Download PDF
Rofo 2021; 193(04): 388-398
DOI: 10.1055/a-1271-7405
Review

Abdominal Applications of 4D Flow MRI

Abdominelle Anwendungen der 4D-Fluss-MRT
Christoph Riedel
1   Department of Diagnostic and Interventional Radiology and Nuclear Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Alexander Lenz
1   Department of Diagnostic and Interventional Radiology and Nuclear Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Lutz Fischer
2   Department of Visceral Transplantation, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Jun Li
2   Department of Visceral Transplantation, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
3   Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Feilix Piecha
4   I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Johannes Kluwe
4   I. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Gerhard Adam
1   Department of Diagnostic and Interventional Radiology and Nuclear Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Peter Bannas
1   Department of Diagnostic and Interventional Radiology and Nuclear Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
› Author AffiliationsSupported by: Deutsche Stiftung für Herzforschung F/35/17
Supported by: Forschungszentrum Medizintechnik Hamburg 04fmthh2019
› Further Information
Also available at
   Permissions and Reprints

Abstract

Background Four-dimensional flow magnetic resonance imaging (4D flow MRI) provides volumetric and time-resolved visualization and quantification of blood flow. This review presents an overview of possible applications of 4D flow MRI for non-invasive assessment of abdominal hemodynamics.

Method This review is based on the authors’ experience and the current literature. A PubMed database literature research was performed in December 2019 focusing on abdominal applications of 4D flow MRI. We illustrated the review with exemplary figures and movies of clinical cases from our institution.

Results and Conclusion 4D flow MRI offers the possibility of comprehensive assessment of abdominal blood flows in different vascular territories and organ systems. Results of recent studies indicate that 4D flow MRI improves understanding of altered hemodynamics in patients with abdominal disease and may be useful for monitoring therapeutic response. Future studies with larger cohorts aiming to integrate 4D flow MRI in the clinical routine setting are needed.

Key Points: 

  • 4D flow MRI enables comprehensive visualization of the complex abdominal vasculature

  • 4D flow MRI enables quantification of abdominal blood flow velocities and flow rates

  • 4D flow MRI may enable deeper understanding of altered hemodynamics in abdominal disease

  • Further validation studies are needed prior to broad distribution of abdominal 4D flow MRI

Citation Format

  • Riedel C, Lenz A, Fischer L et al. Abdominal Applications of 4D Flow MRI. Fortschr Röntgenstr 2021; 193: 388 – 398

Zusammenfassung

Hintergrund Die 4-dimensionale Fluss-Magnetresonanztomografie (4D-Fluss-MRT) erlaubt die zeitaufgelöste Darstellung und Quantifizierung des Blutflusses. Diese Übersichtsarbeit stellt die möglichen Anwendungen der 4D-Fluss-MRT zur nichtinvasiven Bildgebung der Hämodynamik im Abdomen zusammen.

Methode Diese Übersichtsarbeit basiert auf der Erfahrung der Autoren sowie einer aktuellen Literaturrecherche. Die Literaturrecherche wurde in der PubMed-Datenbank bezüglich abdomineller Anwendungen der 4D-Fluss-MRT im Dezember 2019 durchgeführt. Wir haben die Arbeit mit Abbildungen und Filmen klinischer Fälle aus unserer Institution illustriert.

Ergebnisse und Schlussfolgerung Die 4D-Fluss-MRT erlaubt die umfassende Beurteilung des abdominellen Blutflusses in verschiedenen Organsystemen und Gefäßterritorien. Die Ergebnisse neuerer Studien zeigen, dass die 4D-Fluss-MRT ein besseres Verständnis der veränderten Hämodynamik bei Patienten mit abdominellen Erkrankungen sowie die Überwachung des therapeutischen Ansprechens ermöglicht. Zukünftige Studien in größeren Kohorten sind nötig, um die 4D-Fluss-MRT in den klinischen Alltag zu integrieren.

Kernaussagen: 

  • Die 4D-Fluss-MRT ermöglicht eine umfassende Visualisierung der komplexen abdominellen Gefäßanatomie.

  • Die 4D-Fluss-MRT ermöglicht die Quantifizierung der Geschwindigkeiten und der Flussraten in abdominellen Blutgefäßen.

  • Die 4D-Fluss-MRT könnte zu einem besseren Verständnis der veränderten Hämodynamik bei unterschiedlichen abdominellen Erkrankungen beitragen.

