Abstract
Purpose
The purpose of this work was to establish normal reference values for 4D flow MRI-derived flow, velocity, and vessel diameters, and to define characteristic flow patterns in the portal venous system of healthy adult subjects.
Methods
For this retrospective study, we screened all available 4D flow MRI exams of the upper abdomen in healthy adults acquired at our institution between 2012 and 2022 at either 1.5 T or 3.0 T MRI after ≥ 5 h fasting. Flow, velocity, and effective diameter were quantified in the 8 planes in the portal venous system (splenic vein, superior mesenteric vein, main, right, and left portal veins). Vessel delineation was manually adjusted over time. Reference ranges for were defined as the mean ± 2 standard deviations. Three readers noted helical and vortical flow on time-resolved pathline visualizations. Conservation of mass flow analysis was performed for quality assurance.
Results
We included 44 healthy subjects (26 female, 18–74 years) in the analysis. We report reference values for mean and peak flow, mean velocity, and vessel diameter in the healthy portal vein using 4D flow MRI. Normal flow patterns in the portal vein included faint helical (66%) or linear flow (34%). Conservation of mass analysis demonstrated a relative error of 1.1 ± 4.6% standard deviation (SD) at the splenomesenteric confluence and − 1.4 ± 4.1% SD at the portal bifurcation.
Conclusion
We have reported normal hemodynamic values that are necessary baseline data for emerging clinical applications of 4D flow MRI in the portal venous system. Results are consistent with previously published values from smaller cohorts.
Graphical abstract

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References
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. https://doi.org/10.1186/s12968-015-0174-5.
Oechtering TH, Roberts GS, Panagiotopoulos N, Wieben O, Reeder SB, Roldán-Alzate A. Clinical Applications of 4D Flow MRI in the Portal Venous System. Magn Reson Med Sci. 2022. https://doi.org/10.2463/mrms.rev.2021-0105.
Frydrychowicz A, Roldan-Alzate A, Winslow E, Consigny D, Campo CA, Motosugi U, 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(12):5316-24. https://doi.org/10.1007/s00330-017-4862-4.
Motosugi U, Roldán-Alzate A, Bannas P, Said A, Kelly S, Zea R, et al. Four-dimensional Flow MRI as a Marker for Risk Stratification of Gastroesophageal Varices in Patients with Liver Cirrhosis. Radiology. 2019;290(1):101-7. https://doi.org/10.1148/radiol.2018180230.
Roberts GS, François CJ, Starekova J, Roldán-Alzate A, Wieben O. Non-invasive assessment of mesenteric hemodynamics in patients with suspected chronic mesenteric ischemia using 4D flow MRI. Abdom Radiol (NY). 2021. https://doi.org/10.1007/s00261-020-02900-0.
Roldan-Alzate A, Frydrychowicz A, Said A, Johnson KM, Francois CJ, Wieben O, 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(4):1009-17. https://doi.org/10.1002/jmri.24886.
Keller EJ, Kulik L, Stankovic Z, Lewandowski RJ, Salem R, Carr JC, et al. JOURNAL CLUB: Four-Dimensional Flow MRI-Based Splenic Flow Index for Predicting Cirrhosis-Associated Hypersplenism. AJR American journal of roentgenology. 2017;209(1):46-54. https://doi.org/10.2214/AJR.16.17620.
Oechtering TH, Roberts GS, Panagiotopoulos N, Wieben O, Reeder SB, Roldan-Alzate A. Clinical Applications of 4D Flow MRI in the Portal Venous System. Magn Reson Med Sci. 2022. https://doi.org/10.2463/mrms.rev.2021-0105.
Krishnamurthy R, Bahouth SM, Muthupillai R. 4D Contrast-enhanced MR Angiography with the Keyhole Technique in Children: Technique and Clinical Applications. Radiographics. 2016;36(2):523-37. https://doi.org/10.1148/rg.2016150106.
Owen JW, Saad NE, Foster G, Fowler KJ. The Feasibility of Using Volumetric Phase-Contrast MR Imaging (4D Flow) to Assess for Transjugular Intrahepatic Portosystemic Shunt Dysfunction. Journal of vascular and interventional radiology : JVIR. 2018;29(12):1717-24. https://doi.org/10.1016/j.jvir.2018.07.022.
Stankovic Z, Rossle M, Euringer W, Schultheiss M, Salem R, Barker A, et al. Effect of TIPS placement on portal and splanchnic arterial blood flow in 4-dimensional flow MRI. Eur Radiol. 2015;25(9):2634-40. https://doi.org/10.1007/s00330-015-3663-x.
Motosugi U, Roldan-Alzate A, Bannas P, Said A, Kelly S, Zea R, et al. Four-dimensional Flow MRI as a Marker for Risk Stratification of Gastroesophageal Varices in Patients with Liver Cirrhosis. Radiology. 2019;290(1):101-7. https://doi.org/10.1148/radiol.2018180230.
