially Parallel Acquisition

IVC:

Inferior vena cava

KE:

Kinetic energy

LAVV:

Left atrioventricular valve

LV:

Left ventricle

MRI:

Magnetic resonance imaging

PC:

Phase contrast

PR:

Pulmonary regurgitation

RL-BAV:

Right–left cusp fusion bicuspid aortic valve

RN-BAV:

Right-noncoronary cusp fusion bicuspid aortic valve

RV:

Right ventricle

SENSE:

Sensitivity encoding

TCPC:

Total cavopulmonary connection

TOF:

Tetralogy of Fallot

VENC:

Velocity encoding

VIPR:

Vastly undersampled isotropic projection reconstruction

WSS:

Wall shear stress

References

  1. van der Linde D, Konings EE, Slager MA et al (2011) Birth prevalence of congenital heart disease worldwide: a systematic review and meta-analysis. J Am Coll Cardiol 58:2241–2247

    PubMed  Google Scholar 

  2. Hoffman JI, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39:1890–1900

    PubMed  Google Scholar 

  3. Marelli AJ, Mackie AS, Ionescu-Ittu R, Rahme E, Pilote L (2007) Congenital heart disease in the general population. Circulation 115:163

    PubMed  Google Scholar 

  4. Bhatt AB, Foster E, Kuehl K et al (2015) Congenital heart disease in the older adult: a scientific statement from the American Heart Association. Circulation 131:1884–1931

    PubMed  Google Scholar 

  5. Stout KK, Daniels CJ, Aboulhosn JA et al (2019) 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. J Am Coll Cardiol 73:1494–1563

  6. Di Salvo G, Miller O, Babu Narayan S et al (2018) Imaging the adult with congenital heart disease: a multimodality imaging approach—position paper from the EACVI. Eur Heart J Cardiovasc Imaging 19:1077–1098

    PubMed  Google Scholar 

  7. Quiñones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA (2002) Recommendations for quantification of Doppler echocardiography: a report from the Doppler quantification task force of the nomenclature and standards committee of the American Society of Echocardiography. J Am Soc Echocardiogr 15:167–184

    PubMed  Google Scholar 

  8. Babu-Narayan SV, Giannakoulas G, Valente AM, Li W, Gatzoulis MA (2016) Imaging of congenital heart disease in adults. Eur Heart J 37:1182–1195

    PubMed  Google Scholar 

  9. Fratz S, Chung T, Greil GF et al (2013) Guidelines and protocols for cardiovascular magnetic resonance in children and adults with congenital heart disease: SCMR expert consensus group on congenital heart disease. J Cardiovasc Magn Reson 15:51

    PubMed  PubMed Central  Google Scholar 

  10. Burchill LJ, Huang J, Tretter JT et al (2017) Noninvasive imaging in adult congenital heart disease. Circ Res 120:995–1014

    CAS  PubMed  Google Scholar 

  11. Kilner PJ, Geva T, Kaemmerer H, Trindade PT, Schwitter J, Webb GD (2010) Recommendations for cardiovascular magnetic resonance in adults with congenital heart disease from the respective working groups of the European Society of Cardiology. Eur Heart J 31:794–805

    PubMed  PubMed Central  Google Scholar 

  12. Selzer A, Sudrann RB (1958) Reliability of the determination of cardiac output in man by means of the Fick principle. Circ Res 6:485–490

    CAS  PubMed  Google Scholar 

  13. Ganz W, Donoso R, Marcus HS, Forrester JS, Swan HJ (1971) A new technique for measurement of cardiac output by thermodilution in man. Am J Cardiol 27:392–396

    CAS  PubMed  Google Scholar 

  14. Markl M, Kilner PJ, Ebbers T (2011) Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 13:7

    PubMed  PubMed Central  Google Scholar 

  15. Dyverfeldt P, Bissell M, Barker AJ et al (2015) 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson 17:72

    PubMed  PubMed Central  Google Scholar 

  16. Kamphuis VP, Westenberg JJ, van der Palen RL et al (2017) Unravelling cardiovascular disease using four dimensional flow cardiovascular magnetic resonance. Int J Cardiovasc Imaging 33:1069–1081

    PubMed  Google Scholar 

  17. Markl M, Wallis W, Harloff A (2011) Reproducibility of flow and wall shear stress analysis using flow-sensitive four-dimensional MRI. J Magn Reson Imaging 33:988–994

    PubMed  Google Scholar 

  18. Richter Y, Edelman ER (2006) Cardiology is flow. Circulation 113:2679–2682

    PubMed  Google Scholar 

  19. Hanneman K, Sivagnanam M, Nguyen ET et al (2014) Magnetic resonance assessment of pulmonary (QP) to systemic (QS) flows using 4D phase-contrast imaging: pilot study comparison with standard through-plane 2D phase-contrast imaging. Acad Radiol 21:1002–1008

    PubMed  Google Scholar 

  20. Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M (2008) Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med 60:1218–1231

    CAS  PubMed  Google Scholar 

  21. Nordmeyer S, Riesenkampff E, Messroghli D et al (2012) Four-dimensional velocity-encoded magnetic resonance imaging improves blood flow quantification in patients with complex accelerated flow. J Magn Reson Imaging 37:208–216

