Reviews

Advances in the evaluation of hepatic function by magnetic resonance imaging

Expand
  • Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University, Shanghai 200025, China

Received date: 2023-01-11

  Online published: 2023-08-31

Abstract

Quantitative assessment of liver function reserve is crucial for preoperative evaluation of patients with liver diseases. The use of magnetic resonance imaging (MRI) for quantitative assessment of liver function reserve has been limited by technical challenges for a long time; recently, MRI has developed and improved in various aspects, such as imaging methods, contrast agents, quantitative parameters, etc., leading to new techniques and applications for liver function quantification. Magnetic resonance elastography (MRE) can measure the biomechanical properties of liver tissue, and provide information on liver microstructure and function based on parameters such as vibration wave propagation speed in the liver; hepatobiliary-specific contrast-enhanced MRI can visualize the hepatocyte uptake and biliary excretion of contrast agent, thus revealing the functional distribution of the liver; T1ρ and diffusion-weighted imaging (DWI) can capture the local microenvironment features such as macromolecular components and water diffusion, and quantify liver function using these characteristics. Moreover, the latest technological advances such as three-dimensional shear wave elastography (3D-SWE) and hepatobiliary-specific contrast-enhanced MRI combined with T1 mapping quantification have further enhanced the performance of these examinations in liver function quantification. Compared with the commonly used clinical methods for liver function assessment, such as biochemical indicators, Child-Pugh score and indocyanine green test, the advantage of imaging techniques is that they can offer spatial distribution information of liver function reserve that is not available from clinical methods, providing new tools for preoperative evaluation of liver function reserve. This is expected to bridge the gap of current clinical examinations, assist in preoperative planning of liver surgery, and has promising development prospects.

Cite this article

CHEN Qian, LIN Huimin, YAN Fuhua . Advances in the evaluation of hepatic function by magnetic resonance imaging[J]. Journal of Diagnostics Concepts & Practice, 2023 , 22(02) : 190 -196 . DOI: 10.16150/j.1671-2870.2023.02.014

