Advertisement

Clinical Applications of MRA 4D-Flow

  • Lilia M. Sierra-GalanEmail author
  • Christopher J. François
Imaging (Q Truong, Section Editor)
  • 43 Downloads
Part of the following topical collections:
  1. Topical Collection on Imaging

Abstract

Purpose of review

Four-dimensional (4D)-Flow cardiovascular magnetic resonance (CMR) is three-dimensional, time-resolved, three-directional velocity-encoded magnetic resonance that provides flow velocity data within a volumetric region across the cardiac cycle (CC). The goals of this paper are to review the current clinical applications of this technique; provide an overview of the general physics; discuss key points from the expert consensus document; and present recent advances in the field. The advantages and disadvantages of 4D-Flow CMR in comparison with the standard and gold standard methods are summarized.

Recent findings

4D-Flow CMR offers unique insights into cardiac and circulatory physiology with an ability to quantify advanced hemodynamic parameters in a variety of pathologic entities including aortic and pulmonary artery diseases, valvular heart disease, complex congenital heart disease, and extra-thoracic cardiovascular diseases. Recent large cohort studies highlight how it provides information that has clinical impact beyond a better understanding of the disease and that will permit better and more timely management and prognosis.

Summary

4D-Flow CMR provides unique qualitative and quantitative flow dynamics information and its impact on cardiac chambers, vessel walls, and myocardium. As scan acquisition and post-processing of 4D-Flow CMR become faster and simpler, the investigational and clinical opportunities will expand dramatically.

Keywords

MRA 4D-Flow 4D Flow CMR Magnetic resonance Phase contrast Blood flow Aorta 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

11936_2019_758_MOESM1_ESM.mp4 (5.3 mb)
ESM 1 (MP4 927 kb)
11936_2019_758_MOESM2_ESM.mp4 (927 kb)
ESM 2 (MP4 5382 kb)

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    •• Dyverfeldt P, Bissell M, Barker AJ, Bolger AF, Carlhall C-J, Ebbers T, et al. 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson. 2015;17:72 This reference contains the most updated agreement of experts’ opinion endorsed by the Society for Cardiovascular Magnetic Resonance (SCMR) containing state-of-the-art information.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Wigstrom L, Sjoqvist L, Wranne B. Temporally resolved 3D phase-contrast imaging. Magn Reson Med. 1996;36(5):800–3.PubMedCrossRefGoogle Scholar
  3. 3.
    Kozerke S, Hasenkam JM, Pedersen EM, Boesiger P. Visualization of flow patterns distal to aortic valve prostheses in humans using a fast approach for cine 3D velocity mapping. J Magn Reson Imaging. 2001;13(5):690–8.PubMedCrossRefGoogle Scholar
  4. 4.
    • Bustamante M, Gupta V, Carlhall C-J, Ebbers T. Improving visualization of 4D flow cardiovascular magnetic resonance with four-dimensional angiographic data: generation of a 4D phase-contrast magnetic resonance cardioAngiography (4D PC-MRCA). J Cardiovasc Magn Reson. 2017;19(1):47.This article describes an alternative method, the 4D PC-MRCA that can visualize the motion of the heart and great vessels across the cardiac cycle in addition to conventional 4D Flow CMR.Google Scholar
  5. 5.
    Dumoulin CL. Phase contrast MR angiography techniques. Magn Reson Imaging Clin N Am. 1995;3(3):399–411.PubMedGoogle Scholar
  6. 6.
    Gatehouse PD, Keegan J, Crowe LA, Masood S, Mohiaddin RH, Kreitner K-F, et al. Applications of phase-contrast flow and velocity imaging in cardiovascular MRI. Eur Radiol. 2005;15(10):2172–84.PubMedCrossRefGoogle Scholar
  7. 7.
    Markl M, Kilner PJ, Ebbers T. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2011;13:7.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Dumoulin CL, Souza SP, Walker MF, Wagle W. Three-dimensional phase contrast angiography. Magn Reson Med. 1989;9(1):139–49.PubMedCrossRefGoogle Scholar
  9. 9.