    PubMed  Google Scholar 

  22. Gabbour M, Schnell S, Jarvis K, Robinson JD, Markl M, Rigsby CK (2015) 4-D flow magnetic resonance imaging: blood flow quantification compared to 2-D phase-contrast magnetic resonance imaging and Doppler echocardiography. Pediatr Radiol 45:804–813

    PubMed  Google Scholar 

  23. Nordmeyer S, Riesenkampff E, Crelier G et al (2010) Flow-sensitive four-dimensional cine magnetic resonance imaging for offline blood flow quantification in multiple vessels: a validation study. J Magn Reson Imaging 32:677–683

    PubMed  Google Scholar 

  24. Valverde I, Nordmeyer S, Uribe S et al (2012) Systemic-to-pulmonary collateral flow in patients with palliated univentricular heart physiology: measurement using cardiovascular magnetic resonance 4D velocity acquisition. J Cardiovasc Magn Reson 14:25

    PubMed  PubMed Central  Google Scholar 

  25. Hsiao A, Alley MT, Massaband P, Herfkens RJ, Chan FP, Vasanawala SS (2011) Improved cardiovascular flow quantification with time-resolved volumetric phase-contrast MRI. Pediatr Radiol 41:711–720

    PubMed  Google Scholar 

  26. Hsiao A, Tariq U, Alley MT, Lustig M, Vasanawala SS (2015) Inlet and outlet valve flow and regurgitant volume may be directly and reliably quantified with accelerated, volumetric phase-contrast MRI. J Magn Reson Imaging 41:376–385

    PubMed  Google Scholar 

  27. van der Hulst AE, Westenberg JJ, Kroft LJ et al (2010) Tetralogy of fallot: 3D velocity-encoded MR imaging for evaluation of right ventricular valve flow and diastolic function in patients after correction. Radiology 256:724–734

    PubMed  Google Scholar 

  28. Jarvis K, Vonder M, Barker AJ et al (2016) Hemodynamic evaluation in patients with transposition of the great arteries after the arterial switch operation: 4D flow and 2D phase contrast cardiovascular magnetic resonance compared with Doppler echocardiography. J Cardiovasc Magn Reson 18:59

    PubMed  PubMed Central  Google Scholar 

  29. Uribe S, Beerbaum P, Sørensen Thomas S, Rasmusson A, Razavi R, Schaeffter T (2009) Four-dimensional (4D) flow of the whole heart and great vessels using real-time respiratory self-gating. Magn Reson Med 62:984–992

    PubMed  Google Scholar 

  30. van Wijk WHS, Breur JMPJ, Westenberg JJM et al (2019) Validation of aortic valve 4D flow analysis and myocardial deformation by cardiovascular magnetic resonance in patients after the arterial switch operation. J Cardiovasc Magn Reson 21:20

    PubMed  PubMed Central  Google Scholar 

  31. She HL, Roest AAW, Calkoen EE et al (2017) Comparative evaluation of flow quantification across the atrioventricular valve in patients with functional univentricular heart after Fontan’s surgery and healthy controls: measurement by 4D flow magnetic resonance imaging and streamline visualization. Congenit Heart Dis 12:40–48

    PubMed  Google Scholar 

  32. Hsiao A, Yousaf U, Alley MT et al (2015) Improved quantification and mapping of anomalous pulmonary venous flow with four-dimensional phase-contrast MRI and interactive streamline rendering. J Magn Reson Imaging 42:1765–1776

    PubMed  PubMed Central  Google Scholar 

  33. Rose MJ, Jarvis K, Chowdhary V et al (2016) Efficient method for volumetric assessment of peak blood flow velocity using 4D flow MRI. J Magn Reson Imaging 44:1673–1682

    PubMed  PubMed Central  Google Scholar 

  34. van Ooij P, Powell AL, Potters WV, Carr JC, Markl M, Barker AJ (2016) Reproducibility and interobserver variability of systolic blood flow velocity and 3D wall shear stress derived From 4D flow MRI in the healthy aorta. J Magn Reson Imaging 43:236–248

    PubMed  Google Scholar 

  35. Kamphuis VP, van der Palen RLF, de Koning PJH et al (2018) In-scan and scan–rescan assessment of LV in- and outflow volumes by 4D flow MRI versus 2D planimetry. J Magn Reson Imaging 47:511–522

    PubMed  Google Scholar 

  36. Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O (2012) 4D flow MRI. J Magn Reson Imaging 36:1015–1036

    PubMed  Google Scholar 

  37. Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB (1993) Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 88:2235–2247

    CAS  PubMed  Google Scholar 

  38. Kilner PJ, Yang G-Z, Wilkes AJ, Mohiaddin RH, Firmin DN, Yacoub MH (2000) Asymmetric redirection of flow through the heart. Nature 404:759–761

    CAS  PubMed  Google Scholar 

  39. Zhong L, Schrauben EM, Garcia J et al (2019) Intracardiac 4D flow MRI in congenital heart disease: recommendations on behalf of the ISMRM Flow & Motion Study Group. J Magn Reson Imaging 50:677–681

    PubMed  Google Scholar 

  40. Thunberg P, Karlsson M, Wigström L (2003) Accuracy and reproducibility in phase contrast imaging using SENSE. Magn Reson Med 50:1061–1068