References

[1] 国家卫生健康委办公厅. 原发性肝癌诊疗指南(2022年版)[J]. 中华外科杂志, 2022, 60(4):273-309.
[1] General Office of the National Health Commission. Guidelines for diagnosis and treatment of primary liver cancer(The 2022 edition)[J]. Chin J Surg, 2022, 60(4):273-309.
[2] Zheng R, Zhang S, Zeng H, et al. Cancer incidence and mortality in China, 2016[J]. J Natl Cancer Center, 2022, 2(1):1-9.
[3] RAHNEMAI-AZAR A A, CLOYD J M, WEBER S M, et al. Update on Liver Failure Following Hepatic Resection: Strategies for Prediction and Avoidance of Post-operative Liver Insufficiency[J]. J Clin Transl Hepatol, 2018, 6(1): 97-104.
[4] VENKATESH S K, YIN M, EHMAN R L. Magnetic resonance elastography of liver: technique, analysis, and clinical applications[J]. J Magn Reson Imaging, 2013, 37(3):544-555.
[5] SINGH S, VENKATESH S K, WANG Z, et al. Diagnostic performance of magnetic resonance elastography in sta-ging liver fibrosis: a systematic review and meta-analysis of individual participant data[J]. Clin Gastroenterol Hepatol, 2015, 13(3):440-451,e6.
[6] KARIN D, KOYAMA Y, BRENNER D, et al. The characteristics of activated portal fibroblasts/myofibroblasts in liver fibrosis[J]. Differentiation, 2016, 92(3):84-92.
[7] VENKATESH S K, WELLS M L, MILLER F H, et al. Magnetic resonance elastography: beyond liver fibrosis-a case-based pictorial review[J]. Abdom Radiol (NY), 2018, 43(7):1590-1611.
[8] KUSAKA K, HARIHARA Y, TORZILLI G, et al. Objective evaluation of liver consistency to estimate hepatic fibrosis and functional reserve for hepatectomy[J]. J Am Coll Surg, 2000, 191(1):47-53.
[9] LI B, MIN J, LIANG W R, et al. Use of magnetic resonance elastography for assessing liver functional reserve: A clinical study[J]. World J Gastroenterol, 2015, 21(24):7522-7528.
[10] LIN H, WANG Y, ZHOU J, et al. Tomoelastography based on multifrequency MR elastography predicts liver function reserve in patients with hepatocellular carcinoma: a prospective study[J]. Insights Imaging, 2022, 13(1):95.
[11] HOFFMAN D H, AYOOLA A, NICKEL D, et al. MR elastography, T1 and T2 relaxometry of liver: role in noninvasive assessment of liver function and portal hypertension[J]. Abdom Radiol (NY), 2020, 45(9):2680-2687.
[12] HOODESHENAS S, YIN M, VENKATESH S K. Magnetic Resonance Elastography of Liver: Current Update[J]. Top Magn Reson Imaging, 2018, 27(5):319-333.
[13] LIU L, YOU Z, YU H, et al. Mechanotransduction-modulated fibrotic microniches reveal the contribution of angiogenesis in liver fibrosis[J]. Nat Mater, 2017, 16(12):1252-1261.
[14] ZHANG Y N, FOWLER K J, OZTURK A, et al. Liver fibrosis imaging: A clinical review of ultrasound and magnetic resonance elastography[J]. J Magn Reson Imaging, 2020, 51(1):25-42.
[15] WANG J, WANG Q, YU G, et al. Correlation Between Liver Stiffness Measured by Shear Wave Elastography and Child-Pugh Classification[J]. J Ultrasound Med, 2018, 37(9):2191-2199.
[16] HEUCKE N, WUENSCH T, MOHR J, et al. Non-invasive structure-function assessment of the liver by 2D time-harmonic elastography and the dynamic Liver MAximum capacity (LiMAx) test[J]. J Gastroenterol Hepatol, 2019, 34(9):1611-1619.
[17] IMAJO K, HONDA Y, KOBAYASHI T, et al. Direct Comparison of US and MR Elastography for Staging Liver Fibrosis in Patients With Nonalcoholic Fatty Liver Disease[J]. Clin Gastroenterol Hepatol, 2022, 20(4):908-917,e11.
[18] European Association for the Study of the Liver. EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis - 2021 update[J]. J Hepatol, 2021, 75(3):659-689.
[19] VAN BEERS B E, PASTOR C M, HUSSAIN H K. Primovist, Eovist: what to expect?[J]. J Hepatol, 2012, 57(2):421-429.
[20] FREITAS P S, JANICAS C, VEIGA J, et al. Imaging evaluation of the liver in oncology patients: A comparison of techniques[J]. World J Hepatol, 2021, 13(12):1936-1955.
[21] DAHLSTR?M N, PERSSON A, ALBIIN N, et al. Contrast-enhanced magnetic resonance cholangiography with Gd-BOPTA and Gd-EOB-DTPA in healthy subjects[J]. Acta Radiol, 2007, 48(4):362-368.
[22] YOON J H, LEE J M, PAEK M, et al. Quantitative assessment of hepatic function: modified look-locker inversion recovery (MOLLI) sequence for T1 mapping on Gd-EOB-DTPA-enhanced liver MR imaging[J]. Eur Radiol, 2016, 26(6):1775-1782.
[23] YOON J H, LEE J M, KANG H J, et al. Quantitative Assessment of Liver Function by Using Gadoxetic Acid-enhanced MRI: Hepatocyte Uptake Ratio[J]. Radiology, 2019, 290(1):125-133.
[24] SANDRASEGARAN K, CUI E, ELKADY R, et al. Can functional parameters from hepatobiliary phase of gadoxetate MRI predict clinical outcomes in patients with cirrhosis?[J]. Eur Radiol, 2018, 28(10):4215-4224.
[25] WIBMER A, PRUSA A M, NOLZ R, et al. Liver failure after major liver resection: risk assessment by using preoperative Gadoxetic acid-enhanced 3-T MR imaging[J]. Radiology, 2013, 269(3):777-786.
[26] LUO N, HUANG X, JI Y, et al. A functional liver ima-ging score for preoperative prediction of liver failure after hepatocellular carcinoma resection[J]. Eur Radiol, 2022, 32(8):5623-5632.