    Markl M, Harloff A, Bley TA, Zaitsev M, Jung B, Weigang E, et al. Time-resolved 3D MR velocity mapping at 3T: improved navigator-gated assessment of vascular anatomy and blood flow. J Magn Reson Imaging. 2007;25(4):824–31.PubMedCrossRefGoogle Scholar
  10. 10.
    Frydrychowicz A, Berger A, Munoz Del Rio A, Russe MF, Bock J, Harloff A, et al. Interdependencies of aortic arch secondary flow patterns, geometry, and age analysed by 4-dimensional phase contrast magnetic resonance imaging at 3 Tesla. Eur Radiol. 2012;22(5):1122–30.PubMedCrossRefGoogle Scholar
  11. 11.
    • Schnell S, Entezari P, Mahadewia RJ, Malaisrie SC, McCarthy PM, Collins JD, et al. Improved semiautomated 4D flow MRI analysis in the aorta in patients with congenital aortic valve anomalies versus tricuspid aortic valves. J Comput Assist Tomogr. 2016;40(1):102–8.In biscuspid and tricuspid aotric valves 4D Flow CMR using semiautomated analysis of aotric hemodynamics shows accuracy and reproducibility; which is better for peak velocity measurements than for regurgitant flows.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Bustamante M, Petersson S, Eriksson J, Alehagen U, Dyverfeldt P, Carlhall C-J, et al. Atlas-based analysis of 4D flow CMR: automated vessel segmentation and flow quantification. J Cardiovasc Magn Reson. 2015;17:87.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Harloff A, Nussbaumer A, Bauer S, Stalder AF, Frydrychowicz A, Weiller C, et al. In vivo assessment of wall shear stress in the atherosclerotic aorta using flow-sensitive 4D MRI. Magn Reson Med. 2010;63(6):1529–36.PubMedCrossRefGoogle Scholar
  14. 14.
    • Isorni M-A, Tortigue M, Ben MN, Hascoët S, Monnot S. 4D flow CMR analysis in repaired tetralogy of Fallot: where we are and where we are going. Arch Cardiovasc Dis Suppl. 2018;10(3):285. Available from: http://www.sciencedirect.com/science/article/pii/S1878648018302192.4D Flow CMR is useful in repaired Tetralogy of Fallot with good diagnostic accuracy.CrossRefGoogle Scholar
  15. 15.
    •• Garcia J, Barker AJ, Murphy I, Jarvis K, Schnell S, Collins JD, et al. 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. 2016;17(8):877–84 This paper analyzes the impact of different morphology and hemodynamic of the aorta by age and gender groups along with aortic diameters contributing to further application of the technique in the clinical practice.PubMedCrossRefGoogle Scholar
  16. 16.
    •• Azarine A, Garçon P, Stansal A, Canepa N, Angelopoulos G, Silvera S, et al. Four-dimensional flow MRI: principles and cardiovascular applications. RadioGraphics. 2019;39(3):632–48.  https://doi.org/10.1148/rg.2019180091 This paper provides a comprehensive approach to the technique to a physician with more radiological-oriented background.CrossRefPubMedGoogle Scholar
  17. 17.
    Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O. 4D flow MRI. J Magn Reson Imaging. 2012;36(5):1015–36.  https://doi.org/10.1002/jmri.23632.CrossRefPubMedGoogle Scholar
  18. 18.
    Carlsson M, Töger J, Kanski M, Bloch KM, Ståhlberg F, Heiberg E, et al. 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. 2011;13(1):55.  https://doi.org/10.1186/1532-429X-13-55.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Markl M, Wallis W, Harloff A. Reproducibility of flow and wall shear stress analysis using flow-sensitive four-dimensional MRI. J Magn Reson Imaging. 2011;33(4):988–94.PubMedCrossRefGoogle Scholar
  20. 20.
    Uribe S, Beerbaum P, Sorensen TS, Rasmusson A, Razavi R, Schaeffter T. Four-dimensional (4D) flow of the whole heart and great vessels using real-time respiratory self-gating. Magn Reson Med. 2009;62(4):984–92.PubMedCrossRefGoogle Scholar
  21. 21.
