Share：
Share this content in WeChat
X
[Chinese][PDF]541
• Review •
Advances in 4D Flow CMR quantitative analysis of intracardiac hemodynamics
ZHANG Mengyuan  LIU Fenghai  LI Guoce  WANG Xiaoyu 

Cite this article as: ZHANG M Y, LIU F H, LI G C, et al. Advances in 4D Flow CMR quantitative analysis of intracardiac hemodynamics[J]. Chin J Magn Reson Imaging, 2024, 15(10): 193-199, 210. DOI:10.12015/issn.1674-8034.2024.10.033.


[Abstract] Currently, research on cardiac function evaluation mainly focuses on observing ventricular wall motion and deformation, as well as measuring the velocity of heart valves. Meanwhile, assessing the complex hemodynamics within the heart is an essential part of diagnosing and treating cardiovascular diseases. With the development of four-dimensional flow cardiac magnetic resonance imaging (4D Flow CMR), this technology can comprehensively and retrospectively evaluate cardiac anatomy and function, allowing measurements within the heart area and quantifying and visualizing changes in cardiac hemodynamics through parameters such as kinetic energy (KE), flow components, and vorticity. This review summarizes the principles of 4D Flow CMR technology, data acquisition and post-processing, its advantages and disadvantages, and discusses the analysis of cardiac hemodynamics using KE, flow components, and vorticity parameters. Finally, it compares existing techniques for analyzing intracardiac hemodynamics, summarizes the latest developments, and proposes prospects for the development of 4D Flow CMR technology and its clinical applications. This review can provide a new perspective for future exploration of cardiac diseases using 4D Flow CMR technology, aiming to offer physiological and pathological references for the progression and prognosis of diseases.
[Keywords] cardiac；magnetic resonance imaging；four-dimensional flow cardiac magnetic resonance；hemodynamics；quantitative analysis

ZHANG Mengyuan   LIU Fenghai*   LI Guoce   WANG Xiaoyu  

Department of Magnetic Resonance Imaging, Cangzhou Central Hospital Affiliated to Hebei Medical University, Cangzhou 061000, China

Corresponding author: LIU F H, E-mail: 1874210040@qq.com

Conflicts of interest   None.

Received  2024-06-29
Accepted  2024-10-10
DOI: 10.12015/issn.1674-8034.2024.10.033
Cite this article as: ZHANG M Y, LIU F H, LI G C, et al. Advances in 4D Flow CMR quantitative analysis of intracardiac hemodynamics[J]. Chin J Magn Reson Imaging, 2024, 15(10): 193-199, 210. DOI:10.12015/issn.1674-8034.2024.10.033.

