Comparison of 4D Flow MRI to 2D Flow MRI in the pulmonary arteries in healthy volunteers and patients with pulmonary hypertension

Autoři: Malte Maria Sieren aff001;  Clara Berlin aff001;  Thekla Helene Oechtering aff001;  Peter Hunold aff001;  Daniel Drömann aff002;  Jörg Barkhausen aff001;  Alex Frydrychowicz aff001
Působiště autorů: Department of Radiology and Nuclear Medicine, University Hospital Schleswig-Holstein, Lübeck, Germany aff001;  Department of Pneumology, University Hospital Schleswig-Holstein, Lübeck, Germany aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224121



4D and 2D phase-contrast MRI (2D Flow MRI, 4D Flow MRI, respectively) are increasingly being used to noninvasively assess pulmonary hypertension (PH). The goals of this study were i) to evaluate whether established quantitative parameters in 2D Flow MRI associated with pulmonary hypertension can be assessed using 4D Flow MRI; ii) to compare results from 4D Flow MRI on a digital broadband 3T MR system with data from clinically established MRI-techniques as well as conservation of mass analysis and phantom correction and iii) to elaborate on the added value of secondary flow patterns in detecting PH.


11 patients with PH (4f, 63 ± 16y), 15 age-matched healthy volunteers (9f, 56 ± 11y), and 20 young healthy volunteers (13f, 23 ± 2y) were scanned on a 3T MR scanner (Philips Ingenia). Subjects were examined with a 4D Flow, a 2D Flow and a bSSFP sequence. For extrinsic comparison, quantitative parameters measured with 4D Flow MRI were compared to i) a static phantom, ii) 2D Flow acquisitions and iii) stroke volume derived from a bSSFP sequence. For intrinsic comparison conservation of mass-analysis was employed. Dedicated software was used to extract various flow, velocity, and anatomical parameters. Visualization of blood flow was performed to detect secondary flow patterns.


Overall, there was good agreement between all techniques, 4D Flow results revealed a considerable spread. Data improved after phantom correction. Both 4D and 2D Flow MRI revealed concordant results to differentiate patients from healthy individuals, especially based on values derived from anatomical parameters. The visualization of a vortex, indicating the presence of PH was achieved in 9 /11 patients and 2/35 volunteers.


This study confirms that quantitative parameters used for characterizing pulmonary hypertension can be gathered using 4D Flow MRI within clinically reasonable limits of agreement. Despite its unfavorable spatial and lesser temporal resolution and a non-neglible spread of results, the identification of diseased study participants was possible.

Klíčová slova:

Blood flow – Blood pressure – Data visualization – Diagnostic medicine – Hemodynamics – Magnetic resonance imaging – Pulmonary arteries – Pulmonary hypertension


1. Rich JD, Rich S. Clinical diagnosis of pulmonary hypertension. Circulation. 2014;130(20):1820–30. doi: 10.1161/CIRCULATIONAHA.114.006971 25385937

2. Galie N, Humbert M, Vachiery JL, Gibbs S, Lang I, Torbicki A, et al. 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: The Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Heart J. 2016;37(1):67–119. doi: 10.1093/eurheartj/ehv317 26320113

3. Alunni JP, Degano B, Arnaud C, Tetu L, Blot-Souletie N, Didier A, et al. Cardiac MRI in pulmonary artery hypertension: correlations between morphological and functional parameters and invasive measurements. Eur Radiol. 2010;20(5):1149–59. doi: 10.1007/s00330-009-1664-3 20094890

4. Roeleveld RJ, Marcus JT, Faes TJ, Gan TJ, Boonstra A, Postmus PE, et al. Interventricular septal configuration at mr imaging and pulmonary arterial pressure in pulmonary hypertension. Radiology. 2005;234(3):710–7. doi: 10.1148/radiol.2343040151 15634939

5. Sanz J, Dellegrottaglie S, Kariisa M, Sulica R, Poon M, O'Donnell TP, et al. Prevalence and correlates of septal delayed contrast enhancement in patients with pulmonary hypertension. Am J Cardiol. 2007;100(4):731–5. doi: 10.1016/j.amjcard.2007.03.094 17697838

6. Ley S, Mereles D, Risse F, Grunig E, Ley-Zaporozhan J, Tecer Z, et al. Quantitative 3D pulmonary MR-perfusion in patients with pulmonary arterial hypertension: correlation with invasive pressure measurements. Eur J Radiol. 2007;61(2):251–5. doi: 10.1016/j.ejrad.2006.08.028 17045440

7. Skrok J, Shehata ML, Mathai S, Girgis RE, Zaiman A, Mudd JO, et al. Pulmonary arterial hypertension: MR imaging-derived first-pass bolus kinetic parameters are biomarkers for pulmonary hemodynamics, cardiac function, and ventricular remodeling. Radiology. 2012;263(3):678–87. doi: 10.1148/radiol.12111001 22509050

8. Sanz J, Kariisa M, Dellegrottaglie S, Prat-Gonzalez S, Garcia MJ, Fuster V, et al. Evaluation of pulmonary artery stiffness in pulmonary hypertension with cardiac magnetic resonance. JACC Cardiovasc Imaging. 2009;2(3):286–95. doi: 10.1016/j.jcmg.2008.08.007 19356573

9. Sanz J, Kuschnir P, Rius T, Salguero R, Sulica R, Einstein A, et al. Pulmonary Arterial Hypertension: Noninvasive Detection with Phase-Contrast MR Imaging. Radiology. 2007;243(1):70–9. doi: 10.1148/radiol.2431060477 17329691

10. Swift AJ, Rajaram S, Hurdman J, Hill C, Davies C, Sproson TW, et al. Noninvasive estimation of PA pressure, flow, and resistance with CMR imaging: derivation and prospective validation study from the ASPIRE registry. JACC Cardiovasc Imaging. 2013;6(10):1036–47. doi: 10.1016/j.jcmg.2013.01.013 23769494

11. Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O. 4D flow MRI. J Magn Reson Imaging. 2012;36(5):1015–36. doi: 10.1002/jmri.23632 23090914

12. 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. doi: 10.1161/CIRCIMAGING.108.780247 19808511

13. Reiter U, Reiter G, Kovacs G, Stalder AF, Gulsun MA, Greiser A, et al. Evaluation of elevated mean pulmonary arterial pressure based on magnetic resonance 4D velocity mapping: comparison of visualization techniques. PLoS One. 2013;8(12):e82212. doi: 10.1371/journal.pone.0082212 24349224

14. Reiter G, Reiter U, Kovacs G, Olschewski H, Fuchsjager M. Blood flow vortices along the main pulmonary artery measured with MR imaging for diagnosis of pulmonary hypertension. Radiology. 2015;275(1):71–9. doi: 10.1148/radiol.14140849 25372980

15. Barker AJ, Roldan-Alzate A, Entezari P, Shah SJ, Chesler NC, Wieben O, et al. Four-dimensional flow assessment of pulmonary artery flow and wall shear stress in adult pulmonary arterial hypertension: results from two institutions. Magn Reson Med. 2015;73(5):1904–13. doi: 10.1002/mrm.25326 24974951

16. 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. doi: 10.1186/1532-429X-12-5 20074359

17. Simonneau G, Gatzoulis MA, Adatia I, Celermajer D, Denton C, Ghofrani A, et al. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol. 2013;62(25 Suppl):D34–41. doi: 10.1016/j.jacc.2013.10.029 24355639

18. Chernobelsky A, Shubayev O, Comeau CR, Wolff SD. Baseline correction of phase contrast images improves quantification of blood flow in the great vessels. J Cardiovasc Magn Reson. 2007;9(4):681–5. doi: 10.1080/10976640601187588 17578724

19. 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. doi: 10.1002/mrm.22199 20024953

20. Dyverfeldt P, Bissell M, Barker AJ, Bolger AF, Carlhall CJ, Ebbers T, et al. 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson. 2015;17:72. doi: 10.1186/s12968-015-0174-5 26257141

21. Alfakih K, Plein S, Thiele H, Jones T, Ridgway JP, Sivananthan MU. Normal human left and right ventricular dimensions for MRI as assessed by turbo gradient echo and steady-state free precession imaging sequences. J Magn Reson Imaging. 2003;17(3):323–9. doi: 10.1002/jmri.10262 12594722

22. Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M. Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med. 2008;60(5):1218–31. doi: 10.1002/mrm.21778 18956416

23. 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. doi: 10.1097/RLI.0b013e31829a4f2f 23857136

24. Caro CG, Pedly TJ, Schroter RC, Seed WA. The Mechanics of the Circulation. Cambridge University Press; 2012. p. 229–31.

25. Bland Altman. Statistical methods for assessing agreement between two methods of clinical measurment. Lancet. 1986;1(1):307–10.

26. Koo TK, Li MY. A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research. J Chiropr Med. 2016;15(2):155–63. doi: 10.1016/j.jcm.2016.02.012 27330520

27. Jarvis K, Vonder M, Barker AJ, Schnell S, Rose M, Carr J, et al. 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. 2016;18(1):59. doi: 10.1186/s12968-016-0276-8 27659876

28. Bollache E, van Ooij P, Powell A, Carr J, Markl M, Barker AJ. Comparison of 4D flow and 2D velocity-encoded phase contrast MRI sequences for the evaluation of aortic hemodynamics. Int J Cardiovasc Imaging. 2016.

29. Gabbour M, Schnell S, Jarvis K, Robinson JD, Markl M, Rigsby CK. 4-D flow magnetic resonance imaging: blood flow quantification compared to 2-D phase-contrast magnetic resonance imaging and Doppler echocardiography. Pediatr Radiol. 2015;45(6):804–13. doi: 10.1007/s00247-014-3246-z 25487721

30. Carlsson M, Toger J, Kanski M, Bloch KM, Stahlberg 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;13:55. doi: 10.1186/1532-429X-13-55 21970399

31. 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. doi: 10.1002/jmri.22280 20815066

32. 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. doi: 10.1186/1532-429X-11-3 19232119

33. Sakuma H, Kawada N, Kubo H, Nishide Y, Takano K, Kato N, et al. Effect of breath holding on blood flow measurement using fast velocity encoded cine MRI. Magn Reson Med. 2001;45(2):346–8. doi: 10.1002/1522-2594(200102)45:2<346::aid-mrm1044>;2-i 11180443

34. Giese D, Haeberlin M, Barmet C, Pruessmann KP, Schaeffter T, Kozerke S. Analysis and correction of background velocity offsets in phase-contrast flow measurements using magnetic field monitoring. Magn Reson Med. 2012;67(5):1294–302. doi: 10.1002/mrm.23111 21826731

35. Lankhaar JW, Hofman MB, Marcus JT, Zwanenburg JJ, Faes TJ, Vonk-Noordegraaf A. Correction of phase offset errors in main pulmonary artery flow quantification. J Magn Reson Imaging. 2005;22(1):73–9. doi: 10.1002/jmri.20361 15971181

36. Zhang T, Chowdhury S, Lustig M, Barth RA, Alley MT, Grafendorfer T, et al. Clinical performance of contrast enhanced abdominal pediatric MRI with fast combined parallel imaging compressed sensing reconstruction. J Magn Reson Imaging. 2014;40(1):13–25. doi: 10.1002/jmri.24333 24127123

37. Tariq U, Hsiao A, Alley M, Zhang T, Lustig M, Vasanawala SS. Venous and arterial flow quantification are equally accurate and precise with parallel imaging compressed sensing 4D phase contrast MRI. J Magn Reson Imaging. 2013;37(6):1419–26. doi: 10.1002/jmri.23936 23172846

38. Han QJ, Witschey WR, Fang-Yen CM, Arkles JS, Barker AJ, Forfia PR, et al. 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(9):e0138365. doi: 10.1371/journal.pone.0138365 26418553

39. Odagiri K, Inui N, Hakamata A, Inoue Y, Suda T, Takehara Y, et al. Non-invasive evaluation of pulmonary arterial blood flow and wall shear stress in pulmonary arterial hypertension with 3D phase contrast magnetic resonance imaging. Springerplus. 2016;5(1):1071. doi: 10.1186/s40064-016-2755-7 27462519

40. Schafer M, Kheyfets VO, Schroeder JD, Dunning J, Shandas R, Buckner JK, et al. Main pulmonary arterial wall shear stress correlates with invasive hemodynamics and stiffness in pulmonary hypertension. Pulm Circ. 2016;6(1):37–45. doi: 10.1086/685024 27076906

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