Clinical applications of intra-cardiac four-dimensional flow cardiovascular magnetic resonance: A systematic review

Saul Crandon, Mohammed S M Elbaz, Jos J M Westenberg, Rob J van der Geest, Sven Plein, Pankaj Garg, Saul Crandon, Mohammed S M Elbaz, Jos J M Westenberg, Rob J van der Geest, Sven Plein, Pankaj Garg

Abstract

Background: Four-dimensional flow cardiovascular magnetic resonance (4D flow CMR) is an emerging non-invasive imaging technology used to visualise and quantify intra-cardiac blood flow. The aim of this systematic review is to assess the literature on the current clinical applications of intra-cardiac 4D flow CMR.

Methods: A systematic review was conducted to evaluate the literature on the intra-cardiac clinical applications of 4D flow CMR. Structured searches were carried out on Medline, EMBASE and the Cochrane Library in October 2016. A modified Critical Skills Appraisal Programme (CASP) tool was used to objectively assess and score the included studies. Studies were categorised as 'highly clinically applicable' for scores of 67-100%, 'potentially clinically applicable' for 34-66% and 'less clinically applicable' for 0-33%.

Results: Of the 1608 articles screened, 44 studies met eligibility for systematic review. The included literature consisted of 22 (50%) mechanistic studies, 18 (40.9%) pilot studies and 4 (9.1%) diagnostic studies. Based on the modified CASP tool, 27 (62%) studies were 'highly clinically applicable', 9 (20%) were 'potentially clinically applicable' and 8 (18%) were 'less clinically applicable'.

Conclusions: There are many proposed methods for using 4D flow CMR to quantify intra-cardiac flow. The evidence base is mainly mechanistic, featuring single-centred designs. Larger, multi-centre studies are required to validate the proposed techniques and investigate the clinical advantages that 4D flow CMR offers over standard practices. PROSPERO=CRD42016051438.

Keywords: 4D flow CMR; 4D flow MRI; Cardiovascular magnetic resonance; Four-dimensional; Intra-cardiac; Systematic review.

Copyright © 2017 The Authors. Published by Elsevier B.V. All rights reserved.

Figures

Fig. 1
Fig. 1
Overview of study selection process. Panel A = Article screening algorithm. Two reviewers independently screened the titles and abstracts of 936 studies using this system. The number of studies excluded at each stage is shown. Panel B = Flow diagram used for identifying the included studies. The full-texts of the 73 studies that were identified from the screening process were assessed. Of these, 4 (5.5%) were excluded as being irrelevant to the systematic review. The remaining 69 studies underwent citation tracking through the OvidSP databases, as well as manual reference searching. This process identified a further 4 relevant studies for inclusion. Of the final 73 studies included, 44 (60.3%) were full studies, whereas 29 (39.7%) were abstracts only. Flow diagram adapted from Moher et al. . Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLOS Medicine 2009. 6 (7):e1000097. The PRISMA Statement is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium.
Fig. 2
Fig. 2
Graphical representations of the percentage of clinical applicability against various study design factors, Panel A = against study type, Panel B = against study year, Panel C = against the 4D flow methods used and Panel D = against intra-cardiac structure. KE = kinetic energy, TKE = turbulent kinetic energy, Haem forces = haemodynamic forces, RVT = retrospective valve tracking, JSLD = jet shear layer detection method, VT = volume tracking, RV = regurgitant volume, LA = left atrium, LV = left ventricle, MV = mitral valve, AV = aortic valve, TV = tricuspid valve, PV = pulmonary valve, RA = right atrium, RV = right ventricle.
Fig. 3
Fig. 3
4D flow streamline visualisation and retrospective valve tracking quantification. Panels A and B = Four-dimensional mitral inflow in a patient with mitral regurgitation. Panel A shows the mitral regurgitation (yellow arrow) as well as tricuspid regurgitation (red arrow). Panel B = Mitral valve inflow quantification using retrospective valve-tracking. Panels C and D = Four-dimensional aortic flow in a patient with aortic root dilatation. Panel C shows pathological vortex formation in the ascending aorta (red arrow) as well as aortic regurgitation (yellow arrow). Panel D = Aortic valve flow quantification using retrospective valve-tracking.