[1]
GOLDSBOROUGH E, OSUJI N, BLAHA M J. Assessment of cardiovascular disease risk: a 2022Update[J]. Endocrinol Metab Clin North Am, 2022, 51(3): 483-509. DOI: 10.1016/j.ecl.2022.02.005.
[2]
MELE D, SMARRAZZO V, PEDRIZZETTI G, et al. Intracardiac flow analysis: techniques and potential clinical applications[J]. J Am Soc Echocardiogr, 2019, 32(3): 319-332. DOI: 10.1016/j.echo.2018.10.018.
[3]
CRANDON S, ELBAZ M S M, WESTENBERG J J M, et al. Clinical applications of intra-cardiac four-dimensional flow cardiovascular magnetic resonance: a systematic review[J/OL]. Int J Cardiol, 2017, 249: 486-493 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/28964555/. DOI: 10.1016/j.ijcard.2017.07.023.
[4]
STRÄTER A, HUBER A, RUDOLPH J, et al. 4D-flow MRI: technique and applications[J]. Rofo, 2018, 190(11): 1025-1035. DOI: 10.1055/a-0647-2021.
[5]
ASHKIR Z, MYERSON S, NEUBAUER S, et al. Four-dimensional flow cardiac magnetic resonance assessment of left ventricular diastolic function[J/OL]. Front Cardiovasc Med, 2022, 9: 866131 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/35935619/. DOI: 10.3389/fcvm.2022.866131.
[6]
BISSELL M M, RAIMONDI F, AIT ALI L, et al. 4D Flow cardiovascular magnetic resonance consensus statement: 2023 update[J/OL]. J Cardiovasc Magn Reson, 2023, 25(1): 40 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/37474977/. DOI: 10.1186/s12968-023-00942-z.
[7]
VAN HESPEN K M, KUIJF H J, HENDRIKSE J, et al. Blood flow velocity pulsatility and arterial diameter pulsatility measurements of the intracranial arteries using 4D PC-MRI[J]. Neuroinformatics, 2022, 20(2): 317-326. DOI: 10.1007/s12021-021-09526-7.
[8]
KROEGER J R, PAVESIO F C, MÖRSDORF R, et al. Velocity quantification in 44 healthy volunteers using accelerated multi-VENC 4D flow CMR[J/OL]. Eur J Radiol, 2021, 137: 109570 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/33596498/. DOI: 10.1016/j.ejrad.2021.109570.
[9]
DEMIRKIRAN A, VAN OOIJ P, WESTENBERG J J M, et al. Clinical intra-cardiac 4D flow CMR: acquisition, analysis, and clinical applications[J]. Eur Heart J Cardiovasc Imaging, 2022, 23(2): 154-165. DOI: 10.1093/ehjci/jeab112.
[10]
MARKL M, FRYDRYCHOWICZ A, KOZERKE S, et al. 4D flow MRI[J]. J Magn Reson Imaging, 2012, 36(5): 1015-1036. DOI: 10.1002/jmri.23632.
[11]
AZARINE A, GARÇON P, STANSAL A, et al. Four-dimensional flow MRI: principles and cardiovascular applications[J]. Radiographics, 2019, 39(3): 632-648. DOI: 10.1148/rg.2019180091.
[12]
DEMIRKIRAN A, HASSELL M E C J, GARG P, et al. Left ventricular four-dimensional blood flow distribution, energetics, and vorticity in chronic myocardial infarction patients with/without left ventricular thrombus[J/OL]. Eur J Radiol, 2022, 150: 110233 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/35278980/. DOI: 10.1016/j.ejrad.2022.110233.
[13]
VOS J L, LEINER T, VAN DIJK A P J, et al. Cardiovascular magnetic resonance-derived left ventricular intraventricular pressure gradients among patients with precapillary pulmonary hypertension[J]. Eur Heart J Cardiovasc Imaging, 2022, 24(1): 78-87. DOI: 10.1093/ehjci/jeab294.
[14]
OECHTERING T H, NOWAK A, SIEREN M M, et al. Repeatability and reproducibility of various 4D Flow MRI postprocessing software programs in a multi-software and multi-vendor cross-over comparison study[J/OL]. J Cardiovasc Magn Reson, 2023, 25(1): 22 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/36978131/. DOI: 10.1186/s12968-023-00921-4.
[15]
KHAN J N, MCCANN G P. Cardiovascular magnetic resonance imaging assessment of outcomes in acute myocardial infarction[J]. World J Cardiol, 2017, 9(2): 109-133. DOI: 10.4330/wjc.v9.i2.109.
[16]
PAUL J F. Assessment of intracardiac flows by Magnetic Resonance Imaging: the 4D Flow imaging[J]. Ann Cardiol Angeiol, 2020, 69(5): 273-275. DOI: 10.1016/j.ancard.2020.09.011.
[17]
RIBEYROLLES S, MONIN J L, ROHNEAN A, et al. Grading mitral regurgitation using 4D flow CMR: comparison to transthoracic echocardiography[J]. Echocardiography, 2022, 39(6): 783-793. DOI: 10.1111/echo.15364.
[18]