    PubMed  Google Scholar 

  41. Griswold MA, Jakob PM, Heidemann RM et al (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210

    PubMed  Google Scholar 

  42. Tariq U, Hsiao A, Alley M, Zhang T, Lustig M, Vasanawala SS (2013) Venous and arterial flow quantification are equally accurate and precise with parallel imaging compressed sensing 4D phase contrast MRI. J Magn Reson Imaging 37:1419–1426

    PubMed  Google Scholar 

  43. Schnell S, Markl M, Entezari P et al (2014) k-t GRAPPA accelerated four-dimensional flow MRI in the aorta: effect on scan time, image quality, and quantification of flow and wall shear stress. Magn Reson Med 72:522–533

    PubMed  Google Scholar 

  44. Ebel S, Dufke J, Köhler B et al (2019) Comparison of two accelerated 4D-flow sequences for aortic flow quantification. Sci Rep 9:8643

    PubMed  PubMed Central  Google Scholar 

  45. Jung B, Ullmann P, Honal M, Bauer S, Hennig J, Markl M (2008) Parallel MRI with extended and averaged GRAPPA kernels (PEAK-GRAPPA): optimized spatiotemporal dynamic imaging. J Magn Reson Imaging 28:1226–1232

    PubMed  Google Scholar 

  46. Carlsson M, Töger J, Kanski M et al (2011) Quantification and visualization of cardiovascular 4D velocity mapping accelerated with parallel imaging or k-t BLAST: head to head comparison and validation at 1.5 T and 3 T. J Cardiovasc Magn Reson 13:55

    PubMed  PubMed Central  Google Scholar 

  47. Gu T, Korosec FR, Block WF et al (2005) PC VIPR: a high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. AJNR Am J Neuroradiol 26:743

    PubMed  PubMed Central  Google Scholar 

  48. Petersson S, Sigfridsson A, Dyverfeldt P, Carlhäll CJ, Ebbers T (2016) Retrospectively gated intracardiac 4 D flow MRI using spiral trajectories. Magn Reson Med 75:196–206

    PubMed  Google Scholar 

  49. Biglands JD, Radjenovic A, Ridgway JP (2012) Cardiovascular magnetic resonance physics for clinicians: part II. J Cardiovasc Magn Reson 14:66

    PubMed  PubMed Central  Google Scholar 

  50. Callaghan FM, Kozor R, Sherrah AG et al (2016) Use of multi-velocity encoding 4D flow MRI to improve quantification of flow patterns in the aorta. J Magn Reson Imaging 43:352–363

    PubMed  Google Scholar 

  51. Ma LE, Markl M, Chow K et al (2019) Aortic 4D flow MRI in 2 minutes using compressed sensing, respiratory controlled adaptive k-space reordering, and inline reconstruction. Magn Reson Med 81:3675–3890

    PubMed  PubMed Central  Google Scholar 

  52. Moersdorf R, Treutlein M, Kroeger JR et al (2019) Precision, reproducibility and applicability of an undersampled multi-venc 4D flow MRI sequence for the assessment of cardiac hemodynamics. Magn Reson Imaging 61:73–82

    PubMed  Google Scholar 

  53. Callahan S, Singam NS, Kendrick M et al (2020) Dual-Venc acquisition for 4D flow MRI in aortic stenosis with spiral readouts. J Magn Reson Imaging 52:117–128

    PubMed  Google Scholar 

  54. Bollache E, Barker AJ, Dolan RS et al (2018) k-t accelerated aortic 4D flow MRI in under two minutes: feasibility and impact of resolution, k-space sampling patterns, and respiratory navigator gating on hemodynamic measurements. Magn Reson Med 79:195–207

    PubMed  Google Scholar 

  55. Baltes C, Kozerke S, Atkinson D, Boesiger P (2004) Retrospective respiratory motion correction for navigated cine velocity mapping. J Cardiovasc Magn Reson 6:785–792

    PubMed  Google Scholar 

  56. Dyverfeldt P, Ebbers T (2017) Comparison of respiratory motion suppression techniques for 4D flow MRI. Magn Reson Med 78:1877–1882

    PubMed  PubMed Central  Google Scholar 

  57. Westenberg JJM, Roes SD, Ajmone Marsan N et al (2008) Mitral valve and tricuspid valve blood flow: accurate quantification with 3D velocity-encoded MR imaging with retrospective valve tracking. Radiology 249:792–800

    PubMed  Google Scholar 

  58. Kamphuis VP, Roest AAW, Marsan NA et al (2019) Automated cardiac valve tracking for flow quantification with four-dimensional flow MRI. Radiology 290:70–78

    PubMed  Google Scholar 

  59. Ward C (2000) Clinical significance of the bicuspid aortic valve. Heart 83:81

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Huntington K, Hunter AGW, Chan K-L (1997) A prospective study to assess the frequency of familial clustering of congenital bicuspid aortic valve. J Am Coll Cardiol 30:1809–1812

    CAS  PubMed  Google Scholar 

  61. Garg V, Muth AN, Ransom JF et al (2005) Mutations in NOTCH1 cause aortic valve disease. Nature 437:270–274

    CAS  PubMed  Google Scholar 

  62. Girdauskas E, Borger MA, Secknus M-A, Girdauskas G, Kuntze T (2011) Is aortopathy in bicuspid aortic valve disease a congenital defect or a result of abnormal hemodynamics? A critical reappraisal of a one-sided argument. Eur J Cardiothorac Surg 39:809–814