Bannas P, Roldan-Alzate A, Johnson KM, Woods MA, Ozkan O, Motosugi U, et al. Longitudinal Monitoring of Hepatic Blood Flow before and after TIPS by Using 4D-Flow MR Imaging. Radiology. 2016;281(2):574-82. https://doi.org/10.1148/radiol.2016152247.
Roldán-Alzate A, Campo CA, Mao L, Said A, Wieben O, Reeder SB. Characterization of mesenteric and portal hemodynamics using 4D flow MRI: the effects of meals and diurnal variation. Abdom Radiol (NY). 2022;47(6):2106-14. https://doi.org/10.1007/s00261-022-03513-5.
Brunsing RL, Brown D, Almahoud H, Kono Y, Loomba R, Vodkin I, et al. Quantification of the Hemodynamic Changes of Cirrhosis with Free-Breathing Self-Navigated MRI. J Magn Reson Imaging. 2021;53(5):1410-21. https://doi.org/10.1002/jmri.27488.
Stankovic Z, Csatari Z, Deibert P, Euringer W, Jung B, Kreisel W, 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(6):669-75. https://doi.org/10.1097/MEG.0b013e32835e1297.
Roldan-Alzate A, Frydrychowicz A, Niespodzany E, Landgraf BR, Johnson KM, Wieben O, et al. In vivo validation of 4D flow MRI for assessing the hemodynamics of portal hypertension. J Magn Reson Imaging. 2013;37(5):1100-8. https://doi.org/10.1002/jmri.23906.
Rutkowski DR, Medero R, Garcia FJ, Roldán-Alzate A. MRI-based modeling of spleno-mesenteric confluence flow. J Biomech. 2019;88:95-103. https://doi.org/10.1016/j.jbiomech.2019.03.025.
Stankovic Z, Csatari Z, Deibert P, Euringer W, Blanke P, Kreisel W, et al. Normal and altered three-dimensional portal venous hemodynamics in patients with liver cirrhosis. Radiology. 2012;262(3):862-73. https://doi.org/10.1148/radiol.11110127.
Iranpour P, Lall C, Houshyar R, Helmy M, Yang A, Choi JI, et al. Altered Doppler flow patterns in cirrhosis patients: an overview. Ultrasonography. 2016;35(1):3-12. https://doi.org/10.14366/usg.15020.
Sugimoto H, Kaneko T, Nakao A. Poststenotic dilatation and helical flow in the umbilical portion of the portal vein. J Hepatol. 2002;36(5):704. https://doi.org/10.1016/s0168-8278(02)00053-3.
Rosenthal SJ, Harrison LA, Baxter KG, Wetzel LH, Cox GG, Batnitzky S. Doppler US of helical flow in the portal vein. Radiographics. 1995;15(5):1103-11. https://doi.org/10.1148/radiographics.15.5.7501853.
Stankovic Z, Frydrychowicz A, Csatari Z, Panther E, Deibert P, Euringer W, et al. MR-based visualization and quantification of three-dimensional flow characteristics in the portal venous system. J Magn Reson Imaging. 2010;32(2):466-75. https://doi.org/10.1002/jmri.22248.
Garcia-Tsao G, Groszmann RJ, Fisher RL, Conn HO, Atterbury CE, Glickman M. Portal pressure, presence of gastroesophageal varices and variceal bleeding. Hepatology. 1985;5(3):419-24. https://doi.org/10.1002/hep.1840050313.
Garcia-Tsao G, Abraldes JG, Berzigotti A, Bosch J. Portal hypertensive bleeding in cirrhosis: Risk stratification, diagnosis, and management: 2016 practice guidance by the American Association for the study of liver diseases. Hepatology. 2017;65(1):310-35. https://doi.org/10.1002/hep.28906.
Gaiani S, Bolondi L, Li Bassi S, Santi V, Zironi G, Barbara L. Effect of meal on portal hemodynamics in healthy humans and in patients with chronic liver disease. Hepatology. 1989;9(6):815-9. https://doi.org/10.1002/hep.1840090604.
Moriyasu F, Ban N, Nishida O, Nakamura T, Miyake T, Uchino H, et al. Clinical application of an ultrasonic duplex system in the quantitative measurement of portal blood flow. J Clin Ultrasound. 1986;14(8):579-88. https://doi.org/10.1002/jcu.1870140802.
Landgraf BR, Johnson KM, Roldán-Alzate A, Francois CJ, Wieben O, Reeder SB. Effect of temporal resolution on 4D flow MRI in the portal circulation. J Magn Reson Imaging. 2014;39(4):819-26. https://doi.org/10.1002/jmri.24233.
Walker PG, Cranney GB, Scheidegger MB, Waseleski G, Pohost GM, Yoganathan AP. Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J Magn Reson Imaging. 1993;3(3):521-30. https://doi.org/10.1002/jmri.1880030315.
