European Radiology

, Volume 27, Issue 12, pp 5316–5324 | Cite as

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

  • A. Frydrychowicz
  • A. Roldan-Alzate
  • E. Winslow
  • D. Consigny
  • C. A. Campo
  • U. Motosugi
  • K. M. Johnson
  • O. Wieben
  • S. B. Reeder
Magnetic Resonance



Objectives of this study were to compare radial time-resolved phase contrast magnetic resonance imaging (4D Flow-MRI) with perivascular ultrasound (pvUS) and to explore a porcine model of acute pre-hepatic portal hypertension (PHTN).


Abdominal 4D Flow-MRI and pvUS in portal and splenic vein, hepatic and both renal arteries were performed in 13 pigs of approximately 60 kg. In six pigs, measurements were repeated after partial portal vein (PV) ligature. Inter- and intra-reader comparisons and statistical analysis including Bland–Altman (BA) comparison, paired Student’s t tests and linear regression were performed.


PvUS and 4D Flow-MRI measurements agreed well; flow before partial PV ligature was 322 ± 30 ml/min in pvUS and 297 ± 27 ml/min in MRI (p = 0.294), and average BA difference was 25 ml/min [−322; 372]. Inter- and intra-reader results differed very little, revealed excellent correlation (R 2 = 0.98 and 0.99, respectively) and resulted in BA differences of −5 ml/min [−161; 150] and −2 ml/min [−28; 25], respectively. After PV ligature, PV flow decreased from 356 ± 50 to 298 ± 61 ml/min (p = 0.02), and hepatic arterial flow increased from 277 ± 36 to 331 ± 65 ml/min (p = n.s.).


The successful in vivo comparison of radial 4D Flow-MRI to perivascular ultrasound revealed good agreement of abdominal blood flow although with considerable spread of results. A model of pre-hepatic PHTN was successfully introduced and acute responses monitored.

Key Points

Radial 4D Flow-MRI in the abdomen was successfully compared to perivascular ultrasound.

Inter- and intra-reader testing demonstrated excellent reproducibility of upper abdominal 4D Flow-MRI.

A porcine model of acute pre-hepatic portal hypertension was successfully introduced.

4D Flow-MRI successfully monitored acute changes in a model of portal hypertension.


Phase contrast magnetic resonance imaging Blood flow Portal hypertension 4D Flow-MRI Animal model 





Body weight




Flip angle


Field of view


Generalized autocalibrating partially parallel acquisitions


Hepatic artery


Hepatic arterial buffer response


Hepatic venous pressure gradient


Spatial and temporal


Left renal artery


Magnetic resonance imaging


Principal component analysis


Portal hypertension


Portal vein


Perivascular ultrasound


Research Animal Resources Center


Right renal artery


Standard error of the mean


Standard deviation


Signal-to-noise ratio


Splenic vein




Echo time


Repetition time




Velocity encoding sensitivity



The authors would like to thank Sara John and Kelli Hellenbrand for their support in conducting this study. We also wish to thank the NIH, the University of Wisconsin Department of Radiology R&D committee, Bracco Diagnostics and GE Healthcare for their support.

Compliance with ethical standards


The scientific guarantor of this publication is Dr. Alex Frydrychowicz.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.


This study has received funding by NIH (R01DK09616, R01HL072260, K24DK102595), the University of Wisconsin Department of Radiology R&D committee, Bracco Diagnostics and GE Healthcare.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Ethical approval

Approval from the institutional animal care committee was obtained.