    PubMed  Google Scholar 

  63. Hope MD, Hope TA, Meadows AK et al (2010) Bicuspid aortic valve: four-dimensional MR evaluation of ascending aortic systolic flow patterns. Radiology 255:53–61

    PubMed  Google Scholar 

  64. Mahadevia R, Barker Alex J, Schnell S et al (2014) Bicuspid aortic cusp fusion morphology alters aortic three-dimensional outflow patterns, wall shear stress, and expression of aortopathy. Circulation 129:673–682

    CAS  PubMed  Google Scholar 

  65. Barker AJ, Markl M, Bürk J et al (2012) Bicuspid aortic valve is associated with altered wall shear stress in the ascending aorta. Circ Cardiovasc Imaging 5:457

    PubMed  Google Scholar 

  66. Bissell MM, Hess AT, Biasiolli L et al (2013) Aortic dilation in bicuspid aortic valve disease. Circ Cardiovasc Imaging 6:499

    PubMed  Google Scholar 

  67. Rodríguez-Palomares JF, Dux-Santoy L, Guala A et al (2018) Aortic flow patterns and wall shear stress maps by 4D-flow cardiovascular magnetic resonance in the assessment of aortic dilatation in bicuspid aortic valve disease. J Cardiovasc Magn Reson 20:28

    PubMed  PubMed Central  Google Scholar 

  68. Hope MD, Hope TA, Crook SES et al (2011) 4D Flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging 4:781–787

    PubMed  Google Scholar 

  69. Hope MD, Sigovan M, Wrenn SJ, Saloner D, Dyverfeldt P (2014) MRI hemodynamic markers of progressive bicuspid aortic valve-related aortic disease. J Magn Reson Imaging 40:140–145

    PubMed  Google Scholar 

  70. Garcia J, Barker AJ, Murphy I et al (2016) Four-dimensional flow magnetic resonance imaging-based characterization of aortic morphometry and haemodynamics: impact of age, aortic diameter, and valve morphology. Eur Heart J Cardiovasc Imaging 17:877–884

    PubMed  Google Scholar 

  71. Guzzardi DG, Barker AJ, van Ooij P et al (2015) Valve-related hemodynamics mediate human bicuspid aortopathy: insights from wall shear stress mapping. J Am Coll Cardiol 66:892–900

    PubMed  PubMed Central  Google Scholar 

  72. Bollache E, Guzzardi DG, Sattari S et al (2018) Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. J Thorac Cardiovasc Surg 156:2112–2120.e2112

    PubMed  PubMed Central  Google Scholar 

  73. Dux-Santoy L, Guala A, Teixidó-Turà G et al (2019) Increased rotational flow in the proximal aortic arch is associated with its dilation in bicuspid aortic valve disease. Eur Heart J Cardiovasc Imaging 20:1407–1417

    PubMed  Google Scholar 

  74. Raghav V, Barker AJ, Mangiameli D, Mirabella L, Markl M, Yoganathan AP (2018) Valve mediated hemodynamics and their association with distal ascending aortic diameter in bicuspid aortic valve subjects. J Magn Reson Imaging 47:246–254

    PubMed  Google Scholar 

  75. Bauer M, Gliech V, Siniawski H, Hetzer R (2006) Configuration of the ascending aorta in patients with bicuspid and tricuspid aortic valve disease undergoing aortic valve replacement with or without reduction aortoplasty. J Heart Valve Dis 15:594–600

    PubMed  Google Scholar 

  76. Lorenz R, Bock J, Barker AJ et al (2014) 4D flow magnetic resonance imaging in bicuspid aortic valve disease demonstrates altered distribution of aortic blood flow helicity. Magn Reson Med 71:1542–1553

    CAS  PubMed  Google Scholar 

  77. Garcia J, Barker AJ, Collins JD, Carr JC, Markl M (2017) Volumetric quantification of absolute local normalized helicity in patients with bicuspid aortic valve and aortic dilatation. Magn Reson Med 78:689–701

    PubMed  Google Scholar 

  78. Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V (2007) Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Dis 49:307–329

    PubMed  Google Scholar 

  79. Farag ES, Ooij P, Planken RN et al (2018) Aortic valve stenosis and aortic diameters determine the extent of increased wall shear stress in bicuspid aortic valve disease. J Magn Reson Imaging 48:522–530

    PubMed  PubMed Central  Google Scholar 

  80. Geiger J, Rahsepar AA, Suwa K et al (2018) 4D flow MRI, cardiac function, and T1-mapping: association of valve-mediated changes in aortic hemodynamics with left ventricular remodeling. J Magn Reson Imaging 48:121–131

    PubMed  Google Scholar 

  81. van Ooij P, Markl M, Collins JD et al (2017) Aortic valve stenosis alters expression of regional aortic wall shear stress: new insights from a 4-dimensional flow magnetic resonance imaging study of 571 subjects. J Am Heart Assoc 6:e005959

    PubMed  PubMed Central  Google Scholar 

  82. Shan Y, Li J, Wang Y et al (2018) Aortic stenosis exacerbates flow aberrations related to the bicuspid aortic valve fusion pattern and the aortopathy phenotype. Eur J Cardiothorac Surg 55:534–542