References

    1. World Health Organisation Cardiovascular disease. (Fact sheet no. 317) 2017. Retrieved from.
    1. Dyverfeldt P., Bissell M., Barker A.J., Bolger A.F., Carlhall C.J., Ebbers T., Francios C.J., Frydrychowicz A., Geiger J., Giese D., Hope M.D., Kilner P.J., Kozerke S., Myerson S., Neubauer S., Wieben O., Markl M. 4D flow cardiovascular magnetic resonance consensus statement. J. Cardiovasc. Magn. Reson. 2015;17:72.
    1. Bax J.J., Delgado V. Advanced imaging in valvular heart disease. Nat. Rev. Cardiol. 2017;14:209–223.
    1. Markl M., Frydrychowicz A., Kozerke S., Hope M., Wieben O. 4D flow MRI. J. Magn. Reson. Imaging. 2012;36:1015–1036.
    1. Stankovic Z., Allen B.D., Garcia J., Jarvis K.B., Markl M. 4D flow imaging with MRI. Cardiovasc. Diagn. Ther. 2014;4:173–192.
    1. Ebbers T. Flow imaging: cardiac applications of 3D cine phase-contrast MRI. Curr. Cardiovasc. Imaging Rep. 2011;4:127–133.
    1. Markl M., Kilner P.J., Ebbers T. Comprehensive 4D velocity mapping of the heart and great vessels by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2011;13:7.
    1. Coffey S., Cairns B.J., Iung B. The modern epidemiology of heart valve disease. Heart. 2015
    1. Roger V.L. Epidemiology of heart failure. Circ. Res. 2013;113:646–659.
    1. Crandon S., Garg P., Elbaz M.S., Plein S. 2016. Intra-cardiac clinical applications of 4D flow MRI (four-dimensional magnetic resonance imaging) review protocol.
    1. Moher D., Liberati A., Tetzlaff J., Altman D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6
    1. Lee D.C., Markl M., Ng J., Carr M., Benefield B., Carr J.C., Goldberger J.J. Three-dimensional left atrial blood flow characteristics in patients with atrial fibrillation assessed by 4D flow CMR. Eur. Heart J. Cardiovasc. Imaging. 2016;17:1259–1268.
    1. Markl M., Carr M., Ng J., Lee D.C., Jarvis K., Carr J., Goldberger J.J. Assessment of left and right atrial 3D hemodynamics in patients with atrial fibrillation: a 4D flow MRI study. Int. J. Cardiovasc. Imaging. 2016;32:807–815.
    1. Markl M., Lee D.C., Ng J., Carr M., Carr J., Goldberger J.J. Left atrial 4-dimensional flow magnetic resonance imaging stasis and velocity mapping in patients with atrial fibrillation. Investig. Radiol. 2016;51:147–154.
    1. Markl M., Lee D.C., Furiasse N., Carr M., Foucar C., Ng J., Carr J., Goldberger J.J. Left atrial and left atrial appendage 4D blood flow dynamics in atrial fibrillation. Circ. Cardiovasc. Imaging. 2016;9(9):e004984.
    1. Steding-Ehrenborg K., Arvidsson P.M., Toger J., Rydberg M., Heiberg E., Carlsson M., Arheden H. Determinants of kinetic energy of blood flow in the four-chambered heart in athletes and sedentary controls. Am. J. Physiol. Heart Circ. Physiol. 2016;310:H113–22.
    1. Suwa K., Saitoh T., Takehara Y., Sano M., Nobuhara M., Saotome M., Urushida T., Katoh H., Satoh H., Sugiyama M., Wakayama T., Alley M., Sakahara H., Hayashi H. 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. Circ. J. 2015;79:144–152.
    1. Arvidsson P.M., Toger J., Heiberg E., Carlsson M., Arheden H. Quantification of left and right atrial kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. J. Appl. Physiol. 2013;114:1472–1481.