    Wentland AL, Grist TM, Wieben O. Repeatability and internal consistency of abdominal 2D and 4D phase contrast MR flow measurements. Acad Radiol. 2013;20(6):699–704. Available from: https://www.ncbi.nlm.nih.gov/pubmed/23510798.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Brix L, Ringgaard S, Rasmusson A, Sorensen TS, Kim WY. Three dimensional three component whole heart cardiovascular magnetic resonance velocity mapping: comparison of flow measurements from 3D and 2D acquisitions. J Cardiovasc Magn Reson. 2009;11:3.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Hope MD, Meadows AK, Hope TA, Ordovas KG, Saloner D, Reddy GP, et al. Clinical evaluation of aortic coarctation with 4D flow MR imaging. J Magn Reson Imaging. 2010;31(3):711–8.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Nordmeyer S, Riesenkampff E, Crelier G, Khasheei A, Schnackenburg B, Berger F, et al. Flow-sensitive four-dimensional cine magnetic resonance imaging for offline blood flow quantification in multiple vessels: a validation study. J Magn Reson Imaging. 2010;32(3):677–83.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Valverde I, Nordmeyer S, Uribe S, Greil G, Berger F, Kuehne T, et al. Systemic-to-pulmonary collateral flow in patients with palliated univentricular heart physiology: measurement using cardiovascular magnetic resonance 4D velocity acquisition. J Cardiovasc Magn Reson 2012;14(1):25. Available from: https://www.ncbi.nlm.nih.gov/pubmed/22541134.
  26. 26.
    Nordmeyer S, Riesenkampff E, Messroghli D, Kropf S, Nordmeyer J, Berger F, et al. Four-dimensional velocity-encoded magnetic resonance imaging improves blood flow quantification in patients with complex accelerated flow. J Magn Reson Imaging. 2013;37(1):208–16.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Giese D, Wong J, Greil GF, Buehrer M, Schaeffter T, Kozerke S. Towards highly accelerated Cartesian time-resolved 3D flow cardiovascular magnetic resonance in the clinical setting. J Cardiovasc Magn Reson. 2014;16(1):42.  https://doi.org/10.1186/1532-429X-16-42.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    François CJ, Lum DP, Johnson KM, Landgraf BR, Bley TA, Reeder SB, et al. Renal arteries: isotropic, high-spatial-resolution, unenhanced MR angiography with three-dimensional radial phase contrast. Radiology. 2011;258(1):254–60. Available from: https://www.ncbi.nlm.nih.gov/pubmed/20980449.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    François 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. Available from: https://www.ncbi.nlm.nih.gov/pubmed/22313680.Whole heart 4D VM-CMR enables detection of both normal and abnormal right heart flow patterns and main pulmonary artery hemodynamics in tetralogy of Fallot of post-surgically altered geometries and hemodynamics.
  30. 30.
    Uribe S, Bachler P, Valverde I, Crelier GR, Beerbaum P, Tejos C, et al. Hemodynamic assessment in patients with one-and-a-half ventricle repair revealed by four-dimensional flow magnetic resonance imaging. Pediatr Cardiol. 2013;34(2):447–51.PubMedCrossRefGoogle Scholar
  31. 31.
    Geiger J, Hirtler D, Burk J, Stiller B, Arnold R, Jung B, et al. Postoperative pulmonary and aortic 3D haemodynamics in patients after repair of transposition of the great arteries. Eur Radiol. 2014;24(1):200–8.PubMedCrossRefGoogle Scholar
  32. 32.
    • van Wijk WHS, Breur JMPJ, Westenberg JJM, Driessen MMP, Meijboom FJ, Driesen B, et al. 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. 2019;21(1):20.  https://doi.org/10.1186/s12968-019-0527-6.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hope MD, Hope TA, Crook SES, Ordovas KG, Urbania TH, Alley MT, et al. 4D flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging. 2011;4:781–7.PubMedCrossRefGoogle Scholar
  34. 34.
    Hope MD, Hope TA, Meadows AK, Ordovas KG, Urbania TH, Alley MT, et al. Bicuspid aortic valve: four-dimensional MR evaluation of ascending aortic systolic flow patterns. Radiology. 2010;255(1):53–61.PubMedCrossRefGoogle Scholar
  35. 35.
    Hope MD, Dyverfeldt P, Acevedo-Bolton G, Wrenn J, Foster E, Tseng E, et al. Post-stenotic dilation: evaluation of ascending aortic dilation with 4D flow MR imaging. Vol. 156, International journal of cardiology. Netherlands; 2012. p. e40–2.Google Scholar
  36. 36.
    Bissell MM, Hess AT, Biasiolli L, Glaze SJ, Loudon M, Pitcher A, et al. Aortic dilation in bicuspid aortic valve disease: flow pattern is a major contributor and differs with valve fusion type. Circ Cardiovasc Imaging. 2013;6(4):499–507.PubMedCrossRefGoogle Scholar
  37. 37.
    •• Garcia J, Barker AJ, Markl M. The role of imaging of flow patterns by 4D flow MRI in aortic stenosis. JACC Cardiovasc Imaging. 2019;12(2):252 LP–266 Available from: http://imaging.onlinejacc.org/content/12/2/252.abstract. This paper analyzes the impact of different flow patterns of aortic stenosis to help understanding some of the pathophysiological reasons to aortic dilatation in some but not all patients.CrossRefGoogle Scholar
  38. 38.
    Hope MD, Hope TA, Urbania TH, Higgins CB. Four-dimensional flow magnetic resonance imaging with wall shear stress analysis before and after repair of aortopulmonary fistula. Circ Cardiovasc Imaging. 2010;3(6):766–8.  https://doi.org/10.1161/CIRCIMAGING.110.957712.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Frydrychowicz A, Markl M, Hirtler D, Harloff A, Schlensak C, Geiger J, et al. Aortic hemodynamics in patients with and without repair of aortic coarctation: in vivo analysis by 4D flow-sensitive magnetic resonance imaging. Invest Radiol. 2011;46(5):317–25.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Barker AJ, Lanning C, Shandas R. Quantification of hemodynamic wall shear stress in patients with bicuspid aortic valve using phase-contrast MRI. Ann Biomed Eng. 2010;38(3):788–800.PubMedCrossRefGoogle Scholar
  41. 41.
    Sigovan M, Hope MD, Dyverfeldt P, Saloner D. Comparison of four-dimensional flow parameters for quantification of flow eccentricity in the ascending aorta. J Magn Reson Imaging. 2011;34(5):1226–30.PubMedCrossRefGoogle Scholar
  42. 42.
    den Reijer PM, Sallee D 3rd, van der Velden P, Zaaijer ER, Parks WJ, Ramamurthy S, et al. Hemodynamic predictors of aortic dilatation in bicuspid aortic valve by velocity-encoded cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2010;12:4.CrossRefGoogle Scholar
  43. 43.
    •• Allen BD, Aouad PJ, Burris NS, Rahsepar AA, Jarvis KB, François CJ, et al. Detection and hemodynamic evaluation of flap fenestrations in type B aortic dissection with 4D flow MRI: comparison with conventional MRI and CT angiography. Radiol Cardiothorac Imaging. 2019;1(1):e180009.  https://doi.org/10.1148/ryct.2019180009 This paper shows further clinical unique possibilities of the technique that could change the patient treatment and prognosis.CrossRefGoogle Scholar
  44. 44.
    Harloff A, Strecker C, Frydrychowicz AP, Dudler P, Hetzel A, Geibel A, et al. Plaques in the descending aorta: a new risk factor for stroke? Visualization of potential embolization pathways by 4D MRI. J Magn Reson Imaging. 2007;26(6):1651–5.PubMedCrossRefGoogle Scholar
  45. 45.
    Svedlund S, Wetterholm R, Volkmann R, Caidahl K. Retrograde blood flow in the aortic arch determined by transesophageal Doppler ultrasound. Cerebrovasc Dis. 2009;27(1):22–8 Available from: https://www.ncbi.nlm.nih.gov/pubmed/19018134.PubMedCrossRefGoogle Scholar
  46. 46.
    Bogren HG, Buonocore MH, Valente RJ. Four-dimensional magnetic resonance velocity mapping of blood flow patterns in the aorta in patients with atherosclerotic coronary artery disease compared to age-matched normal subjects. J Magn Reson Imaging. 2004;19(4):417–27.PubMedCrossRefGoogle Scholar
  47. 47.
    Markl M, Geiger J, Kilner PJ, Foll D, Stiller B, Beyersdorf F, et al. Time-resolved three-dimensional magnetic resonance velocity mapping of cardiovascular flow paths in volunteers and patients with Fontan circulation. Eur J Cardiothorac Surg. 2011;39(2):206–12.PubMedCrossRefGoogle Scholar
  48. 48.
    Reiter G, Reiter U, Kovacs G, Kainz B, Schmidt K, Maier R, et al. Magnetic resonance-derived 3-dimensional blood flow patterns in the main pulmonary artery as a marker of pulmonary hypertension and a measure of elevated mean pulmonary arterial pressure. Circ Cardiovasc Imaging. 2008;1(1):23–30.PubMedCrossRefGoogle Scholar
  49. 49.
    Helderman F, Mauritz G-J, Andringa KE, Vonk-Noordegraaf A, Marcus JT. Early onset of retrograde flow in the main pulmonary artery is a characteristic of pulmonary arterial hypertension. J Magn Reson Imaging. 2011;33(6):1362–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Sanz J, Kuschnir P, Rius T, Salguero R, Sulica R, Einstein AJ, et al. Pulmonary arterial hypertension: noninvasive detection with phase-contrast MR imaging. Radiology. 2007;243(1):70–9.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Yang GZ, Kilner PJ, Wood NB, Underwood SR, Firmin DN. Computation of flow pressure fields from magnetic resonance velocity mapping. Magn Reson Med. 1996;36(4):520–6.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    •• Markl M, Lee DC, Furiasse N, Carr M, Foucar C, Ng J, et al. Left atrial and left atrial appendage 4D blood flow dynamics in atrial fibrillation. Circ Cardiovasc Imaging. 2016;9(9):e004984 This paper shows further clinical application of the technique in a very important area that could provide additional information to improve the timing of the treatment and prognosis of atrial fibrillation.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kim WY, Walker PG, Pedersen EM, Poulsen JK, Oyre S, Houlind K, et al. Left ventricular blood flow patterns in normal subjects: a quantitative analysis by three-dimensional magnetic resonance velocity mapping. J Am Coll Cardiol. 1995;26(1):224–38.PubMedCrossRefGoogle Scholar
  54. 54.
    Eriksson J, Carlhäll CJ, Dyverfeldt P, Engvall J, Bolger AF, Ebbers T. Semi-automatic quantification of 4D left ventricular blood flow. J Cardiovasc Magn Reson. 2010;12(1):9.  https://doi.org/10.1186/1532-429X-12-9.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Bolger AF, Heiberg E, Karlsson M, Wigstrom L, Engvall J, Sigfridsson A, et al. Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2007;9(5):741–7.PubMedCrossRefGoogle Scholar
  56. 56.
    Carlhall CJ, Bolger A. Passing strange: flow in the failing ventricle. Circ Heart Fail. 2010;3(2):326–31.PubMedCrossRefGoogle Scholar
  57. 57.
    Toger J, Carlsson M, Soderlind G, Arheden H, Heiberg E. Volume tracking: a new method for quantitative assessment and visualization of intracardiac blood flow from three-dimensional, time-resolved, three-component magnetic resonance velocity mapping. BMC Med Imaging. 2011;11:10.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Geiger J, Markl M, Jung B, Grohmann J, Stiller B, Langer M, et al. 4D-MR flow analysis in patients after repair for tetralogy of Fallot. Eur Radiol. 2011;21(8):1651–7.PubMedCrossRefGoogle Scholar
  59. 59.
    • Barker N, Fidock B, Johns CS, Kaur H, Archer G, Rajaram S, et al. A systematic review of right ventricular diastolic assessment by 4D flow CMR. Biomed Res Int. 2019;2019:6074984.CrossRefGoogle Scholar
  60. 60.
    Roes SD, Hammer S, van der Geest RJ, Marsan NA, Bax JJ, Lamb HJ, et al. Flow assessment through four heart valves simultaneously using 3-dimensional 3-directional velocity-encoded magnetic resonance imaging with retrospective valve tracking in healthy volunteers and patients with valvular regurgitation. Invest Radiol. 2009;44(10):669–75.PubMedCrossRefGoogle Scholar
  61. 61.