Liu J, Redmond MJ, Brodsky EK, Alexander AL, Lu A, Thornton FJ, et al. Generation and visualization of four-dimensional MR angiography data using an undersampled 3-D projection trajectory. IEEE Trans Med Imaging. 2006;25(2):148-57. https://doi.org/10.1109/tmi.2005.861706.
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. https://doi.org/10.1002/mrm.21778.
Oechtering TH, Sieren MM, Hunold P, Hennemuth A, Huellebrand M, Scharfschwerdt M, et al. Time-resolved 3-dimensional magnetic resonance phase contrast imaging (4D Flow MRI) reveals altered blood flow patterns in the ascending aorta of patients with valve-sparing aortic root replacement. J Thorac Cardiovasc Surg. 2020;159(3):798-810.e1. https://doi.org/10.1016/j.jtcvs.2019.02.127.
Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation. 1993;88(5 Pt 1):2235-47. https://doi.org/10.1161/01.cir.88.5.2235.
Horn PS, Pesce AJ, Copeland BE. A robust approach to reference interval estimation and evaluation. Clin Chem. 1998;44(3):622-31.
Kempfert J, Van Linden A, Lehmkuhl L, Rastan AJ, Holzhey D, Blumenstein J, et al. Aortic annulus sizing: echocardiographic versus computed tomography derived measurements in comparison with direct surgical sizing. Eur J Cardiothorac Surg. 2012;42(4):627-33. https://doi.org/10.1093/ejcts/ezs064.
Vasanawala SS, Nguyen KL, Hope MD, Bridges MD, Hope TA, Reeder SB, et al. Safety and technique of ferumoxytol administration for MRI. Magn Reson Med. 2016;75(5):2107-11. https://doi.org/10.1002/mrm.26151.
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. https://doi.org/10.1016/j.acra.2012.12.019.
Santini F, Pansini M, Hrabak-Paar M, Yates D, Langenickel TH, Bremerich J, et al. On the optimal temporal resolution for phase contrast cardiovascular magnetic resonance imaging: establishment of baseline values. J Cardiovasc Magn Reson. 2020;22(1):72. https://doi.org/10.1186/s12968-020-00669-1.
Muthusami P, Yoo SJ, Chaturvedi R, Gill N, Windram J, Schantz D, et al. Splanchnic, Thoracoabdominal, and Cerebral Blood Flow Volumes in Healthy Children and Young Adults in Fasting and Postprandial States: Determining Reference Ranges by Using Phase-Contrast MR Imaging. Radiology. 2017;285(1):231-41. https://doi.org/10.1148/radiol.2017162114.
Parekh K, Markl M, Rose M, Schnell S, Popescu A, Rigsby CK. 4D flow MR imaging of the portal venous system: a feasibility study in children. Eur Radiol. 2017;27(2):832-40. https://doi.org/10.1007/s00330-016-4396-1.
Nishida O, Moriyasu F, Nakamura T, Ban N, Miura K, Sakai M, et al. Interrelationship between splenic and superior mesenteric venous circulation manifested by transient splenic arterial occlusion using a balloon catheter. Hepatology. 1987;7(3):442-6. https://doi.org/10.1002/hep.1840070305.
Yzet T, Bouzerar R, Allart JD, Demuynck F, Legallais C, Robert B, et al. Hepatic vascular flow measurements by phase contrast MRI and doppler echography: a comparative and reproducibility study. J Magn Reson Imaging. 2010;31(3):579-88. https://doi.org/10.1002/jmri.22079.
Mise Y, Satou S, Shindoh J, Conrad C, Aoki T, Hasegawa K, et al. Three-dimensional volumetry in 107 normal livers reveals clinically relevant inter-segment variation in size. HPB (Oxford). 2014;16(5):439-47. https://doi.org/10.1111/hpb.12157.
Stamm ER, Meier JM, Pokharel SS, Clark T, Glueck DH, Lind KE, et al. Normal main portal vein diameter measured on CT is larger than the widely referenced upper limit of 13Â mm. Abdom Radiol (NY). 2016;41(10):1931-6. https://doi.org/10.1007/s00261-016-0785-9.
Stankovic Z, Jung B, Collins J, Russe MF, Carr J, Euringer W, 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(2):477-84. https://doi.org/10.1002/mrm.24939.
Acknowledgements
The authors wish to acknowledge the NIH (R01 DK125783) for supporting this study, as well as GE Healthcare who provides research support to the University of Wisconsin. Dr. Reeder is a Fred Lee Sr. Endowed Chair of Radiology. Dr. Oechtering receives funding from the German Research Foundation (OE 746/1-1).
Funding
Funding was provided by National Institutes of Health (R01 DK125783) and Deutsche Forschungsgemeinschaft (OE 746/1-1).
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Huang, A., Roberts, G.S., Roldán-Alzate, A. et al. Reference values for 4D flow magnetic resonance imaging of the portal venous system. Abdom Radiol 48, 2049–2059 (2023). https://doi.org/10.1007/s00261-023-03892-3
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DOI: https://doi.org/10.1007/s00261-023-03892-3