FIDOCK B, BARKER N, BALASUBRAMANIAN N, et al. A systematic review of 4D-flow MRI derived mitral regurgitation quantification methods[J/OL]. Front Cardiovasc Med, 2019, 6: 103 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/31428619/. DOI: 10.3389/fcvm.2019.00103.
[19]
SAFARKHANLO Y, JUNG B, BERNHARD B, et al. Mitral valve regurgitation assessed by intraventricular CMR 4D-flow: a systematic review on the technological aspects and potential clinical applications[J]. Int J Cardiovasc Imaging, 2023, 39(10): 1963-1977. DOI: 10.1007/s10554-023-02893-z.
[20]
URETSKY S, ANIMASHAUN I B, SAKUL S, et al. American society of echocardiography algorithm for degenerative mitral regurgitation: comparison with CMR[J]. JACC Cardiovasc Imaging, 2022, 15(5): 747-760. DOI: 10.1016/j.jcmg.2021.10.006.
[21]
CAVALCANTE J L, KUSUNOSE K, OBUCHOWSKI N A, et al. Prognostic impact of ischemic mitral regurgitation severity and myocardial infarct quantification by cardiovascular magnetic resonance[J]. JACC Cardiovasc Imaging, 2020, 13(7): 1489-1501. DOI: 10.1016/j.jcmg.2019.11.008.
[22]
GUPTA A N, AVERY R, SOULAT G, et al. Direct mitral regurgitation quantification in hypertrophic cardiomyopathy using 4D flow CMR jet tracking: evaluation in comparison to conventional CMR[J/OL]. J Cardiovasc Magn Reson, 2021, 23(1): 138 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/34865629/. DOI: 10.1186/s12968-021-00828-y.
[23]
ASHKIR Z, JOHNSON S, LEWANDOWSKI A J, et al. Novel insights into diminished cardiac reserve in non-obstructive hypertrophic cardiomyopathy from four-dimensional flow cardiac magnetic resonance component analysis[J]. Eur Heart J Cardiovasc Imaging, 2023, 24(9): 1192-1200. DOI: 10.1093/ehjci/jead074.
[24]
GORECKA M, BISSELL M M, HIGGINS D M, et al. Rationale and clinical applications of 4D flow cardiovascular magnetic resonance in assessment of valvular heart disease: a comprehensive review[J/OL]. J Cardiovasc Magn Reson, 2022, 24(1): 49 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/35989320/. DOI: 10.1186/s12968-022-00882-0.
[25]
GARG P, CRANDON S, SWOBODA P P, et al. Left ventricular blood flow kinetic energy after myocardial infarction - insights from 4D flow cardiovascular magnetic resonance[J/OL]. J Cardiovasc Magn Reson, 2018, 20(1): 61 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/30165869/. DOI: 10.1186/s12968-018-0483-6.
[26]
SVALBRING E, FREDRIKSSON A, ERIKSSON J, et al. Altered diastolic flow patterns and kinetic energy in subtle left ventricular remodeling and dysfunction detected by 4D flow MRI[J/OL]. PLoS One, 2016, 11(8): e0161391 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/27532640/. DOI: 10.1371/journal.pone.0161391.
[27]
DAS A, KELLY C, BEN-ARZI H, et al. Acute intra-cavity 4D flow cardiovascular magnetic resonance predicts long-term adverse remodelling following ST-elevation myocardial infarction[J/OL]. J Cardiovasc Magn Reson, 2022, 24(1): 64 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/36404326/. DOI: 10.1186/s12968-022-00889-7.
[28]
DEMIRKIRAN A, VAN DER GEEST R J, HOPMAN L H G A, et al. Association of left ventricular flow energetics with remodeling after myocardial infarction: new hemodynamic insights for left ventricular remodeling[J/OL]. Int J Cardiol, 2022, 367: 105-114 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/36007668/. DOI: 10.1016/j.ijcard.2022.08.040.
[29]
CONTIJOCH F J, HOROWITZ M, MASUTANI E, et al. 4D flow vorticity visualization predicts regions of quantitative flow inconsistency for optimal blood flow measurement[J/OL]. Radiol Cardiothorac Imaging, 2020, 2(1): e190054 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/32715299/. DOI: 10.1148/ryct.2020190054.
[30]
OLSEN F J, PEDERSEN S, GALATIUS S, et al. Association between regional longitudinal strain and left ventricular thrombus formation following acute myocardial infarction[J]. Int J Cardiovasc Imaging, 2020, 36(7): 1271-1281. DOI: 10.1007/s10554-020-01825-5.
[31]
GARG P, VAN DER GEEST R J, SWOBODA P P, et al. Left ventricular thrombus formation in myocardial infarction is associated with altered left ventricular blood flow energetics[J]. Eur Heart J Cardiovasc Imaging, 2019, 20(1): 108-117. DOI: 10.1093/ehjci/jey121.
[32]