    1. Fluckiger J.U., Goldberger J.J., Lee D.C., Ng J., Lee R., Goyal A., Markl M. Left atrial flow velocity distribution and flow coherence using four-dimensional FLOW MRI: a pilot study investigating the impact of age and pre- and postintervention atrial fibrillation on atrial hemodynamics. J. Magn. Reson. Imaging. 2013;38:580–587.
    1. Foll D., Taeger S., Bode C., Jung B., Markl M. Age, gender, blood pressure, and ventricular geometry influence normal 3D blood flow characteristics in the left heart. Eur. Heart J. Cardiovasc. Imaging. 2013;14:366–373.
    1. Dyverfeldt P., Kvitting J.P., Carlhall C.J., Boano G., Sigfridsson A., Hermansson U., Bolger A.F., Engvall J., Ebbers T. Hemodynamic aspects of mitral regurgitation assessed by generalized phase-contrast MRI. J. Magn. Reson. Imaging. 2011;33:582–588.
    1. Fyrenius A., Wigstrom L., Ebbers T., Karlsson M., Engvall J., Bolger A. Three dimensional flow in the human left atrium. Heart. 2001;86:448–455.
    1. Eriksson J., Bolger A.F., Ebbers T., Carlhall C.J. Assessment of left ventricular hemodynamic forces in healthy subjects and patients with dilated cardiomyopathy using 4D flow MRI. Physiol. Rep. 2016;4(3)
    1. Suwa K., Saitoh T., Takehara Y., Sano M., Saotome M., Urushida T., Katoh H., Satoh H., Sugiyama M., Wakayama T., Alley M., Sakahara H., Hayashi H. Intra-left ventricular flow dynamics in patients with preserved and impaired left ventricular function: analysis with 3D cine phase contrast MRI (4D-flow) J. Magn. Reson. Imaging. 2016;44(6):1493–1503.
    1. Svalbring E., Fredriksson A., Eriksson J., Dyverfeldt P., Ebbers T., Bolger A.F., Engvall J., Carlhäll C.J. Altered diastolic flow patterns and kinetic energy in subtle left ventricular remodeling and dysfunction detected by 4D flow MRI. PLoS One. 2016;11(8):e0161391.
    1. Van Ooij P., Allen B.D., Contaldi C., Garcia J., Collins J., Carr J., Choudhury L., Bonow R.O., Barker A.J., Markl M. 4D flow MRI and T1-mapping: assessment of altered cardiac hemodynamics and extracellular volume fraction in hypertrophic cardiomyopathy. J. Magn. Reson. Imaging. 2016;43:107–114.
    1. Wong J., Chabiniok R., deVecchi A., Dedieu N., Sammut E., Schaeffter T., Razavi R. Age-related changes in intraventricular kinetic energy: a physiological or pathological adaptation? Am. J. Physiol. Heart Circ. Physiol. 2016;310:H747–55.
    1. Al-Wakeel N., Fernandes J.F., Amiri A., Siniawski H., Goubergrits L., Berger F., Kuehne T. Hemodynamic and energetic aspects of the left ventricle in patients with mitral regurgitation before and after mitral valve surgery. J. Magn. Reson. Imaging. 2015;42:1705–1712.
    1. Eriksson J., Bolger A.F., Carlhall C.J., Ebbers T. Spatial heterogeneity of four-dimensional relative pressure fields in the human left ventricle. Magn. Reson. Med. 2015;74:1716–1725.
    1. Kanski M., Arvidsson P.M., Toger J., Borgquist R., Heiberg E., Carlsson M., Arheden H. Left ventricular fluid kinetic energy time curves in heart failure from cardiovascular magnetic resonance 4D flow data. J. Cardiovasc. Magn. Reson. 2015;17:111.
    1. Kanski M., Toger J., Steding-Ehrenborg K., Xanthis C., Bloch K.M., Heiberg E., Carlsson M., Arheden H. Whole-heart four-dimensional flow can be acquired with preserved quality without respiratory gating, facilitating clinical use: a head-to-head comparison. BMC Med. Imaging. 2015;15:20.