[27] SALERNO M, JANARDHANAN R, JIJI R S, et al. Comparison of methods for determining the partition coefficient of gadolinium in the myocardium using T1 mapping[J]. J Magn Reson Imaging, 2013, 38(1):217-224.
[28] DAHLQVIST LEINHARD O, DAHLSTR?M N, KIHLBERG J, et al. Quantifying differences in hepatic uptake of the liver specific contrast agents Gd-EOB-DTPA and Gd-BOPTA: a pilot study[J]. Eur Radiol, 2012, 22(3):642-653.
[29] HAIMERL M, VERLOH N, ZEMAN F, et al. Gd-EOB-DTPA-enhanced MRI for evaluation of liver function: Comparison between signal-intensity-based indices and T1 relaxometry[J]. Sci Rep, 2017, 7:43347.
[30] BESA C, BANE O, JAJAMOVICH G, et al. 3D T1 relaxo-metry pre and post gadoxetic acid injection for the assessment of liver cirrhosis and liver function[J]. Magn Reson Imaging, 2015, 33(9):1075-1082.
[31] GEISEL D, LüDEMANN L, HAMM B, et al. Imaging-Based Liver Function Tests--Past, Present and Future[J]. Rofo, 2015, 187(10):863-871.
[32] 王荣福, 庞小溪, 刘敏, 等. 99mTc-GSA肝受体显像在肝功能评估临床研究应用及进展[J]. 世界华人消化杂志, 2017, 25(21):1903-1909.
[32] WANG R F, PANG X X, LIU M, et al. Clinical application of 99mTc-GSA in assessment of liver function by hepatic receptor imaging[J]. World Chin J Digestol, 2017, 25(21):1903-1909.
[33] KUDO M, TODO A, IKEKUBO K, et al. Functional hepatic imaging with receptor-binding radiopharmaceutical: clinical potential as a measure of functioning hepatocyte mass[J]. Gastroenterol Jpn, 1991, 26(6):734-741.
[34] BENNINK R J, DINANT S, ERDOGAN D, et al. Preope-rative assessment of postoperative remnant liver function using hepatobiliary scintigraphy[J]. J Nucl Med, 2004, 45(6):965-971.
[35] ERDOGAN D, HEIJNEN B H, BENNINK R J, et al. Preoperative assessment of liver function: a comparison of 99mTc-Mebrofenin scintigraphy with indocyanine green clearance test[J]. Liver Int, 2004, 24(2):117-123.
[36] NAKAGAWA M, NAMIMOTO T, SHIMIZU K, et al. Measuring hepatic functional reserve using T1 mapping of Gd-EOB-DTPA enhanced 3T MR imaging: A preliminary study comparing with 99mTc GSA scintigraphy and signal intensity based parameters[J]. Eur J Radiol, 2017, 92:116-123.
[37] RONG P, FENG Z, GUO R, et al. CT-based estimation of liver function using arterial enhancement fraction in liver cirrhosis patients[J]. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2019, 44(5):469-476.
[38] DE GRAAF W, BENNINK R J, HEGER M, et al. Quantitative assessment of hepatic function during liver regeneration in a standardized rat model[J]. J Nucl Med, 2011, 52(2):294-302.
[39] NILSSON H, BLOMQVIST L, DOUGLAS L, et al. Gd-EOB-DTPA-enhanced MRI for the assessment of liver function and volume in liver cirrhosis[J]. Br J Radiol, 2013, 86(1026):20120653.
[40] HUANG M, SHEN S, CAI H, et al. Regional liver function analysis with gadoxetic acid-enhanced MRI and virtual hepatectomy: prediction of postoperative short-term outcomes for HCC[J]. Eur Radiol, 2021, 31(7):4720-4730.
[41] CLEMéNT O, MüHLER A, VEXLER V S, et al. Comparison of Gd-EOB-DTPA and Gd-DTPA for contrast-enhanced MR imaging of liver tumors[J]. J Magn Reson Ima-ging, 1993, 3(1):71-77.
[42] IMAI Y, KATAYAMA K, HORI M, et al. Prospective Comparison of Gd-EOB-DTPA-Enhanced MRI with Dynamic CT for Detecting Recurrence of HCC after Radiofrequency Ablation[J]. Liver Cancer, 2017, 6(4):349-359.
[43] UNAL E, IDILMAN I S, KAR?AALTINCABA M. Multiparametric or practical quantitative liver MRI: towards millisecond, fat fraction, kilopascal and function era[J]. Expert Rev Gastroenterol Hepatol, 2017, 11(2):167-182.
[44] DING Y, RAO S X, CHEN C, et al. Assessing liver function in patients with HBV-related HCC: a comparison of T1 mapping on Gd-EOB-DTPA-enhanced MR imaging with DWI[J]. Eur Radiol, 2015, 25(5):1392-1398.
[45] ZHANG J, GUO Y, TAN X, et al. MRI-based estimation of liver function by intravoxel incoherent motion diffusion-weighted imaging[J]. Magn Reson Imaging, 2016, 34(8):1220-1225.
[46] CHEN F, CHEN Y L, CHEN T W, et al. Liver lobe based intravoxel incoherent motion diffusion weighted imaging in hepatitis B related cirrhosis: Association with child-pugh class and esophageal and gastric fundic varices[J]. Medicine (Baltimore), 2020, 99(2):e18671.
[47] WANG L, REGATTE R R. T?ρ MRI of human musculoskeletal system[J]. J Magn Reson Imaging, 2015, 41(3): 586-600.
[48] RAUSCHER I, EIBER M, GANTER C, et al. Evaluation of T1ρ as a potential MR biomarker for liver cirrhosis: comparison of healthy control subjects and patients with liver cirrhosis[J]. Eur J Radiol, 2014, 83(6):900-904.
[49] TAKAYAMA Y, NISHIE A, ASAYAMA Y, et al. T1 ρ Relaxation of the liver: A potential biomarker of liver function[J]. J Magn Reson Imaging, 2015, 42(1):188-195.
[50] SINGH A, REDDY D, HARIS M, et al. T1ρ MRI of healthy and fibrotic human livers at 1.5 T[J]. J Transl Med, 2015, 13:292.
Outlines

/