BARKER N, ZAFAR H, FIDOCK B, et al. Age-associated changes in 4D flow CMR derived Tricuspid Valvular Flow and Right Ventricular Blood Flow Kinetic Energy[J/OL]. Sci Rep, 2020, 10(1): 9908 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/32555252/. DOI: 10.1038/s41598-020-66958-y.
[33]
ELBAZ M S, CALKOEN E E, WESTENBERG J J, et al. Vortex flow during early and late left ventricular filling in normal subjects: quantitative characterization using retrospectively-gated 4D flow cardiovascular magnetic resonance and three-dimensional Vortex core analysis[J/OL]. J Cardiovasc Magn Reson, 2014, 16(1): 78 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/25270083/. DOI: 10.1186/s12968-014-0078-9.
[34]
SUWA K, SAITOH T, TAKEHARA Y, et al. Characteristics of intra-left atrial flow dynamics and factors affecting formation of the vortex flow-analysis with phase-resolved 3-dimensional cine phase contrast magnetic resonance imaging[J]. Circ J, 2015, 79(1): 144-152. DOI: 10.1253/circj.CJ-14-0562.
[35]
SUWA K, SAITOH T, TAKEHARA Y, et al. Intra-left ventricular flow dynamics in patients with preserved and impaired left ventricular function: analysis with 3D cine phase contrast MRI (4D-Flow)[J]. J Magn Reson Imaging, 2016, 44(6): 1493-1503. DOI: 10.1002/jmri.25315.
[36]
SAKAKIBARA T, SUWA K, USHIO T, et al. Intra-left ventricular hemodynamics assessed with 4D flow magnetic resonance imaging in patients with left ventricular Thrombus[J]. Int Heart J, 2021, 62(6): 1287-1296. DOI: 10.1536/ihj.20-792.
[37]
BROWNING J R, HERTZBERG J R, SCHROEDER J D, et al. 4D flow assessment of vorticity in right ventricular diastolic dysfunction[J/OL]. Bioengineering, 2017, 4(2): 30 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/28952510/. DOI: 10.3390/bioengineering4020030.
[38]
HIRTLER D, GARCIA J, BARKER A J, et al. Assessment of intracardiac flow and vorticity in the right heart of patients after repair of tetralogy of Fallot by flow-sensitive 4D MRI[J]. Eur Radiol, 2016, 26(10): 3598-3607. DOI: 10.1007/s00330-015-4186-1.
[39]
BORHANI A, PORTER K K, UMAIR M, et al. Quantifying 4D flow cardiovascular magnetic resonance vortices in patients with pulmonary hypertension: a pilot study[J/OL]. Pulm Circ, 2023, 13(4): e12298 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/37859803/. DOI: 10.1002/pul2.12298.
[40]
SCHÄFER M, BARKER A J, MORGAN G J, et al. Increased systolic vorticity in the left ventricular outflow tract is associated with abnormal aortic flow formations in Tetralogy of Fallot[J]. Int J Cardiovasc Imaging, 2020, 36(4): 691-700. DOI: 10.1007/s10554-019-01764-w.
[41]
FENSTER B E, BROWNING J, SCHROEDER J D, et al. Vorticity is a marker of right ventricular diastolic dysfunction[J/OL]. Am J Physiol Heart Circ Physiol, 2015, 309(6): H1087-H1093 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/26254331/. DOI: 10.1152/ajpheart.00278.2015.
[42]
CAIN M T, SCHÄFER M, ROSS L K, et al. 4D-Flow MRI intracardiac flow analysis considering different subtypes of pulmonary hypertension[J/OL]. Pulm Circ, 2023, 13(4): e12307 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/37941938/. DOI: 10.1002/pul2.12307.
[43]
SCHÄFER M, HUMPHRIES S, STENMARK K R, et al. 4D-flow cardiac magnetic resonance-derived vorticity is sensitive marker of left ventricular diastolic dysfunction in patients with mild-to-moderate chronic obstructive pulmonary disease[J]. Eur Heart J Cardiovasc Imaging, 2018, 19(4): 415-424. DOI: 10.1093/ehjci/jex069.
[44]
SCHÄFER M, BROWNING J, SCHROEDER J D, et al. Vorticity is a marker of diastolic ventricular interdependency in pulmonary hypertension[J]. Pulm Circ, 2016, 6(1): 46-54. DOI: 10.1086/685052.
[45]
KAMPHUIS V P, WESTENBERG J J M, VAN DER PALEN R L F, et al. Scan-rescan reproducibility of diastolic left ventricular kinetic energy, viscous energy loss and vorticity assessment using 4D flow MRI: analysis in healthy subjects[J]. Int J Cardiovasc Imaging, 2018, 34(6): 905-920. DOI: 10.1007/s10554-017-1291-z.
[46]
KAMPHUIS V P, ROEST A A W, VAN DEN BOOGAARD P J, et al. Hemodynamic interplay of vorticity, viscous energy loss, and kinetic energy from 4D Flow MRI and link to cardiac function in healthy subjects and Fontan patients[J/OL]. Am J Physiol Heart Circ Physiol, 2021, 320(4): H1687-H1698 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/33635164/. DOI: 10.1152/ajpheart.00806.2020.