  • Weitere Studien zur Validierung der 4D-Fluss-MRT in der abdominellen Bildgebung sind vor der breiten Anwendung notwendig.

Key words

MRI - phase contrast MRI - 4D flow MRI - flow imaging - abdominal hemodynamics


Publication History

Received: 17 March 2020

Accepted: 09 September 2020

Article published online:
02 December 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Strater A, Huber A, Rudolph J. et al 4D-Flow MRI: Technique and Applications. Rofo 2018; 190: 1025-1035 . doi:10.1055/a-0647-2021
    Article in Thieme ConnectPubMedGoogle Scholar
  • 2 Roldan-Alzate A, Francois CJ, Wieben O. et al Emerging Applications of Abdominal 4D Flow MRI. Am J Roentgenol 2016; 207: 58-66 . doi:10.2214/Am J Roentgenol.15.15995
    CrossrefPubMedGoogle Scholar
  • 3 Weinrich JM, Lenz A, Girdauskas E. et al Current and Emerging Imaging Techniques in Patients with Genetic Aortic Syndromes. Rofo 2020; 192: 50-58 . doi:10.1055/a-0914-3321
    Article in Thieme ConnectPubMedGoogle Scholar
  • 4 Dyverfeldt P, Bissell M, Barker AJ. et al 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson 2015; 17: 72 . doi:10.1186/s12968-015-0174-5
    CrossrefPubMedGoogle Scholar
  • 5 Lenz A, Petersen J, Riedel C. et al 4D flow cardiovascular magnetic resonance for monitoring of aortic valve repair in bicuspid aortic valve disease. J Cardiovasc Magn Reson 2020; 22: 29 . doi:10.1186/s12968-020-00608-0
    CrossrefPubMedGoogle Scholar
  • 6 Feneis JF, Kyubwa E, Atianzar K. et al 4D flow MRI quantification of mitral and tricuspid regurgitation: Reproducibility and consistency relative to conventional MRI. J Magn Reson Imaging 2018; 48: 1147-1158 . doi:10.1002/jmri.26040
    CrossrefPubMedGoogle Scholar
  • 7 Schoennagel BP, Yamamura J, Kording F. et al Fetal dynamic phase-contrast MR angiography using ultrasound gating and comparison with Doppler ultrasound measurements. Eur Radiol 2019; 29: 4169-4176 . doi:10.1007/s00330-018-5940-y
    CrossrefPubMedGoogle Scholar
  • 8 Stankovic Z. Four-dimensional flow magnetic resonance imaging in cirrhosis. World J Gastroenterol 2016; 22: 89-102 . doi:10.3748/wjg.v22.i1.89
    CrossrefPubMedGoogle Scholar
  • 9 Putz FJ, Verloh N, Erlmeier A. et al Influence of limited examination conditions on contrast-enhanced sonography for characterising liver lesions. Clin Hemorheol Microcirc 2019; 71: 267-276 . doi:10.3233/CH-189417
    CrossrefPubMedGoogle Scholar
  • 10 Sabba C, Merkel C, Zoli M. et al Interobserver and interequipment variability of echo-Doppler examination of the portal vein: effect of a cooperative training program. Hepatology 1995; 21: 428-433 . doi:10.1002/hep.1840210225
    PubMedGoogle Scholar
  • 11 Wentland AL, Grist TM, Wieben O. Repeatability and internal consistency of abdominal 2D and 4D phase contrast MR flow measurements. Acad Radiol 2013; 20: 699-704 . doi:10.1016/j.acra.2012.12.019
    CrossrefPubMedGoogle Scholar
  • 12 Frydrychowicz A, Roldan-Alzate A, Winslow E. et al Comparison of radial 4D Flow-MRI with perivascular ultrasound to quantify blood flow in the abdomen and introduction of a porcine model of pre-hepatic portal hypertension. Eur Radiol 2017; 27: 5316-5324 . doi:10.1007/s00330-017-4862-4
    CrossrefPubMedGoogle Scholar
  • 13 Azarine A, Garcon P, Stansal A. et al Four-dimensional Flow MRI: Principles and Cardiovascular Applications. Radiographics 2019; 39: 632-648 . doi:10.1148/rg.2019180091
    CrossrefPubMedGoogle Scholar