  • retrospective

  • diagnostic study/experimental

  • performed at one institution


  1. 1.
    Bosch J, Garcia-Pagan JC (2000) Complications of cirrhosis I. Portal hypertension. J Hepatol 32:141–156CrossRefPubMedGoogle Scholar
  2. 2.
    de Franchis R (2010) Revising consensus in portal hypertension: report of the Baveno V consensus workshop on methodology of diagnosis and therapy in portal hypertension. J Hepatol 53:762–768CrossRefPubMedGoogle Scholar
  3. 3.
    Bosch J, Abraldes JG, Berzigotti A, Garcia-Pagan JC (2009) The clinical use of HVPG measurements in chronic liver disease. Nat Rev Gastroenterol Hepatol 6:573–582CrossRefPubMedGoogle Scholar
  4. 4.
    Frydrychowicz AP, Landgraf BR, Niespodzany E et al (2011) Four-dimensional velocity mapping of the hepatic and splanchnic vasculature with radial sampling at 3 tesla: a feasibility study in portal hypertension. J Magn Reson Imaging 34:577–584CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Roldán-Alzate A, Frydrychowicz A, Niespodzany E et al (2013) In vivo validation of 4D flow MRI for assessing the hemodynamics of portal hypertension. J Magn Reson Imaging 37:1100–1108CrossRefPubMedGoogle Scholar
  6. 6.
    Roldán-Alzate A, Frydrychowicz A, Said A et al (2015) Impaired regulation of portal venous flow in response to a meal challenge as quantified by 4D flow MRI. J Magn Reson Imaging 42:1009–1017CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Stankovic Z, Csatari Z, Deibert P et al (2012) Normal and altered three-dimensional portal venous hemodynamics in patients with liver cirrhosis. Radiology 262:862–873CrossRefPubMedGoogle Scholar
  8. 8.
    Stankovic Z, Blanke P, Markl M (2012) Usefulness of 4D MRI flow imaging to control TIPS function. Am J Gastroenterol 107:327–328CrossRefPubMedGoogle Scholar
  9. 9.
    Stankovic Z, Frydrychowicz A, Csatari Z et al (2010) MR-based visualization and quantification of three-dimensional flow characteristics in the portal venous system. J Magn Reson Imaging 32:466–475CrossRefPubMedGoogle Scholar
  10. 10.
    Bannas P, Roldán-Alzate A, Johnson KM et al (2016) Longitudinal monitoring of hepatic blood flow before and after TIPS by using 4D-flow MR imaging. Radiology 281:574–582CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Wentland AL, Grist TM, Wieben O (2013) Repeatability and internal consistency of abdominal 2D and 4D phase contrast MR flow measurements. Acad Radiol 20:699–704CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Stankovic Z, Jung B, Collins J et al (2014) Reproducibility study of four-dimensional flow MRI of arterial and portal venous liver hemodynamics: influence of spatio-temporal resolution. Magn Reson Med 72:477–484CrossRefPubMedGoogle Scholar
  13. 13.
    Stankovic Z, Fink J, Collins JD et al (2015) K-t GRAPPA-accelerated 4D flow MRI of liver hemodynamics: influence of different acceleration factors on qualitative and quantitative assessment of blood flow. MAGMA 28:149–159CrossRefPubMedGoogle Scholar
  14. 14.
    Parekh K, Markl M, Rose M et al (2017) 4D flow MR imaging of the portal venous system: a feasibility study in children. Eur Radiol 27:832–840CrossRefPubMedGoogle Scholar
  15. 15.
    Dyvorne H, Knight-Greenfield A, Jajamovich G et al (2015) Abdominal 4D flow MR imaging in a breath hold: combination of spiral sampling and dynamic compressed sensing for highly accelerated acquisition. Radiology 275:245–254CrossRefPubMedGoogle Scholar
  16. 16.
    Stankovic Z, Rössle M, Euringer W et al (2015) Effect of TIPS placement on portal and splanchnic arterial blood flow in 4-dimensional flow MRI. Eur Radiol 25:2634–2640CrossRefPubMedGoogle Scholar
  17. 17.
    Giese D, Schaeffter T, Kozerke S (2013) Highly undersampled phase-contrast flow measurements using compartment-based k-t principal component analysis. Magn Reson Med 69:434–443CrossRefPubMedGoogle Scholar
  18. 18.
    Jung B, Honal M, Ullmann P et al (2008) Highly k-t-space-accelerated phase-contrast MRI. Magn Reson Med 60:1169–1177CrossRefPubMedGoogle Scholar
  19. 19.
    Gu T, Korosec FR, Block WF et al (2005) PC VIPR: a high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. Am J Neuroradiol 26:743–749PubMedGoogle Scholar
  20. 20.
    Dyverfeldt P, Bissell M, Barker AJ et al (2015) 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson 17:1–19CrossRefGoogle Scholar
  21. 21.
    Nordmeyer S, Riesenkampff E, Khasheei A et al (2010) Flow-sensitive four-dimensional cine magnetic resonance imaging for offline blood flow quantification in multiple vessels: a validation study. J Magn Reson Imaging 32:677–683CrossRefPubMedGoogle Scholar
  22. 22.
    Uribe S, Beerbaum P, Sørensen TS et al (2009) Four-dimensional (4D) flow of the whole heart and great vessels using real-time respiratory self-gating. Magn Reson Med 62:984–992CrossRefPubMedGoogle Scholar
  23. 23.
    Frydrychowicz AP, Wieben O, Niespodzany E et al (2013) Quantification of thoracic blood flow using volumetric magnetic resonance imaging with radial velocity encoding: in vivo validation. Invest Radiol 48:819–825CrossRefPubMedGoogle Scholar
  24. 24.
    Hsiao A, Tariq U, Alley MT et al (2015) Inlet and outlet valve flow and regurgitant volume may be directly and reliably quantified with accelerated, volumetric phase-contrast MRI. J Magn Reson Imaging 41:376–385CrossRefPubMedGoogle Scholar
  25. 25.
    Ley S, Unterhinninghofen R, Ley-Zaporozhan J et al (2008) Validation of magnetic resonance phase-contrast flow measurements in the main pulmonary artery and aorta using perivascular ultrasound in a large animal model. Invest Radiol 43:421–426CrossRefPubMedGoogle Scholar
  26. 26.
    Ganter CC, Buser C, Haenggi M et al (2009) Inverse thermodilution with conventional pulmonary artery catheters for the assessment of cerebral, hepatic, renal, and femoral blood flow. Shock 32:194–200CrossRefPubMedGoogle Scholar
  27. 27.
    Bock J, Frydrychowicz A, Stalder AF et al (2010) 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 63:330–338CrossRefPubMedGoogle Scholar
  28. 28.
    Johnson KM, Markl M (2010) Improved SNR in phase contrast velocimetry with five-point balanced flow encoding. Magn Reson Med 63:349–355CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Stalder AF, Russe MF, Frydrychowicz AP et al (2008) Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med 60:1218–1231CrossRefPubMedGoogle Scholar
  30. 30.
    Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310CrossRefPubMedGoogle Scholar
  31. 31.
    Nett EJ, Johnson KM, Frydrychowicz A et al (2012) Four-dimensional phase contrast MRI with accelerated dual velocity encoding. J Magn Reson Imaging 35:1462–1471CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Binter C, Knobloch V, Manka R et al (2013) Bayesian multipoint velocity encoding for concurrent flow and turbulence mapping. Magn Reson Med 69:1337–1345CrossRefPubMedGoogle Scholar
  33. 33.
    Bernstein MA, Zhou XJ, Polzin JA et al (1998) Concomitant gradient terms in phase contrast MR: analysis and correction. Magn Reson Med 39:300–308CrossRefPubMedGoogle Scholar
  34. 34.
    Walker PG, Cranney GB, Scheidegger MB et al (1993) Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J Magn Reson Imaging 3:521–530CrossRefPubMedGoogle Scholar
  35. 35.
    Giese D, Haeberlin M, Barmet C et al (2012) Analysis and correction of background velocity offsets in phase‐contrast flow measurements using magnetic field monitoring. Magn Reson Med 67:1294–1302CrossRefPubMedGoogle Scholar
  36. 36.
    Busch J, Vannesjo SJ, Barmet C et al (2014) Analysis of temperature dependence of background phase errors in phase-contrast cardiovascular magnetic resonance. J Cardiovasc Magn Reson 16:97CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kaufman S, Levasseur J (2003) Effect of portal hypertension on splenic blood flow, intrasplenic extravasation and systemic blood pressure. Am J Physiol Regul Integr Comp Physiol 284:R1580–R1585CrossRefPubMedGoogle Scholar
  38. 38.
    Lautt WW (1985) Mechanism and role of intrinsic regulation of hepatic arterial blood flow: hepatic arterial buffer response. Am J Physiol 249:G549–G556PubMedGoogle Scholar
  39. 39.
    Abraldes JG, Pasarín M, Garcia-Pagan JC (2006) Animal models of portal hypertension. World J Gastroenterol 12:6577–6584CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Burgener FA, Gutierrez OH, Logsdon GA (1982) Angiographic, hemodynamic, and histologic evaluation of portal hypertension and periportal fibrosis induced in the dog by intraportal polyvinyl alcohol injections. Radiology 143:379–385CrossRefPubMedGoogle Scholar
  41. 41.
    Chuang VP, Tsai CC, Soo CS et al (1982) Experimental canine hepatic artery embolization with polyvinyl alcohol foam particles. Radiology 145:21–25CrossRefPubMedGoogle Scholar
  42. 42.
    Bosch J, Enriquez R, Groszmann RJ, Storer EH (1983) Chronic bile duct ligation in the dog: hemodynamic characterization of a portal hypertensive model. Hepatology 3:1002–1007CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2017