    PubMed Central  Google Scholar 

  83. Rizk J, Latus H, Shehu N et al (2019) Elevated diastolic wall shear stress in regurgitant semilunar valvular lesions. J Magn Reson Imaging 50:763–770

    PubMed  Google Scholar 

  84. Shan Y, Li J, Wang Y et al (2017) Aortic shear stress in patients with bicuspid aortic valve with stenosis and insufficiency. J Thorac Cardiovasc Surg 153:1263–1272.e1261

    PubMed  PubMed Central  Google Scholar 

  85. Rahman O, Scott M, Bollache E et al (2019) Interval changes in aortic peak velocity and wall shear stress in patients with bicuspid aortic valve disease. Int J Cardiovasc Imaging 35:1925–1934

    PubMed  PubMed Central  Google Scholar 

  86. Allen BD, van Ooij P, Barker AJ et al (2015) Thoracic aorta 3D hemodynamics in pediatric and young adult patients with bicuspid aortic valve. J Magn Reson Imaging 42:954–963

    PubMed  PubMed Central  Google Scholar 

  87. Stefek HA, Berhane H, Robinson JD et al (2019) Comprehensive MR analysis of cardiac function, aortic hemodynamics and left ventricular strain in pediatric cohort with isolated bicuspid aortic valve. Pediatr Cardiol 40:1450–1459

    PubMed  PubMed Central  Google Scholar 

  88. Rose MJ, Rigsby CK, Berhane H et al (2019) 4-D flow MRI aortic 3-D hemodynamics and wall shear stress remain stable over short-term follow-up in pediatric and young adult patients with bicuspid aortic valve. Pediatr Radiol 49:57–67

    PubMed  Google Scholar 

  89. Baumgartner H, Falk V, Bax JJ et al (2017) 2017 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J 38:2739–2791

    PubMed  Google Scholar 

  90. Borger MA, Fedak PWM, Stephens EH et al (2018) The American Association for Thoracic Surgery consensus guidelines on bicuspid aortic valve–related aortopathy: full online-only version. J Thorac Cardiovasc Surg 156:e41–e74

    PubMed  PubMed Central  Google Scholar 

  91. Baumgartner H, Bonhoeffer P, De Groot NM et al (2010) ESC guidelines for the management of grown-up congenital heart disease (new version 2010). Eur Heart J 31:2915–2957

    PubMed  Google Scholar 

  92. Hope MD, Meadows AK, Hope TA et al (2010) Clinical evaluation of aortic coarctation with 4D flow MR imaging. J Magn Reson Imaging 31:711–718

    PubMed  Google Scholar 

  93. Rengier F, Delles M, Eichhorn J et al (2015) Noninvasive 4D pressure difference mapping derived from 4D flow MRI in patients with repaired aortic coarctation: comparison with young healthy volunteers. Int J Cardiovasc Imaging 31:823–830

    PubMed  Google Scholar 

  94. Saitta S, Pirola S, Piatti F et al (2019) Evaluation of 4D flow MRI-based non-invasive pressure assessment in aortic coarctations. J Biomech 94:13–21

    PubMed  Google Scholar 

  95. Riesenkampff E, Fernandes JF, Meier S et al (2014) Pressure fields by flow-sensitive, 4D, velocity-encoded CMR in patients with aortic coarctation. JACC Cardiovasc Imaging 7:920–926

    PubMed  Google Scholar 

  96. Goubergrits L, Hellmeier F, Neumann D et al (2019) Patient-specific requirements and clinical validation of MRI-based pressure mapping: a two-center study in patients with aortic coarctation. J Magn Reson Imaging 49:81–89

    PubMed  Google Scholar 

  97. Nordmeyer S, Berger F, Kuehne T, Riesenkampff E (2011) Flow-sensitive four-dimensional magnetic resonance imaging facilitates and improves the accurate diagnosis of partial anomalous pulmonary venous drainage. Cardiol Young 21:528–535

    PubMed  Google Scholar 

  98. Hoohenkerk GJF, Bruggemans EF, Rijlaarsdam M, Schoof PH, Koolbergen DR, Hazekamp MG (2010) More than 30 years’ experience with surgical correction of atrioventricular septal defects. Ann Thorac Surg 90:1554–1561

    PubMed  Google Scholar 

  99. Calkoen EE, Roest AA, Kroft LJ et al (2015) Characterization and improved quantification of left ventricular inflow using streamline visualization with 4DFlow MRI in healthy controls and patients after atrioventricular septal defect correction. J Magn Reson Imaging 41:1512–1520

    PubMed  Google Scholar 

  100. Calkoen EE, Westenberg JJ, Kroft LJ et al (2015) Characterization and quantification of dynamic eccentric regurgitation of the left atrioventricular valve after atrioventricular septal defect correction with 4D Flow cardiovascular magnetic resonance and retrospective valve tracking. J Cardiovasc Magn Reson 17:18

    PubMed  PubMed Central  Google Scholar 

  101. Calkoen EE, Elbaz MS, Westenberg JJ et al (2015) Altered left ventricular vortex ring formation by 4-dimensional flow magnetic resonance imaging after repair of atrioventricular septal defects. J Thorac Cardiovasc Surg 150:1233–1240. e1231

    PubMed  Google Scholar 

  102. Khairy P, Ionescu-Ittu R, Mackie AS, Abrahamowicz M, Pilote L, Marelli AJ (2010) Changing mortality in congenital heart disease. J Am Coll Cardiol 56:1149–1157