    1. Zajac J., Eriksson J., Dyverfeldt P., Bolger A.F., Ebbers T., Carlhall C.J. Turbulent kinetic energy in normal and myopathic left ventricles. J. Magn. Reson. Imaging. 2015;41:1021–1029.
    1. Elbaz M.S., Calkoen E.E., Westenberg J.J., Lelieveldt B.P., Roest A.A., van der Geest R.J. 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. Cardiovasc. Magn. Reson. 2014;16:78.
    1. Eriksson J., Bolger A.F., Ebbers T., Carlhall C.J. Four-dimensional blood flow-specific markers of LV dysfunction in dilated cardiomyopathy. Eur. Heart J. Cardiovasc. Imaging. 2013;14:417–424.
    1. Carlsson M., Heiberg E., Toger J., Arheden H. Quantification of left and right ventricular kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. Am. J. Physiol. Heart Circ. Physiol. 2012;302:H893–900.
    1. Toger J., Kanski M., Carlsson M., Kovacs S.J., Soderlind G., Arheden H., Heiberg E. Vortex ring formation in the left ventricle of the heart: analysis by 4D flow MRI and Lagrangian coherent structures. Ann. Biomed. Eng. 2012;40:2652–2662.
    1. Brandts A., Bertini M., van Dijk E.J., Delgado V., Marsan N.A., van der Geest R.J., Siebelink H.M., de Roos A., Bax J.J., Westenberg J.J. Left ventricular diastolic function assessment from three-dimensional three-directional velocity-encoded MRI with retrospective valve tracking. J. Magn. Reson. Imaging. 2011;33:312–319.
    1. Eriksson J., Dyverfeldt P., Engvall J., Bolger A.F., Ebbers T., Carlhall C.J. Quantification of presystolic blood flow organization and energetics in the human left ventricle. Am. J. Physiol. Heart Circ. Physiol. 2011;300:H2135–H2141.
    1. Kumar R., Charonko J., Hundley W.G., Hamilton C.A., Stewart K.C., McNeal G.R., Vlachos P.P., Little W.C. Assessment of left ventricular diastolic function using 4-dimensional phase-contrast cardiac magnetic resonance. J. Comput. Assist. Tomogr. 2011;35:108–112.
    1. 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.
    1. Eriksson J., Carlhall C.J., Dyverfeldt P., Engvall J., Bolger A.F., Ebbers T. Semi-automatic quantification of 4D left ventricular blood flow. J. Cardiovasc. Magn. Reson. 2010;12:9.
    1. Bolger A.F., Heiberg E., Karlsson M., Wigstrom L., Engvall J., Sigfridsson A., Ebbers T., Kvitting J.P., Carlhall C.J., Wranne B. Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2007;9:741–747.
    1. Ebbers T., Wigstrom L., Bolger A.F., Wranne B., Karlsson M. Noninvasive measurement of time-varying three-dimensional relative pressure fields within the human heart. J. Biomech. Eng. 2002;124:288–293.
    1. Kim W.Y., Walker P.G., Pedersen E.M., Poulsen J.K., Oyre S., Houlind K., Yoganathan A.P. Left ventricular blood flow patterns in normal subjects: a quantitative analysis by three-dimensional magnetic resonance velocity mapping. J. Am. Coll. Cardiol. 1995;26:224–238.
    1. Marsan N.A., Westenberg J.J., Ypenburg C., Delgado V., van Bommel R.J., Roes S.D., Nucifora G., van der Geest R.J., de Roos A., Reiber J.C., Schalij M.J., Bax J.J. Quantification of functional mitral regurgitation by real-time 3D echocardiography: comparison with 3D velocity-encoded cardiac magnetic resonance. J. Am. Coll. Cardiol. Img. 2009;2:1245–1252.