  • 14 Nett EJ, Johnson KM, Frydrychowicz A. et al Four-dimensional phase contrast MRI with accelerated dual velocity encoding. J Magn Reson Imaging 2012; 35: 1462-1471 . doi:10.1002/jmri.23588
    CrossrefPubMedGoogle Scholar
  • 15 Stankovic Z, Jung B, Collins J. et al Reproducibility study of four-dimensional flow MRI of arterial and portal venous liver hemodynamics: influence of spatio-temporal resolution. Magn Reson Med 2014; 72: 477-484 . doi:10.1002/mrm.24939
    CrossrefPubMedGoogle Scholar
  • 16 Dyverfeldt P, Ebbers T. Comparison of respiratory motion suppression techniques for 4D flow MRI. Magn Reson Med 2017; 78: 1877-1882 . doi:10.1002/mrm.26574
    CrossrefPubMedGoogle Scholar
  • 17 Markl M, Harloff A, Bley TA. 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: 824-831 . doi:10.1002/jmri.20871
    CrossrefPubMedGoogle Scholar
  • 18 Markl M, Frydrychowicz A, Kozerke S. et al 4D flow MRI. J Magn Reson Imaging 2012; 36: 1015-1036 . doi:10.1002/jmri.23632
    CrossrefPubMedGoogle Scholar
  • 19 Nguyen TD, Spincemaille P, Cham MD. et al Free-breathing 3-dimensional steady-state free precession coronary magnetic resonance angiography: comparison of four navigator gating techniques. Magn Reson Imaging 2009; 27: 807-814 . doi:10.1016/j.mri.2008.11.010
    CrossrefPubMedGoogle Scholar
  • 20 Kolbitsch C, Prieto C, Smink J. et al Highly efficient whole-heart imaging using radial phase encoding-phase ordering with automatic window selection. Magn Reson Med 2011; 66: 1008-1018 . doi:10.1002/mrm.22888
    CrossrefPubMedGoogle Scholar
  • 21 Kolbitsch C, Bastkowski R, Schaffter T. et al Respiratory motion corrected 4D flow using golden radial phase encoding. Magn Reson Med 2020; 83: 635-644 . doi:10.1002/mrm.27918
    CrossrefPubMedGoogle Scholar
  • 22 Grist TM, Korosec FR, Peters DC. et al Steady-state and dynamic MR angiography with MS-325: initial experience in humans. Radiology 1998; 207: 539-544 . doi:10.1148/radiology.207.2.9577507
    CrossrefPubMedGoogle Scholar
  • 23 Bannas P, Bookwalter CA, Ziemlewicz T. et al Combined gadoxetic acid and gadofosveset enhanced liver MRI for detection and characterization of liver metastases. Eur Radiol 2017; 27: 32-40 . doi:10.1007/s00330-016-4375-6
    CrossrefPubMedGoogle Scholar
  • 24 Bannas P, Bell LC, Johnson KM. et al Pulmonary Embolism Detection with Three-dimensional Ultrashort Echo Time MR Imaging: Experimental Study in Canines. Radiology 2016; 278: 413-421 . doi:10.1148/radiol.2015150606
    CrossrefPubMedGoogle Scholar
  • 25 Bannas P, Roldan-Alzate A, Johnson KM. et al Longitudinal Monitoring of Hepatic Blood Flow before and after TIPS by Using 4D-Flow MR Imaging. Radiology 2016; 281: 574-582 . doi:10.1148/radiol.2016152247
    CrossrefPubMedGoogle Scholar
  • 26 Stankovic Z, Allen BD, Garcia J. et al 4D flow imaging with MRI. Cardiovasc Diagn Ther 2014; 4: 173-192 . doi:10.3978/j.issn.2223-3652.2014.01.02
    PubMedGoogle Scholar
  • 27 Neuhaus E, Weiss K, Bastkowski R. et al Accelerated aortic 4D flow cardiovascular magnetic resonance using compressed sensing: applicability, validation and clinical integration. J Cardiovasc Magn Reson 2019; 21: 65 . doi:10.1186/s12968-019-0573-0
    CrossrefPubMedGoogle Scholar
  • 28 Moersdorf R, Treutlein M, Kroeger JR. et al Precision, reproducibility and applicability of an undersampled multi-venc 4D flow MRI sequence for the assessment of cardiac hemodynamics. Magn Reson Imaging 2019; 61: 73-82 . doi:10.1016/j.mri.2019.05.015
    CrossrefPubMedGoogle Scholar
  • 29 David A, Le Touze D, Warin-Fresse K. et al In-vitro validation of 4D flow MRI measurements with an experimental pulsatile flow model. Diagn Interv Imaging 2019; 100: 17-23 . doi:10.1016/j.diii.2018.08.012
    CrossrefPubMedGoogle Scholar
  • 30 Kweon J, Yang DH, Kim GB. et al Four-dimensional flow MRI for evaluation of post-stenotic turbulent flow in a phantom: comparison with flowmeter and computational fluid dynamics. Eur Radiol 2016; 26: 3588-3597 . doi:10.1007/s00330-015-4181-6
    CrossrefPubMedGoogle Scholar
  • 31 Stam K, Chelu RG, van der Velde N. et al Validation of 4D flow CMR against simultaneous invasive hemodynamic measurements: a swine study. Int J Cardiovasc Imaging 2019; 35: 1111-1118 . doi:10.1007/s10554-019-01593-x
    CrossrefPubMedGoogle Scholar
  • 32 Roldan-Alzate A, Frydrychowicz A, Niespodzany E. et al In vivo validation of 4D flow MRI for assessing the hemodynamics of portal hypertension. J Magn Reson Imaging 2013; 37: 1100-1108 . doi:10.1002/jmri.23906
    CrossrefPubMedGoogle Scholar
  • 33 Stankovic Z, Frydrychowicz A, Csatari Z. et al MR-based visualization and quantification of three-dimensional flow characteristics in the portal venous system. J Magn Reson Imaging 2010; 32: 466-475 . doi:10.1002/jmri.22248
    CrossrefPubMedGoogle Scholar
  • 34 Bock J, Toger J, Bidhult S. et al Validation and reproducibility of cardiovascular 4D-flow MRI from two vendors using 2 × 2 parallel imaging acceleration in pulsatile flow phantom and in vivo with and without respiratory gating. Acta Radiol 2019; 60: 327-337 . doi:10.1177/0284185118784981
    CrossrefPubMedGoogle Scholar
  • 35 Szajer J, Ho-Shon K. A comparison of 4D flow MRI-derived wall shear stress with computational fluid dynamics methods for intracranial aneurysms and carotid bifurcations – A review. Magn Reson Imaging 2018; 48: 62-69 . doi:10.1016/j.mri.2017.12.005
    CrossrefPubMedGoogle Scholar
  • 36 Motosugi U, Hernando D, Bannas P. et al Quantification of liver fat with respiratory-gated quantitative chemical shift encoded MRI. J Magn Reson Imaging 2015; 42: 1241-1248 . doi:10.1002/jmri.24896
    CrossrefPubMedGoogle Scholar
  • 37 Talwalkar JA, Yin M, Fidler JL. et al Magnetic resonance imaging of hepatic fibrosis: emerging clinical applications. Hepatology 2008; 47: 332-342 . doi:10.1002/hep.21972
    CrossrefPubMedGoogle Scholar
  • 38 Sharma SD, Fischer R, Schoennagel BP. et al MRI-based quantitative susceptibility mapping (QSM) and R2* mapping of liver iron overload: Comparison with SQUID-based biomagnetic liver susceptometry. Magn Reson Med 2017; 78: 264-270 . doi:10.1002/mrm.26358
    CrossrefPubMedGoogle Scholar
  • 39 Stankovic Z, Csatari Z, Deibert P. et al A feasibility study to evaluate splanchnic arterial and venous hemodynamics by flow-sensitive 4D MRI compared with Doppler ultrasound in patients with cirrhosis and controls. Eur J Gastroenterol Hepatol 2013; 25: 669-675 . doi:10.1097/MEG.0b013e32835e1297
    CrossrefPubMedGoogle Scholar
  • 40 Roldan-Alzate A, Frydrychowicz A, Said A. et al Impaired regulation of portal venous flow in response to a meal challenge as quantified by 4D flow MRI. J Magn Reson Imaging 2015; 42: 1009-1017 . doi:10.1002/jmri.24886
    CrossrefPubMedGoogle Scholar
  • 41 Bosch J, Mastai R, Kravetz D. et al Measurement of azygos venous blood flow in the evaluation of portal hypertension in patients with cirrhosis. Clinical and haemodynamic correlations in 100 patients. J Hepatol 1985; 1: 125-139 . doi:10.1016/s0168-8278(85)80761-3
    CrossrefPubMedGoogle Scholar
  • 42 Motosugi U, Roldan-Alzate A, Bannas P. et al Four-dimensional Flow MRI as a Marker for Risk Stratification of Gastroesophageal Varices in Patients with Liver Cirrhosis. Radiology 2019; 290: 101-107 . doi:10.1148/radiol.2018180230
    CrossrefPubMedGoogle Scholar
  • 43 Rossle M. TIPS: 25 years later. J Hepatol 2013; 59: 1081-1093 . doi:10.1016/j.jhep.2013.06.014
    CrossrefPubMedGoogle Scholar
  • 44 Piecha F, Radunski UK, Ozga AK. et al Ascites control by TIPS is more successful in patients with a lower paracentesis frequency and is associated with improved survival. JHEP Rep 2019; 1: 90-98 . doi:10.1016/j.jhepr.2019.04.001
    CrossrefPubMedGoogle Scholar
  • 45 Owen JW, Saad NE, Foster G. et al The Feasibility of Using Volumetric Phase-Contrast MR Imaging (4D Flow) to Assess for Transjugular Intrahepatic Portosystemic Shunt Dysfunction. J Vasc Interv Radiol 2018; 29: 1717-1724 . doi:10.1016/j.jvir.2018.07.022
    CrossrefPubMedGoogle Scholar
  • 46 Stankovic Z, Rossle M, Euringer W. et al Effect of TIPS placement on portal and splanchnic arterial blood flow in 4-dimensional flow MRI. Eur Radiol 2015; 25: 2634-2640 . doi:10.1007/s00330-015-3663-x
    PubMedGoogle Scholar
  • 47 Rutkowski DR, Reeder SB, Fernandez LA. et al Surgical planning for living donor liver transplant using 4D flow MRI, computational fluid dynamics and in vitro experiments. Computer Methods in Biomechanics and Biomedical Engineering-Imaging and Visualization 2018; 6: 545-555 . doi:10.1080/21681163.2017.1278619
    CrossrefPubMedGoogle Scholar
  • 48 Lenz A, Fischer L, Li J. et al 4D Flow MRI for Monitoring Portal Flow in a Liver Transplant Recipient with a Renoportal Anastomosis. Rofo 2019; 191: 847-848 . doi:10.1055/a-0862-0778
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Paskonis M, Jurgaitis J, Mehrabi A. et al Surgical strategies for liver transplantation in the case of portal vein thrombosis--current role of cavoportal hemitransposition and renoportal anastomosis. Clin Transplant 2006; 20: 551-562 . doi:10.1111/j.1399-0012.2006.00560.x
    CrossrefPubMedGoogle Scholar
  • 50 Afdhal N, McHutchison J, Brown R. et al Thrombocytopenia associated with chronic liver disease. J Hepatol 2008; 48: 1000-1007 . doi:10.1016/j.jhep.2008.03.009
    CrossrefPubMedGoogle Scholar
  • 51 Keller EJ, Kulik L, Stankovic Z. et al JOURNAL CLUB: Four-Dimensional Flow MRI-Based Splenic Flow Index for Predicting Cirrhosis-Associated Hypersplenism. Am J Roentgenol 2017; 209: 46-54 . doi:10.2214/AJR.16.17620
    CrossrefPubMedGoogle Scholar
  • 52 Plouin PF, Bax L. Diagnosis and treatment of renal artery stenosis. Nat Rev Nephrol 2010; 6: 151-159 . doi:10.1038/nrneph.2009.230
    CrossrefPubMedGoogle Scholar
  • 53 Bley TA, Johnson KM, Francois CJ. et al Noninvasive Assessment of Transstenotic Pressure Gradients in Porcine Renal Artery Stenoses by Using Vastly Undersampled Phase-Contrast MR Angiography. Radiology 2011; 261: 266-273 . doi:10.1148/radiol.11101175
    CrossrefPubMedGoogle Scholar
  • 54 Ishikawa T, Takehara Y, Yamashita S. et al Hemodynamic assessment in a child with renovascular hypertension using time-resolved three-dimensional cine phase-contrast MRI. J Magn Reson Imaging 2015; 41: 165-168 . doi:10.1002/jmri.24522