    Westenberg JJM, Roes SD, Ajmone Marsan N, Binnendijk NMJ, Doornbos J, Bax JJ, et al. Mitral valve and tricuspid valve blood flow: accurate quantification with 3D velocity-encoded MR imaging with retrospective valve tracking. Radiology. 2008;249(3):792–800.PubMedCrossRefGoogle Scholar
  62. 62.
    Dyverfeldt P, Kvitting J-PE, Sigfridsson A, Engvall J, Bolger AF, Ebbers T. Assessment of fluctuating velocities in disturbed cardiovascular blood flow: in vivo feasibility of generalized phase-contrast MRI. J Magn Reson Imaging. 2008;28(3):655–63.PubMedCrossRefGoogle Scholar
  63. 63.
    Kvitting J-PE, Ebbers T, Wigstrom L, Engvall J, Olin CL, Bolger AF. Flow patterns in the aortic root and the aorta studied with time-resolved, 3-dimensional, phase-contrast magnetic resonance imaging: implications for aortic valve-sparing surgery. J Thorac Cardiovasc Surg. 2004;127(6):1602–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Markl M, Draney MT, Miller DC, Levin JM, Williamson EE, Pelc NJ, et al. Time-resolved three-dimensional magnetic resonance velocity mapping of aortic flow in healthy volunteers and patients after valve-sparing aortic root replacement. J Thorac Cardiovasc Surg. 2005;130(2):456–63.PubMedCrossRefGoogle Scholar
  65. 65.
    • Guglielmo M, Muscogiuri G, Baggiano A, Guaricci A, Andreini D, Mushtaq S, et al. Cardiac magnetic resonance with 4D flow imaging for mitral regurgitation severity assessment. Eur Heart J Cardiovasc Imaging. 2019;20(Supplement 2):ii120–63.4D flow CMR allows good accuracy in the evaluation of mitral regurgitation severity analysis even in post-surgically repaired ventricles with altered geometry.Google Scholar
  66. 66.
    Nanashima A, Shibasaki S, Sakamoto I, Sueyoshi E, Sumida Y, Abo T, et al. Clinical evaluation of magnetic resonance imaging flowmetry of portal and hepatic veins in patients following hepatectomy. Liver Int. 2006;26(5):587–94.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Applegate GR, Thaete FL, Meyers SP, Davis PL, Talagala SL, Recht M, et al. Blood flow in the portal vein: velocity quantitation with phase-contrast MR angiography. Radiology. 1993;187(1):253–6.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Bley TA, Johnson KM, François CJ, Reeder SB, Schiebler ML, Landgraf RB, et al. Noninvasive assessment of transstenotic pressure gradients in porcine renal artery stenoses by using vastly undersampled phase-contrast MR angiography. Radiology. 2011;261(1):266–73 Available from: https://www.ncbi.nlm.nih.gov/pubmed/21813739.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Markl M, Wegent F, Zech T, Bauer S, Strecker C, Schumacher M, et al. In vivo wall shear stress distribution in the carotid artery: effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy. Circ Cardiovasc Imaging. 2010;3(6):647–55.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Lee S-W, Antiga L, Spence JD, Steinman DA. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke. 2008;39(8):2341–7.PubMedCrossRefGoogle Scholar
  71. 71.
    Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJAP, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113(23):2744–53.PubMedCrossRefGoogle Scholar
  72. 72.
    Hope TA, Hope MD, Purcell DD, von Morze C, Vigneron DB, Alley MT, et al. Evaluation of intracranial stenoses and aneurysms with accelerated 4D flow. Magn Reson Imaging. 2010;28(1):41–6.PubMedCrossRefGoogle Scholar
  73. 73.
    Isoda H, Ohkura Y, Kosugi T, Hirano M, Takeda H, Hiramatsu H, et al. In vivo hemodynamic analysis of intracranial aneurysms obtained by magnetic resonance fluid dynamics (MRFD) based on time-resolved three-dimensional phase-contrast MRI. Neuroradiology. 2010;52(10):921–8.PubMedCrossRefGoogle Scholar
  74. 74.
    Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, et al. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke. 2008;39(11):2997–3002.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Frydrychowicz A, Winterer JT, Zaitsev M, Jung B, Hennig J, Langer M, et al. Visualization of iliac and proximal femoral artery hemodynamics using time-resolved 3D phase contrast MRI at 3T. J Magn Reson Imaging. 2007;25(5):1085–92.PubMedCrossRefGoogle Scholar
  76. 76.
    Frydrychowicz A, Wieben O, Niespodzany E, Reeder SB, Johnson KM, Francois CJ. Quantification of thoracic blood flow using volumetric magnetic resonance imaging with radial velocity encoding: in vivo validation. Invest Radiol. 2013;48(12):819–25.PubMedCrossRefGoogle Scholar
  77. 77.
    Nett EJ, Johnson KM, Frydrychowicz A, Del Rio AM, Schrauben E, Francois CJ, et al. Four-dimensional phase contrast MRI with accelerated dual velocity encoding. J Magn Reson Imaging. 2012;35(6):1462–71.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Hanneman K, Sivagnanam M, Nguyen ET, Wald R, Greiser A, Crean AM, et al. 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. 2014;21(8):1002–8.PubMedCrossRefGoogle Scholar
  79. 79.
    Bock, J; Kreher, BW; Hennig JMM. Optimized pre-processing of time-resolved 2D and 3D phase contrast MRI data. In: Proc Intl Soc Mag Reson Med. 2007. p. 3138. Available from: https://cds.ismrm.org/ismrm-2007/files/03138.pdf.
  80. 80.
    Bock J, Frydrychowicz A, Stalder AF, Bley TA, Burkhardt H, Hennig J, et al. 4D phase contrast MRI at 3 T: effect of standard and blood-pool contrast agents on SNR, PC-MRA, and blood flow visualization. Magn Reson Med. 2010;63(2):330–8.PubMedCrossRefGoogle Scholar
  81. 81.
    Petersson S, Dyverfeldt P, Ebbers T. Assessment of the accuracy of MRI wall shear stress estimation using numerical simulations. J Magn Reson Imaging. 2012;36(1):128–38.PubMedCrossRefGoogle Scholar
  82. 82.
    •• Prsa, M; Tenisch, E; Piccini, D; Ning, J; Bouchardy JBC et al. 4D flow CMR vs. 2D cine PC­CMR for flow volume quantification in congenital heart disease. In: European Heart Journal ­ Cardiovascular Imaging (2019) 20 (Supplement 2), ii493 [Internet]. 2019. p. P611. Available from: https://esc365.escardio.org/Congress/EuroCMR-2019/Poster-session-3/191835-4d-flow-cmr-vs-2d-cine-pc-cmr-for-flow-volume-quantification-in-congenital-heart-disease#abstract. This paper shows the comparison in diagnosis accuracy of the new technique and the traditional 2D-PC CMR approach in congenital heart disease.
  83. 83.
    • Stam K, Chelu RG, van der Velde N, van Duin R, Wielopolski P, Nieman K, et al. Validation of 4D flow CMR against simultaneous invasive hemodynamic measurements: a swine study. Int J Cardiovasc Imaging. 2019;35(6):1111–8.This article shows that 4D-Flow CMR of the aortic flow in animals has an accurate correlation with simultaneous invasive hemodynamic measurements.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Markl M, Wallis W, Brendecke S, Simon J, Frydrychowicz A, Harloff A. Estimation of global aortic pulse wave velocity by flow-sensitive 4D MRI. Magn Reson Med. 2010;63(6):1575–82.PubMedCrossRefGoogle Scholar
  85. 85.
    Wentland AL, Wieben O, Francois CJ, Boncyk C, Munoz Del Rio A, Johnson KM, et al. Aortic pulse wave velocity measurements with undersampled 4D flow-sensitive MRI: comparison with 2D and algorithm determination. J Magn Reson Imaging. 2013;37(4):853–9.PubMedCrossRefGoogle Scholar
  86. 86.
    Dyverfeldt P, Ebbers T, Lanne T. Pulse wave velocity with 4D flow MRI: systematic differences and age-related regional vascular stiffness. Magn Reson Imaging. 2014;32(10):1266–71.PubMedCrossRefGoogle Scholar
  87. 87.