Authors and Affiliations

  • A. Frydrychowicz
    • 1
    • 2
    • 3
  • A. Roldan-Alzate
    • 1
    • 4
  • E. Winslow
    • 5
  • D. Consigny
    • 1
  • C. A. Campo
    • 1
  • U. Motosugi
    • 1
  • K. M. Johnson
    • 6
  • O. Wieben
    • 1
    • 6
  • S. B. Reeder
    • 1
    • 6
    • 7
    • 8
    • 9
  1. 1.Department of Radiology, School of Medicine and Public Health, E3/366 Clinical Science CenterUniversity of Wisconsin – MadisonMadisonUSA
  2. 2.Clinic for Radiology and Nuclear MedicineUniversity Hospital Schleswig-Holstein, Campus LübeckLübeckGermany
  3. 3.University of LübeckLübeckGermany
  4. 4.Department of Mechanical EngineeringUniversity of WisconsinMadisonUSA
  5. 5.Department of SurgeryUniversity of WisconsinMadisonUSA
  6. 6.Department of Medical PhysicsUniversity of WisconsinMadisonUSA
  7. 7.Department of Biomedical EngineeringUniversity of WisconsinMadisonUSA
  8. 8.Department of MedicineUniversity of WisconsinMadisonUSA
  9. 9.Department of Emergency MedicineUniversity of WisconsinMadisonUSA

Personalised recommendations