    CrossrefPubMedGoogle Scholar
  • 55 Motoyama D, Ishii Y, Takehara Y. et al Four-dimensional phase-contrast vastly undersampled isotropic projection reconstruction (4D PC-VIPR) MR evaluation of the renal arteries in transplant recipients: Preliminary results. J Magn Reson Imaging 2017; 46: 595-603 . doi:10.1002/jmri.25607
    CrossrefPubMedGoogle Scholar
  • 56 von Kodolitsch Y, Rybczynski M, Vogler M. et al The role of the multidisciplinary health care team in the management of patients with Marfan syndrome. J Multidiscip Healthc 2016; 9: 587-614 . doi:10.2147/JMDH.S93680
    CrossrefPubMedGoogle Scholar
  • 57 Guo DC, Papke CL, He R. et al Pathogenesis of thoracic and abdominal aortic aneurysms. Ann N Y Acad Sci 2006; 1085: 339-352 . doi:10.1196/annals.1383.013
    CrossrefPubMedGoogle Scholar
  • 58 Kuivaniemi H, Ryer EJ, Elmore JR. et al Understanding the pathogenesis of abdominal aortic aneurysms. Expert Rev Cardiovasc Ther 2015; 13: 975-987 . doi:10.1586/14779072.2015.1074861
    CrossrefPubMedGoogle Scholar
  • 59 Malek AM, Jackman R, Rosenberg RD. et al Endothelial expression of thrombomodulin is reversibly regulated by fluid shear stress. Circ Res 1994; 74: 852-860 . doi:10.1161/01.res.74.5.852
    CrossrefPubMedGoogle Scholar
  • 60 Tanweer O, Wilson TA, Metaxa E. et al A comparative review of the hemodynamics and pathogenesis of cerebral and abdominal aortic aneurysms: lessons to learn from each other. J Cerebrovasc Endovasc Neurosurg 2014; 16: 335-349 . doi:10.7461/jcen.2014.16.4.335
    CrossrefPubMedGoogle Scholar
  • 61 Dhawan SS, Avati Nanjundappa RP, Branch JR. et al Shear stress and plaque development. Expert Rev Cardiovasc Ther 2010; 8: 545-556 . doi:10.1586/erc.10.28
    CrossrefPubMedGoogle Scholar
  • 62 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: 128-138 . doi:10.1002/jmri.23610
    CrossrefPubMedGoogle Scholar
  • 63 Sughimoto K, Shimamura Y, Tezuka C. et al Effects of arterial blood flow on walls of the abdominal aorta: distributions of wall shear stress and oscillatory shear index determined by phase-contrast magnetic resonance imaging. Heart Vessels 2016; 31: 1168-1175 . doi:10.1007/s00380-015-0758-x
    CrossrefPubMedGoogle Scholar
  • 64 Liu D, Fan Z, Li Y. et al Quantitative Study of Abdominal Blood Flow Patterns in Patients with Aortic Dissection by 4-Dimensional Flow MRI. Sci Rep 2018; 8: 9111 . doi:10.1038/s41598-018-27249-9
    CrossrefPubMedGoogle Scholar
  • 65 Hope TA, Zarins CK, Herfkens RJ. Initial experience characterizing a type I endoleak from velocity profiles using time-resolved three-dimensional phase-contrast MRI. J Vasc Surg 2009; 49: 1580-1584 . doi:10.1016/j.jvs.2009.01.010
    CrossrefPubMedGoogle Scholar
  • 66 Siedek F, Giese D, Weiss K. et al 4D flow MRI for the analysis of celiac trunk and mesenteric artery stenoses. Magn Reson Imaging 2018; 53: 52-62 . doi:10.1016/j.mri.2018.06.021
    CrossrefPubMedGoogle Scholar
  • 67 Macdonald JA, Corrado PA, Nguyen SM. et al Uteroplacental and Fetal 4D Flow MRI in the Pregnant Rhesus Macaque. J Magn Reson Imaging 2019; 49: 534-545 . doi:10.1002/jmri.26206
    CrossrefPubMedGoogle Scholar
  • 68 Schrauben EM, Saini BS, Darby JRT. et al Fetal hemodynamics and cardiac streaming assessed by 4D flow cardiovascular magnetic resonance in fetal sheep. J Cardiovasc Magn Reson 2019; 21: 8 . doi:10.1186/s12968-018-0512-5
    CrossrefPubMedGoogle Scholar