    PubMed  Google Scholar 

  103. Al Habib HF, Jacobs JP, Mavroudis C et al (2010) Contemporary patterns of management of tetralogy of Fallot: data from the Society of Thoracic Surgeons Database. Ann Thorac Surg 90:813–820

    PubMed  Google Scholar 

  104. Geva T (2011) Repaired tetralogy of Fallot: the roles of cardiovascular magnetic resonance in evaluating pathophysiology and for pulmonary valve replacement decision support. J Cardiovasc Magn Reson 13:9

    PubMed  PubMed Central  Google Scholar 

  105. Isorni MA, Martins D, Ben Moussa N et al (2020) 4D flow MRI versus conventional 2D for measuring pulmonary flow after Tetralogy of Fallot repair. Int J Cardiol 300:132–136

    CAS  PubMed  Google Scholar 

  106. Jacobs KG, Chan FP, Cheng JY, Vasanawala SS, Maskatia SA (2020) 4D flow vs. 2D cardiac MRI for the evaluation of pulmonary regurgitation and ventricular volume in repaired tetralogy of Fallot: a retrospective case control study. Int J Cardiovasc Imaging 36:657–669

    PubMed  PubMed Central  Google Scholar 

  107. Jeong D, Anagnostopoulos PV, Roldan-Alzate A et al (2015) Ventricular kinetic energy may provide a novel noninvasive way to assess ventricular performance in patients with repaired tetralogy of Fallot. J Thorac Cardiovasc Surg 149:1339–1347

    PubMed  Google Scholar 

  108. 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 26:3598–3607

    PubMed  PubMed Central  Google Scholar 

  109. François CJ, Srinivasan S, Schiebler ML et al (2012) 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 14:16

    PubMed  PubMed Central  Google Scholar 

  110. Fredriksson A, Trzebiatowska-Krzynska A, Dyverfeldt P, Engvall J, Ebbers T, Carlhäll C-J (2018) Turbulent kinetic energy in the right ventricle: potential MR marker for risk stratification of adults with repaired tetralogy of Fallot. J Magn Reson Imaging 47:1043–1053

    PubMed  Google Scholar 

  111. Sjöberg P, Bidhult S, Bock J et al (2018) Disturbed left and right ventricular kinetic energy in patients with repaired tetralogy of Fallot: pathophysiological insights using 4D-flow MRI. Eur Radiol 28:4066–4076

    PubMed  PubMed Central  Google Scholar 

  112. Robinson JD, Rose MJ, Joh M et al (2019) 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 49:308–317

    PubMed  Google Scholar 

  113. Jatene AD, Fontes VF, de Souza LCB et al (1982) Anatomic correction of transposition of the great arteries. Am J Cardiol 49:987

    Google Scholar 

  114. Fricke TA, d'Udekem Y, Richardson M et al (2012) Outcomes of the arterial switch operation for transposition of the great arteries: 25 years of experience. Ann Thorac Surg 94:139–145

    PubMed  Google Scholar 

  115. Hutter P, Kreb D, Mantel S, Hitchcock J, Meijboom E, Bennink G (2002) Twenty-five years' experience with the arterial switch operation. J Thorac Cardiovasc Surg 124:790–797

    CAS  PubMed  Google Scholar 

  116. Geiger J, Hirtler D, Bürk J et al (2014) Postoperative pulmonary and aortic 3D haemodynamics in patients after repair of transposition of the great arteries. Eur Radiol 24:200–208

    PubMed  Google Scholar 

  117. Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248

    CAS  PubMed  PubMed Central  Google Scholar 

  118. de Leval MR, Kilner P, Gewillig M, Bull C (1988) Total cavopulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. J Thorac Cardiovasc Surg 96:682–695

  119. Gewillig M, Brown SC (2016) The Fontan circulation after 45 years: update in physiology. Heart 102:1081–1086

    PubMed  Google Scholar 

  120. Jarvis K, Schnell S, Barker AJ et al (2016) Evaluation of blood flow distribution asymmetry and vascular geometry in patients with Fontan circulation using 4-D flow MRI. Pediatr Radiol 46:1507–1519

    PubMed  PubMed Central  Google Scholar 

  121. Bächler P, Pinochet N, Sotelo J et al (2013) Assessment of normal flow patterns in the pulmonary circulation by using 4D magnetic resonance velocity mapping. Magn Reson Imaging 31:178–188

    PubMed  Google Scholar 

  122. Sundareswaran KS, Haggerty CM, De Zélicourt D et al (2012) Visualization of flow structures in Fontan patients using 3-dimensional phase contrast magnetic resonance imaging. J Thorac Cardiovasc Surg 143:1108–1116

    PubMed  Google Scholar 

  123. Imoto Y, Sese A, Joh K (2006) Redirection of the hepatic venous flow for the treatment of pulmonary arteriovenous malformations after Fontan operation. Pediatr Cardiol 27:490–492

    PubMed  Google Scholar 

  124. Shinohara T, Yokoyama T (2001) Pulmonary arteriovenous malformation in patients with total cavopulmonary shunt: what role does lack of hepatic venous blood flow to the lungs play? Pediatr Cardiol 22:343–346

    CAS  PubMed  Google Scholar 

  125. McLennan D, Schäfer M, Mitchell MB et al (2019) Usefulness of 4D-flow MRI in mapping flow distribution through failing Fontan circulation prior to cardiac intervention. Pediatr Cardiol 40:1093–1096

    PubMed  Google Scholar 

  126. Rijnberg Friso M, Hazekamp Mark G, Wentzel Jolanda J et al (2018) Energetics of blood flow in cardiovascular disease. Circulation 137:2393–2407

    CAS  PubMed  Google Scholar 

  127. Rijnberg FM, Elbaz MSM, Westenberg JJM et al (2018) Four-dimensional flow magnetic resonance imaging-derived blood flow energetics of the inferior vena cava-to-extracardiac conduit junction in Fontan patients. Eur J Cardiothorac Surg 55:1202–1210

    Google Scholar 

  128. Rutkowski DR, Barton G, François CJ, Bartlett HL, Anagnostopoulos PV, Roldán-Alzate A (2019) Analysis of cavopulmonary and cardiac flow characteristics in Fontan patients: comparison with healthy volunteers. J Magn Reson Imaging 49:1786–1799

  129. 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 38:669–680

    PubMed  PubMed Central  Google Scholar 

  130. Kamphuis VP, Elbaz MSM, Van Den Boogaard PJ et al (2019) Disproportionate intraventricular viscous energy loss in Fontan patients: analysis by 4D flow MRI. Eur Heart J Cardiovasc Imaging 20:323–333

    PubMed  Google Scholar 

  131. Kamphuis VP, Elbaz MS, van den Boogaard PJ et al (2019) Stress increases intracardiac 4D flow cardiovascular magnetic resonance-derived energetics and vorticity and relates to VO 2 max in Fontan patients. J Cardiovasc Magn Reson 21:43

    PubMed  PubMed Central  Google Scholar 

  132. Meierhofer C, Schneider EP, Lyko C et al (2013) Wall shear stress and flow patterns in the ascending aorta in patients with bicuspid aortic valves differ significantly from tricuspid aortic valves: a prospective study. Eur Heart J Cardiovasc Imaging 14:797–804

    PubMed  Google Scholar 

  133. Semaan E, Markl M, Chris Malaisrie S et al (2013) Haemodynamic outcome at four-dimensional flow magnetic resonance imaging following valve-sparing aortic root replacement with tricuspid and bicuspid valve morphology. Eur J Cardiothorac Surg 45:818–825

    PubMed  PubMed Central  Google Scholar 

  134. Mahadevia R, Barker AJ, Schnell S et al (2014) Bicuspid aortic cusp fusion morphology alters aortic 3D outflow patterns, wall shear stress and expression of aortopathy. Circulation 129:673–682

    CAS  PubMed  Google Scholar 

  135. van Ooij P, Potters WV, Collins J et al (2015) Characterization of abnormal wall shear stress using 4D flow MRI in human bicuspid aortopathy. Ann Biomed Eng 43:1385–1397

    PubMed  Google Scholar 

  136. Stephens EH, Hope TA, Kari FA et al (2015) Greater asymmetric wall shear stress in Sievers' type 1/LR compared with 0/LAT bicuspid aortic valves after valve-sparing aortic root replacement. J Thorac Cardiovasc Surg 150:59–68

    PubMed  Google Scholar 

  137. van Ooij P, Garcia J, Potters WV et al (2016) Age-related changes in aortic 3D blood flow velocities and wall shear stress: implications for the identification of altered hemodynamics in patients with aortic valve disease. J Magn Reson Imaging 43:1239–1249

    PubMed  Google Scholar 

  138. Allen BD, Markl M, Barker AJ et al (2016) Influence of beta-blocker therapy on aortic blood flow in patients with bicuspid aortic valve. Int J Cardiovasc Imaging 32:621–628

    PubMed  PubMed Central  Google Scholar 

  139. Schnell S, Smith DA, Barker AJ et al (2016) Altered aortic shape in bicuspid aortic valve relatives influences blood flow patterns. Eur Heart J Cardiovasc Imaging 17:1239–1247

    PubMed  PubMed Central  Google Scholar 

  140. Bissell MM, Loudon M, Hess AT et al (2018) Differential flow improvements after valve replacements in bicuspid aortic valve disease: a cardiovascular magnetic resonance assessment. J Cardiovasc Magn Reson 20:10

    PubMed  PubMed Central  Google Scholar 

  141. Guala A, Rodriguez-Palomares J, Dux-Santoy L et al (2019) Influence of aortic dilation on the regional aortic stiffness of bicuspid aortic valve assessed by 4-dimensional flow cardiac magnetic resonance: comparison with Marfan syndrome and degenerative aortic aneurysm. JACC Cardiovasc Imaging 12:1020–1029

    PubMed  Google Scholar 

  142. Fatehi Hassanabad A, Burns F, Bristow MS et al (2020) Pressure drop mapping using 4D flow MRI in patients with bicuspid aortic valve disease: a novel marker of valvular obstruction. Magn Reson Imaging 65:175–182

    PubMed  Google Scholar 

  143. Frydrychowicz A, Markl M, Hirtler D et al (2011) Aortic hemodynamics in patients with and without repair of aortic coarctation: in vivo analysis by 4D flow-sensitive magnetic resonance imaging. Invest Radiol 46:317–325

    PubMed  Google Scholar 

  144. Juffermans JF, Nederend I, van den Boogaard PJ et al (2019) The effects of age at correction of aortic coarctation and recurrent obstruction on adolescent patients: MRI evaluation of wall shear stress and pulse wave velocity. Eur Radiol Exp 3:24

    PubMed  PubMed Central  Google Scholar 

  145. Desai LP, Berhane H, Husain N, Robinson JD, Rigsby CK, Markl M (2020) Altered 4-D magnetic resonance imaging flow characteristics in complex congenital aortic arch repair. Pediatr Radiol 50:17–27

    PubMed  Google Scholar 

  146. Calkoen EE, de Koning PJ, Blom NA et al (2015) Disturbed intracardiac flow organization after atrioventricular septal defect correction as assessed with 4D flow magnetic resonance imaging and quantitative particle tracing. Invest Radiol 50:850–857

    PubMed  Google Scholar 

  147. Elbaz MSM, van der Geest RJ, Calkoen EE et al (2017) Assessment of viscous energy loss and the association with three-dimensional vortex ring formation in left ventricular inflow: in vivo evaluation using four-dimensional flow MRI. Magn Reson Med 77:794–805

    PubMed  Google Scholar 

  148. Elders B, Westenberg J, van den Boogaard P et al (2019) Altered ascending aortic wall shear stress in patients with corrected atrioventricular septal defect: a comprehensive cardiovascular magnetic resonance and 4D flow MRI evaluation. Cardiol Young 29:637–642

    PubMed  Google Scholar 

  149. Geiger J, Markl M, Jung B et al (2011) 4D-MR flow analysis in patients after repair for tetralogy of Fallot. Eur Radiol 21:1651–1657

    CAS  PubMed  Google Scholar 

  150. Sjöberg P, Töger J, Hedström E et al (2018) 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 315:H1691–H1702

    PubMed  Google Scholar 

  151. Lee S, Kim YJ, Jung JW et al (2019) Evaluation of flow pattern in the ascending aorta in patients with repaired tetralogy of Fallot using four-dimensional flow magnetic resonance imaging. Korean J Radiol 20:1334–1341

    PubMed  PubMed Central  Google Scholar 

  152. Schäfer M, Barker AJ, Morgan GJ et al (2020) Increased systolic vorticity in the left ventricular outflow tract is associated with abnormal aortic flow formations in tetralogy of Fallot. Int J Cardiovasc Imaging 36:691–700

    PubMed  Google Scholar 

  153. Schäfer M, Barker AJ, Jaggers J et al (2019) Abnormal aortic flow conduction is associated with increased viscous energy loss in patients with repaired tetralogy of Fallot. Eur J Cardiothorac Surg 57:588–595

    PubMed Central  Google Scholar 

  154. Riesenkampff E, Nordmeyer S, Al-Wakeel N et al (2013) Flow-sensitive four-dimensional velocity-encoded magnetic resonance imaging reveals abnormal blood flow patterns in the aorta and pulmonary trunk of patients with transposition. Cardiol Young 24:47–53

    PubMed  Google Scholar 

  155. van der Palen RL, Deurvorst QS, Kroft LJ et al (2019) Altered ascending aorta hemodynamics in patients after arterial switch operation for transposition of the great arteries. J Magn Reson Imaging 51:1105–1116

    PubMed  Google Scholar 

  156. Belhadjer Z, Soulat G, Ladouceur M et al (2019) Neopulmonary outflow tract obstruction assessment by 4D flow MRI in adults with transposition of the great arteries after arterial switch operation. J Magn Reson Imaging. https://doi.org/10.1002/jmri.27012

  157. Bächler P, Valverde I, Pinochet N et al (2013) Caval blood flow distribution in patients with Fontan circulation: quantification by using particle traces from 4D flow MR imaging. Radiology 267:67–75

    PubMed  Google Scholar 

  158. Jarvis K, Schnell S, Barker AJ et al (2019) Caval to pulmonary 3D flow distribution in patients with Fontan circulation and impact of potential 4D flow MRI error sources. Magn Reson Med 81:1205–1218

    PubMed  Google Scholar 

  159. Markl M, Schnell S, Barker AJ (2014) 4D flow imaging: current status to future clinical applications. Curr Cardiol Rep 16:481

    PubMed  Google Scholar 

  160. Petersson S, Dyverfeldt P, Ebbers T (2012) Assessment of the accuracy of MRI wall shear stress estimation using numerical simulations. J Magn Reson Imaging 36:128–138

    PubMed  Google Scholar 

  161. Zimmermann J, Demedts D, Mirzaee H et al (2018) Wall shear stress estimation in the aorta: impact of wall motion, spatiotemporal resolution, and phase noise. J Magn Reson Imaging 48:718–728

    Google Scholar 

  162. Cibis M, Potters WV, Gijsen FJ et al (2016) The effect of spatial and temporal resolution of cine phase contrast MRI on wall shear stress and oscillatory shear index assessment. PLoS One 11:e0163316

    PubMed  PubMed Central  Google Scholar 

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    Judy Rizk

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Rizk, J. 4D flow MRI applications in congenital heart disease. Eur Radiol 31, 1160–1174 (2021). https://doi.org/10.1007/s00330-020-07210-z

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