[47]
BARKER A J, VAN OOIJ P, BANDI K, et al. Viscous energy loss in the presence of abnormal aortic flow[J]. Magn Reson Med, 2014, 72(3): 620-628. DOI: 10.1002/mrm.24962.
[48]
ELBAZ M S M, VAN DER GEEST R J, CALKOEN E E, et al. 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[J]. Magn Reson Med, 2017, 77(2): 794-805. DOI: 10.1002/mrm.26129.
[49]
FILOMENA D, CIMINO S, MONOSILIO S, et al. Impact of intraventricular haemodynamic forces misalignment on left ventricular remodelling after myocardial infarction[J]. ESC Heart Fail, 2022, 9(1): 496-505. DOI: 10.1002/ehf2.13719.
[50]
POLA K, BERGSTRÖM E, TÖGER J, et al. Increased biventricular hemodynamic forces in precapillary pulmonary hypertension[J/OL]. Sci Rep, 2022, 12(1): 19933 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/36402861/. DOI: 10.1038/s41598-022-24267-6.
[51]
LOKE Y H, CAPUANO F, KOLLAR S, et al. Abnormal diastolic hemodynamic forces: a link between right ventricular wall motion, intracardiac flow, and pulmonary regurgitation in repaired tetralogy of fallot[J/OL]. Front Cardiovasc Med, 2022, 9: 929470 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/35911535/. DOI: 10.3389/fcvm.2022.929470.
[52]
POLA K, ROIJER A, BORGQUIST R, et al. Hemodynamic forces from 4D flow magnetic resonance imaging predict left ventricular remodeling following cardiac resynchronization therapy[J/OL]. J Cardiovasc Magn Reson, 2023, 25(1): 45 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/37620886/. DOI: 10.1186/s12968-023-00955-8.
[53]
PEDRIZZETTI G, ARVIDSSON P M, TÖGER J, et al. On estimating intraventricular hemodynamic forces from endocardial dynamics: a comparative study with 4D flow MRI[J/OL]. J Biomech, 2017, 60: 203-210 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/28711164/. DOI: 10.1016/j.jbiomech.2017.06.046.
[54]
BUONOCORE E, PAVLICEK W, MODIC M T, et al. Anatomic and functional imaging of congenital heart disease with digital subtraction angiography[J]. Radiology, 1983, 147(3): 647-654. DOI: 10.1148/radiology.147.3.6342029.
[55]
KOZUKA T, OHTA M. Evaluation of left ventricular function using digital subtraction angiography[J]. Jpn Circ J, 1985, 49(7): 710-718. DOI: 10.1253/jcj.49.710.
[56]
MEANEY T F, WEINSTEIN M A, BUONOCORE E, et al. Digital subtraction angiography of the human cardiovascular system[J]. AJR Am J Roentgenol, 1980, 135(6): 1153-1160. DOI: 10.2214/ajr.135.6.1153.
[57]
DA SILVEIRA J S, SMYKE M, RICH A V, et al. Quantification of aortic stenosis diagnostic parameters: comparison of fast 3 direction and 1 direction phase contrast CMR and transthoracic echocardiography[J/OL]. J Cardiovasc Magn Reson, 2017, 19(1): 35 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/28270219/. DOI: 10.1186/s12968-017-0339-5.
[58]
SACCO F, PAUN B, LEHMKUHL O, et al. Left ventricular trabeculations decrease the wall shear stress and increase the intra-ventricular pressure drop in CFD simulations[J/OL]. Front Physiol, 2018, 9: 458 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/29760665/. DOI: 10.3389/fphys.2018.00458.
[59]
IMANPARAST A, FATOURAEE N, SHARIF F. Comprehensive computational assessment of blood flow characteristics of left ventricle based on in-vivo MRI in presence of artificial myocardial infarction[J/OL]. Math Biosci, 2017, 294: 143-159 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/29080776/. DOI: 10.1016/j.mbs.2017.10.007.
[60]
NIU X Q, DUN Y T, LI G C, et al. Evaluation of left ventricular blood flow kinetic energy in patients with acute myocardial infarction by 4D Flow MRI: a preliminary study[J/OL]. BMC Med Imaging, 2024, 24(1): 131 [2024-06-28]. https://pubmed.ncbi.nlm.nih.gov/38840059/. DOI: 10.1186/s12880-024-01310-8.

PREV Value of multiparametric CMR in assessing subclinical myocardial injury in patients with multiple myeloma
NEXT Research progress in MRI evaluation of the therapeutic effect of ablation in hepatocellular carcinoma
  


LINK


Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn