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Advances in application of four dimensional flow MRI in liver diseases
LI Ling  YU Chengxin  LI Liang 

Cite this article as: LI L, YU C X, LI L. Advances in application of four dimensional flow MRI in liver diseases[J]. Chin J Magn Reson Imaging, 2024, 15(6): 212-217. DOI:10.12015/issn.1674-8034.2024.06.034.


[Abstract] Liver blood flow is affected by its complex vascular anatomy, slow blood flow velocity, and human respiratory movement, which is difficult to evaluate liver blood flow by ultrasound, CT, and two dimensional phase contrast MRI (2D PC MRI). Four dimensional flow MRI (4D Flow MRI) can not only visualize the complex blood flow distribution of the liver, but also quantify hemodynamic abnormalities, which is an important imaging tool for evaluating liver hemodynamics. This article mainly introduces the technical principle of 4D Flow MRI and its current application in liver diseases, in order to provide a more comprehensive imaging basis for clinical understanding of the disease progression and efficacy evaluation of related diseases, and provide reference for future research direction.
[Keywords] magnetic resonance imaging;four dimensional flow magnetic resonance imaging;liver;hemodynamics

LI Ling1, 2, 3   YU Chengxin1, 3*   LI Liang1, 3  

1 The First College of Clinical Medical Science, China Three Gorges University, Yichang 443000, China

2 Department of Radiology, The Central Hospital of Enshi Tujia and Miao Autonomous Prefecture, Enshi 445000, China

3 Department of Radiology, Yichang Central People's Hospital, Yichang 443000, China

Corresponding author: YU C X, E-mail: 1542353879@qq.com

Conflicts of interest   None.

Received  2024-01-25
Accepted  2024-04-17
DOI: 10.12015/issn.1674-8034.2024.06.034
Cite this article as: LI L, YU C X, LI L. Advances in application of four dimensional flow MRI in liver diseases[J]. Chin J Magn Reson Imaging, 2024, 15(6): 212-217. DOI:10.12015/issn.1674-8034.2024.06.034.

[1]
ASRANI S K, DEVARBHAVI H, EATON J, et al. Burden of liver diseases in the world[J]. J Hepatol, 2019, 70(1): 151-171. DOI: 10.1016/j.jhep.2018.09.014.
[2]
STANKOVIC Z, CSATARI Z, DEIBERT P, et al. Normal and altered three-dimensional portal venous hemodynamics in patients with liver cirrhosis[J]. Radiology, 2012, 262(3): 862-873. DOI: 10.1148/radiol.11110127.
[3]
MOTOSUGI U, ROLDÁN-ALZATE A, BANNAS P, et al. Four-dimensional flow MRI as a marker for risk stratification of gastroesophageal varices in patients with liver cirrhosis[J]. Radiology, 2019, 290(1): 101-107. DOI: 10.1148/radiol.2018180230.
[4]
HYODO R, TAKEHARA Y, MIZUNO T, et al. Time-resolved 3D cine phase-contrast magnetic resonance imaging (4D-flow MRI) can quantitatively assess portosystemic shunt severity and confirm normalization of portal flow after embolization of large portosystemic shunts[J]. Hepatol Res, 2021, 51(3): 343-349. DOI: 10.1111/hepr.13616.
[5]
TANG Y, ZHANG G Y, KONG W N, et al. Pediatric living donor left lateral segment liver transplantation for biliary atresia: Doppler ultrasound findings in early postoperative period[J]. Jpn J Radiol, 2021, 39(4): 367-375. DOI: 10.1007/s11604-020-01067-4.
[6]
HYODO R, TAKEHARA Y, NAGANAWA S. 4D Flow MRI in the portal venous system: imaging and analysis methods, and clinical applications[J]. Radiol Med, 2022, 127(11): 1181-1198. DOI: 10.1007/s11547-022-01553-x.
[7]
MARUYAMA H, KATO N. Advances in ultrasound diagnosis in chronic liver diseases[J]. Clin Mol Hepatol, 2019, 25(2): 160-167. DOI: 10.3350/cmh.2018.1013.
[8]
LIAO C C, CHEN M H, YU C Y, et al. Non-contrast-enhanced and contrast-enhanced magnetic resonance angiography in living donor liver vascular anatomy[J/OL]. Diagnostics, 2022, 12(2): 498 [2024-03-03]. https://pubmed.ncbi.nlm.nih.gov/35204588/. DOI: 10.3390/diagnostics12020498.
[9]
STANKOVIC Z. Four-dimensional flow magnetic resonance imaging in cirrhosis[J]. World J Gastroenterol, 2016, 22(1): 89-102. DOI: 10.3748/wjg.v22.i1.89.
[10]
RIEDEL C, LENZ A, FISCHER L, et al. Abdominal applications of 4D flow MRI[J]. Rofo, 2021, 193(4): 388-398. DOI: 10.1055/a-1271-7405.
[11]
BRUNSING R L, BROWN D, ALMAHOUD H, et al. Quantification of the hemodynamic changes of cirrhosis with free-breathing self-navigated MRI[J]. J Magn Reson Imaging, 2021, 53(5): 1410-1421. DOI: 10.1002/jmri.27488.
[12]
HIGAKI A, KANKI A, YAMAMOTO A, et al. Liver cirrhosis: relationship between fibrosis-associated hepatic morphological changes and portal hemodynamics using four-dimensional flow magnetic resonance imaging[J]. Jpn J Radiol, 2023, 41(6): 625-636. DOI: 10.1007/s11604-023-01388-0.
[13]
ROLDÁN-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]. J Magn Reson Imaging, 2015, 42(4): 1009-1017. DOI: 10.1002/jmri.24886.
[14]
STANKOVIC Z, RÖSSLE M, EURINGER W, et al. Effect of TIPS placement on portal and splanchnic arterial blood flow in 4-dimensional flow MRI[J]. Eur Radiol, 2015, 25(9): 2634-2640. DOI: 10.1007/s00330-015-3663-x.
[15]
MOON C M, LEE Y Y, KIM S K, et al. Four-dimensional flow MR imaging for evaluating treatment response after transcatheter arterial chemoembolization in cirrhotic patients with hepatocellular carcinoma[J]. Radiol Med, 2023, 128(10): 1163-1173. DOI: 10.1007/s11547-023-01685-8.
[16]
RUTKOWSKI D R, REEDER S B, FERNANDEZ L A, et al. Surgical planning for living donor liver transplant using 4D flow MRI, computational fluid dynamics and in vitro experiments[J]. Comput Methods Biomech Biomed Eng Imaging Vis, 2018, 6(5): 545-555. DOI: 10.1080/21681163.2017.1278619.
[17]
WYMER D T, PATEL K P, BURKE W F, et al. Phase-contrast MRI: physics, techniques, and clinical applications[J]. Radiographics, 2020, 40(1): 122-140. DOI: 10.1148/rg.2020190039.
[18]
SOULAT G, MCCARTHY P, MARKL M. 4D flow with MRI[J]. Annu Rev Biomed Eng, 2020, 22: 103-126. DOI: 10.1146/annurev-bioeng-100219-110055.
[19]
ZHANG H N, SONG Q W, ZHANG Q H, et al. Research advances of magnetic resonance angiography in evaluating carotid arterystenosis[J]. Chin J Magn Reson Imag, 2021, 12(3): 92-94. DOI: 10.12015/issn.1674-8034.2021.03.022.
[20]
DIMOV I P, TOUS C, LI N, et al. Assessment of hepatic arterial hemodynamics with 4D flow MRI: in vitro analysis of motion and spatial resolution related error and in vivo feasibility study in 20 volunteers[J]. Eur Radiol, 2022, 32(12): 8639-8648. DOI: 10.1007/s00330-022-08890-5.
[21]
BANE O, PETI S, WAGNER M, et al. Hemodynamic measurements with an abdominal 4D flow MRI sequence with spiral sampling and compressed sensing in patients with chronic liver disease[J]. J Magn Reson Imaging, 2019, 49(4): 994-1005. DOI: 10.1002/jmri.26305.
[22]
KROEGER J R, STACKL M, WEISS K, et al. K-t accelerated multi-VENC 4D flow MRI improves vortex assessment in pulmonary hypertension[J/OL]. Eur J Radiol, 2021, 145: 110035 [2023-09-28]. https://pubmed.ncbi.nlm.nih.gov/34801875/. DOI: 10.1016/j.ejrad.2021.110035.
[23]
BANE O, STOCKER D, KENNEDY P, et al. 4D flow MRI in abdominal vessels: prospective comparison of k-t accelerated free breathing acquisition to standard respiratory navigator gated acquisition[J/OL]. Sci Rep, 2022, 12(1): 19886 [2023-10-05]. https://pubmed.ncbi.nlm.nih.gov/36400918/. DOI: 10.1038/s41598-022-23864-9.
[24]
BISSELL M M, RAIMONDI F, AIT ALI L, et al. 4D Flow cardiovascular magnetic resonance consensus statement: 2023 update[J/OL]. J Cardiovasc Magn Reson, 2023, 25(1): 40 [2023-10-5]. https://pubmed.ncbi.nlm.nih.gov/37474977/. DOI: 10.1186/s12968-023-00942-z.
[25]
TAKEHARA Y. 4D flow when and how?[J]. Radiol Med, 2020, 125(9): 838-850. DOI: 10.1007/s11547-020-01249-0.
[26]
AZARINE A, GARÇON P, STANSAL A, et al. Four-dimensional flow MRI: principles and cardiovascular applications[J]. Radiographics, 2019, 39(3): 632-648. DOI: 10.1148/rg.2019180091.
[27]
CALLAHAN S, SINGAM N S, KENDRICK M, et al. Dual-Venc acquisition for 4D flow MRI in aortic stenosis with spiral readouts[J]. J Magn Reson Imaging, 2020, 52(1): 117-128. DOI: 10.1002/jmri.27004.
[28]
KROEGER J R, PAVESIO F C, MÖRSDORF R, et al. Velocity quantification in 44 healthy volunteers using accelerated multi-VENC 4D flow CMR[J]. Eur J Radiol, 2021, 137: 109570 [2023-10-25]. https://pubmed.ncbi.nlm.nih.gov/33596498/. DOI: 10.1016/j.ejrad.2021.109570.
[29]
GINÈS P, KRAG A, ABRALDES J G, et al. Liver cirrhosis[J]. Lancet, 2021, 398(10308): 1359-1376. DOI: 10.1016/S0140-6736(21)01374-X.
[30]
LIU H, LIU G Y, ZHOU J L. Progress in imaging assessment of the risk of esophageal varices and bleeding in cirrhosis[J]. Chin J Magn Reson Imag, 2021, 12(9): 109-112. DOI: 10.12015/issn.1674-8034.2021.09.028.
[31]
Chinese Society of Hepatology, Chinese Society of Gastroenterology, Chinese Society of Digestive Endoscopology of Chinese Medical Association. Guidelines for the diagnosis and treatment of esophageal and gastric variceal bleeding in cirrhotic portal hypertension[J]. J Clin Hepatol, 2016, 32(2): 203-219. DOI: 10.3969/j.issn.1001-5256.2016.02.002.
[32]
SANTOPAOLO F, PONZIANI F R, CONTEGIACOMO A, et al. Direct portal pressure gradient measurement in patients withporto-sinusoidal vascular disease[J]. Dig Liver Dis, 2023, 55(1): 144-145. DOI: 10.1016/j.dld.2022.10.013.
[33]
DUNNE P D J, SINHA R, STANLEY A J, et al. Randomised clinical trial: standard of care versus early-transjugular intrahepatic porto-systemic shunt (TIPSS) in patients with cirrhosis and oesophageal variceal bleeding[J]. Aliment Pharmacol Ther, 2020, 52(1): 98-106. DOI: 10.1111/apt.15797.
[34]
SIEDEK F, GIESE D, WEISS K, et al. 4D flow MRI for the analysis of celiac trunk and mesenteric artery stenoses[J]. Magn Reson Imaging, 2018, 53: 52-62. DOI: 10.1016/j.mri.2018.06.021.
[35]
OWEN J W, SAAD N E, FOSTER G, et al. The feasibility of using volumetric phase-contrast MR imaging (4D flow) to assess for transjugular intrahepatic portosystemic shunt dysfunction[J]. J Vasc Interv Radiol, 2018, 29(12): 1717-1724. DOI: 10.1016/j.jvir.2018.07.022.
[36]
BANNAS P, ROLDÁN-ALZATE A, JOHNSON K M, et al. Longitudinal monitoring of hepatic blood flow before and after TIPS by using 4D-flow MR imaging[J]. Radiology, 2016, 281(2): 574-582. DOI: 10.1148/radiol.2016152247.
[37]
RIEDEL C, BANNAS P, LENZ A, et al. 4D flow MRI-guided treatment of portal-hypertensive complications in a patient with multiple extrahepatic arterioportal shunts[J]. Magn Reson Imaging, 2023, 101: 54-56. DOI: 10.1016/j.mri.2023.03.018.
[38]
TRIPATHI D, STANLEY A J, HAYES P C, et al. Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension[J]. Gut, 2020, 69(7): 1173-1192. DOI: 10.1136/gutjnl-2019-320221.
[39]
HIGAKI A, YAMAMOTO A, OKADA T, et al. 4D flow MRI reflects physiological hemodynamics for the diagnosis and management of portosystemic shunts[J/OL]. Magn Reson Med Sci, 2024 [2024-03-04]. https://pubmed.ncbi.nlm.nih.gov/38417875/. DOI: 10.2463/mrms.ici.2023-0161.
[40]
NORTHUP P G, GARCIA-PAGAN J C, GARCIA-TSAO G, et al. Vascular liver disorders, portal vein thrombosis, and procedural bleeding in patients with liver disease: 2020 practice guidance by the American association for the study of liver diseases[J]. Hepatology, 2021, 73(1): 366-413. DOI: 10.1002/hep.31646.
[41]
HYODO R, TAKEHARA Y, MIZUNO T, et al. Assessing the complicated venous hemodynamics and therapeutic outcomes of budd-chiari syndrome with respiratory-gated 4D flow MR imaging during the expiratory and inspiratory phases[J]. Magn Reson Med Sci, 2023, 22(1): 1-6. DOI: 10.2463/mrms.ici.2021-0110.
[42]
CHANG Y, JEONG S W, YOUNG JANG J, et al. Recent updates of transarterial chemoembolilzation in hepatocellular carcinoma[J/OL]. Int J Mol Sci, 2020, 21(21): 8165 [2023-11-01]. https://pubmed.ncbi.nlm.nih.gov/33142892/. DOI: 10.3390/ijms21218165.
[43]
CHEN M, WANG D, ZHAO Y, et al. Preoperative color Doppler ultrasonography predicts early recurrence in AFP-positive hepatocellular carcinoma[J]. Oncol Lett, 2019, 18(5): 4703-4711. DOI: 10.3892/ol.2019.10825.
[44]
CILLO U, FONDEVILA C, DONADON M, et al. Surgery for cholangiocarcinoma[J]. Liver Int, 2019, 39 (Supp l): 143-155. DOI: 10.1111/liv.14089.
[45]
ENTEZARI P, TOSKICH B B, KIM E, et al. Promoting surgical resection through future liver remnant hypertrophy[J]. Radiographics, 2022, 42(7): 2166-2183. DOI: 10.1148/rg.220050.
[46]
HYODO R, TAKEHARA Y, MIZUNO T, et al. Four-dimensional flow MRI assessment of portal hemodynamics and hepatic regeneration after portal vein embolization[J]. Radiology, 2023, 308(3):e230709 [2023-11-15]. https://pubmed.ncbi.nlm.nih.gov/37750777/. DOI: 10.1148/radiol.230709.
[47]
TITHOF J, PRUETT T L, RAO J S. Lumped parameter liver simulation to predict acute haemodynamic alterations following partial resections[J]. J R Soc Interface, 2023, 20(207): 20230444 [2023-11-20]. https://pubmed.ncbi.nlm.nih.gov/37876272/. DOI: 10.1098/rsif.2023.0444.
[48]
KIM D, JEN M L, EISENMENGER L B, et al. Accelerated 4D-flow MRI with 3-point encoding enabled by machine learning[J]. Magn Reson Med, 2023, 89(2): 800-811. DOI: 10.1002/mrm.29469.
[49]
YOU S, MASUTANI E M, ALLEY M T, et al. Deep learning automated background phase error correction for abdominopelvic 4D flow MRI[J]. Radiology, 2022, 302(3): 584-592. DOI: 10.1148/radiol.2021211270.
[50]
BERHANE H, SCOTT M, ELBAZ M, et al. Fully automated 3D aortic segmentation of 4D flow MRI for hemodynamic analysis using deep learning[J]. Magn Reson Med, 2020, 84(4): 2204-2218. DOI: 10.1002/mrm.28257.
[51]
LI S Q, ZHU M L, SUO S T, et al. Assessment of the hemodynamics of autogenous arteriovenous fistulas with 4D phase contrast-based flow quantification MRI in dialysis patients[J]. J Magn Reson Imaging, 2020, 51(4): 1272-1280. DOI: 10.1002/jmri.26936.
[52]
HA S Y, KANG Y, LEE H J, et al. Intracranial flow velocity quantification using non-contrast four-dimensional flow MRI: a prospective comparative study with transcranial Doppler ultrasound[J]. Diagnostics, 2021, 12(1): 23 [2024-01-01]. https://pubmed.ncbi.nlm.nih.gov/35054190/. DOI: 10.3390/diagnostics12010023.
[53]
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[J]. Eur J Gastroenterol Hepatol, 2013, 25(6): 669-675. DOI: 10.1097/MEG.0b013e32835e1297.

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