    1. Roes S.D., Hammer S., van der Geest R.J., Marsan N.A., Bax J.J., Lamb H.J., Reiber J.H., de Roos A., Westenberg J.J. 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. Investig. Radiol. 2009;44:669–675.
    1. Westenberg J.J., Roes S.D., Ajmone Marsan N., Binnendijk N.M., Doornbos J., Bax J.J., Reiber J.H., de Roos A., van der Geest R.J. Mitral valve and tricuspid valve blood flow: accurate quantification with 3D velocity-encoded MR imaging with retrospective valve tracking. Radiology. 2008;249:792–800.
    1. Westenberg J.J., Doornbos J., Versteegh M.I., Bax J.J., van der Geest R.J., de Roos A., Dion R.A., Reiber J.H. Accurate quantitation of regurgitant volume with MRI in patients selected for mitral valve repair. Eur. J. Cardiothorac. Surg. 2005;27:462–466. (discussion 467)
    1. Westenberg J.J., Danilouchkine M.G., Doornbos J., Bax J.J., van der Geest R.J., Labadie G., Lamb H.J., Versteegh M.I., de Roos A., Reiber J.H. Accurate and reproducible mitral valvular blood flow measurement with three-directional velocity-encoded magnetic resonance imaging. J. Cardiovasc. Magn. Reson. 2004;6:767–776.
    1. Chelu R.G., van den Bosch A.E., van Kranenburg M., Hsiao A., van den Hoven A.T., Ouhlous M., Budde R.P.J., Beniest K.M., Swart L.E., Coenen A., Lubbers M.M., Wielopolski P.A., Vasanawala S.S., Roos-Hesselink J.W., Nieman K. Qualitative grading of aortic regurgitation: a pilot study comparing CMR 4D flow and echocardiography. Int. J. Cardiovasc. Imaging. 2016;32:301–307.
    1. Garcia J., Markl M., Schnell S., Allen B., Entezari P., Mahadevia R., Chris Malaisrie S., Pibarot P., Carr J., Barker A.J. Evaluation of aortic stenosis severity using 4D flow jet shear layer detection for the measurement of valve effective orifice area. Magn. Reson. Imaging. 2014;32:891–898.
    1. Ewe S.H., Delgado V., van der Geest R., Westenberg J.J., Haeck M.L., Witkowski T.G., Auger D., Marsan N.A., Holman E.R., de Roos A., Schalij M.J., Bax J.J., Sieders A., Siebelink H.M. Accuracy of three-dimensional versus two-dimensional echocardiography for quantification of aortic regurgitation and validation by three-dimensional three-directional velocity-encoded magnetic resonance imaging. Am. J. Cardiol. 2013;112:560–566.
    1. Callaghan F.M., Arnott C., Figtree G.A., Kutty S., Celermajer D.S., Grieve S.M. Quantifying right atrial filling and emptying: a 4D-flow MRI study. J. Magn. Reson. Imaging. 2016
    1. Han Q.J., Witschey W.R., Fang-Yen C.M., Arkles J.S., Barker A.J., Forfia P.R., Han Y. Altered right ventricular kinetic energy work density and viscous energy dissipation in patients with pulmonary arterial hypertension: a pilot study using 4D flow MRI. PLoS One. 2015;10 ([Electronic Resource])
    1. Fredriksson A.G., Zajac J., Eriksson J., Dyverfeldt P., Bolger A.F., Ebbers T., Carlhall C.J. 4-D blood flow in the human right ventricle. Am. J. Physiol. Heart Circ. Physiol. 2011;301:H2344–50.
    1. Iung B., Baron G., Tornos P., Gohlke-Bärwolf C., Butchart E.G., Vahanian A. Valvular heart disease in the community: a European experience. Curr. Probl. Cardiol. 2007;32:609–661.

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