    Dyverfeldt P, Sigfridsson A, Kvitting J-PE, Ebbers T. Quantification of intravoxel velocity standard deviation and turbulence intensity by generalizing phase-contrast MRI. Magn Reson Med. 2006;56(4):850–8.PubMedCrossRefGoogle Scholar
  88. 88.
    Binter C, Knobloch V, Manka R, Sigfridsson A, Kozerke S. Bayesian multipoint velocity encoding for concurrent flow and turbulence mapping. Magn Reson Med. 2013;69(5):1337–45.PubMedCrossRefGoogle Scholar
  89. 89.
    Dyverfeldt P, Gardhagen R, Sigfridsson A, Karlsson M, Ebbers T. On MRI turbulence quantification. Magn Reson Imaging. 2009;27(7):913–22.PubMedCrossRefGoogle Scholar
  90. 90.
    Ebbers T, Wigstrom L, Bolger AF, Wranne B, Karlsson M. Noninvasive measurement of time-varying three-dimensional relative pressure fields within the human heart. J Biomech Eng. 2002;124(3):288–93.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Riesenkampff E, Fernandes JF, Meier S, Goubergrits L, Kropf S, Schubert S, et al. Pressure fields by flow-sensitive, 4D, velocity-encoded CMR in patients with aortic coarctation. JACC Cardiovasc Imaging. 2014;7(9):920–6. Available from: http://www.sciencedirect.com/science/article/pii/S1936878X14004896.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Eriksson J, Bolger AF, Ebbers T, Carlhall C-J. Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy. Eur Heart J Cardiovasc Imaging. 2013;14(5):417–24.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Gatehouse PD, Rolf MP, Graves MJ, Hofman MB, Totman J, Werner B, et al. Flow measurement by cardiovascular magnetic resonance: a multi-centre multi-vendor study of background phase offset errors that can compromise the accuracy of derived regurgitant or shunt flow measurements. J Cardiovasc Magn Reson. 2010;12:5.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Zwart NR, Pipe JG. Multidirectional high-moment encoding in phase contrast MRI. Magn Reson Med. 2013;69(6):1553–64.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Markl M, Bammer R, Alley MT, Elkins CJ, Draney MT, Barnett A, et al. Generalized reconstruction of phase contrast MRI: analysis and correction of the effect of gradient field distortions. Magn Reson Med. 2003;50(4):791–801.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Peeters JM, Bos C, Bakker CJG. Analysis and correction of gradient nonlinearity and B0 inhomogeneity related scaling errors in two-dimensional phase contrast flow measurements. Magn Reson Med. 2005;53(1):126–33.PubMedCrossRefGoogle Scholar
  97. 97.
    • van der Geest RJ, Garg P. Advanced analysis techniques for intra-cardiac flow evaluation from 4D flow MRI. Curr Radiol Rep. 2016;4(7):38.  https://doi.org/10.1007/s40134-016-0167-7.This article reviews different aspects of 4D Flow CMR in the evaluation of intracardiac flow.
  98. 98.
    • Crandon S, Westenberg JJM, Swoboda PP, Fent GJ, Foley JRJ, Chew PG, et al. Impact of age and diastolic function on novel, 4D flow CMR biomarkers of left ventricular blood flow kinetic energy. Sci Rep. 2018;8(1):14436.  https://doi.org/10.1038/s41598-018-32707-5.This article describes 4D flow CMR normal diastolic, kinetic energy parameters of left ventricular flow in different age groups and its good accuracy with standard metrics.
  99. 99.
    • Schrauben EM, Saini BS, Darby JRT, Soo JY, Lock MC, Stirrat E, et al. Fetal hemodynamics and cardiac streaming assessed by 4D flow cardiovascular magnetic resonance in fetal sheep. J Cardiovasc Magn Reson. 2019;21(1):8.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Lilia M. Sierra-Galan
    • 1
    Email author
  • Christopher J. François
    • 2
  1. 1.American British Cowdray Medical Center05300, Mexico CityMexico
  2. 2.School of Medicine and Public HealthUniversity of WisconsinMadisonUSA

Personalised recommendations