Abstract
Purpose
The ideal contrast agent for imaging patients with hepatocellular carcinoma (HCC) following locoregional therapies (LRT) remains uncertain. We conducted a meta-analysis to assess the diagnostic performance of magnetic resonance imaging with extracellular contrast agent (ECA-MRI) and hepatobiliary agent (EOB-MRI) in detecting residual or recurrence HCC following LRT.
Methods
Original studies comparing the diagnostic performance of ECA-MRI and EOB-MRI were systematically identified through comprehensive searches in PubMed, EMBASE, Cochrane Library and Web of Science databases. The pooled sensitivity and specificity of ECA-MRI and EOB-MRI were calculated using a bivariate-random-effects model. Subgroup-analyses were conducted to compare the diagnostic performance of ECA-MRI and EOB-MRI according to different variables. Meta-regression analysis was employed to explore potential sources of study heterogeneity.
Results
A total of 15 eligible studies encompassing 803 patients and 1018 lesions were included. Comparative analysis revealed no significant difference between ECA-MRI and EOB-MRI in the overall pooled sensitivity (87% vs. 79%) and specificity (92% vs. 96%) for the detection of residual or recurrent HCC after LRT (P = 0.41), with comparable areas under the HSROC of 0.95 and 0.92. Subgroup analyses indicated no significant diagnostic performance differences between ECA-MRI and EOB-MRI according to study design, type of LRT, most common etiology of liver disease, baseline lesion size, time of post-treated examination and MRI field strength (All P > 0.05).
Conclusion
ECA-MRI exhibited overall comparable diagnostic performance to EOB-MRI in assessing residual or recurrent HCC after LRT.
Graphical abstract
Similar content being viewed by others
Abbreviations
- HCC:
-
Hepatocellular carcinoma
- LRT:
-
Locoregional therapies
- ECA:
-
Extracellular contrast agent
- EOB:
-
Hepatobiliary agent
- TACE:
-
Transarterial chemoembolization
- HBP:
-
Hepatobiliary phase
- LI-RADS:
-
Liver Reporting and Data System
- DSA:
-
Digital subtraction angiography
- HSROC:
-
Hierarchical summary receiver operating characteristic
- AUC:
-
Area under the curve
- RFA:
-
Radiofrequency ablation
- BCLC:
-
Barcelona Clinic Liver Cancer
References
Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, Zhu AX, Murad MH, Marrero JA. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology (Baltimore, Md). 2018;67:358-80. https://doi.org/10.1002/hep.29086
EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. Journal of hepatology. 2018;69:182-236. https://doi.org/10.1016/j.jhep.2018.03.019
Llovet JM, De Baere T, Kulik L, Haber PK, Greten TF, Meyer T, Lencioni R. Locoregional therapies in the era of molecular and immune treatments for hepatocellular carcinoma. Nature reviews Gastroenterology & hepatology. 2021;18:293-313. https://doi.org/10.1038/s41575-020-00395-0
Kulik L, El-Serag HB. Epidemiology and Management of Hepatocellular Carcinoma. Gastroenterology. 2019;156:477-91.e1. https://doi.org/10.1053/j.gastro.2018.08.065
Youn SY, Kim B, Kim DH, Choi HJ, Sung PS, Choi JI. Liver Imaging-Reporting and Data System treatment response algorithm predicts postsurgical recurrence in locoregional therapy-treated hepatocellular carcinoma. European radiology. 2022;32:6270-80. https://doi.org/10.1007/s00330-022-08720-8
Chien SC, Chen CY, Cheng PN, Liu YS, Cheng HC, Chuang CH, Chang TT, Chiu HC, Lin YJ, Chiu YC. Combined Transarterial Embolization/Chemoembolization-Based Locoregional Treatment with Sorafenib Prolongs the Survival in Patients with Advanced Hepatocellular Carcinoma and Preserved Liver Function: A Propensity Score Matching Study. Liver cancer. 2019;8:186-202. https://doi.org/10.1159/000489790
Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, Roberts LR, Heimbach JK. Diagnosis, Staging, and Management of Hepatocellular Carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology (Baltimore, Md). 2018;68:723-50. https://doi.org/10.1002/hep.29913
Omata M, Cheng AL, Kokudo N, Kudo M, Lee JM, Jia J, Tateishi R, Han KH, Chawla YK, Shiina S, Jafri W, Payawal DA, Ohki T, Ogasawara S, Chen PJ, Lesmana CRA, Lesmana LA, Gani RA, Obi S, Dokmeci AK, Sarin SK. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatology international. 2017;11:317-70. https://doi.org/10.1007/s12072-017-9799-9
Chernyak V, Fowler KJ, Kamaya A, Kielar AZ, Elsayes KM, Bashir MR, Kono Y, Do RK, Mitchell DG, Singal AG, Tang A, Sirlin CB. Liver Imaging Reporting and Data System (LI-RADS) Version 2018: Imaging of Hepatocellular Carcinoma in At-Risk Patients. Radiology. 2018;289:816-30. https://doi.org/10.1148/radiol.2018181494
Rimola J, Davenport MS, Liu PS, Brown T, Marrero JA, McKenna BJ, Hussain HK. Diagnostic accuracy of MRI with extracellular vs. hepatobiliary contrast material for detection of residual hepatocellular carcinoma after locoregional treatment. Abdominal radiology (New York). 2019;44:549–58. https://doi.org/10.1007/s00261-018-1775-x
Yim JH, Kim YK, Min JH, Lee J, Kang TW, Lee SJ. Diagnosis of recurrent HCC: intraindividual comparison of gadoxetic acid MRI and extracellular contrast-enhanced MRI. Abdominal radiology (New York). 2019;44:2366-76. https://doi.org/10.1007/s00261-019-01968-7
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Annals of internal medicine. 2009;151:W65-94. https://doi.org/10.7326/0003-4819-151-4-200908180-00136
Jeon MY, Lee HW, Kim BK, Park JY, Kim DY, Ahn SH, Han KH, Baek SE, Kim HS, Kim SU, Park MS. Reproducibility of European Association for the Study of the Liver criteria and modified Response Evaluation Criteria in Solid Tumors in patients treated with sorafenib. Liver international : official journal of the International Association for the Study of the Liver. 2018;38:1655-63. https://doi.org/10.1111/liv.13731
Ronot M, Fouque O, Esvan M, Lebigot J, Aubé C, Vilgrain V. Comparison of the accuracy of AASLD and LI-RADS criteria for the non-invasive diagnosis of HCC smaller than 3 cm. Journal of hepatology. 2018;68:715-23. https://doi.org/10.1016/j.jhep.2017.12.014
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Annals of internal medicine. 2011;155:529-36. https://doi.org/10.7326/0003-4819-155-8-201110180-00009
van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Statistics in medicine. 2002;21:589-624. https://doi.org/10.1002/sim.1040
Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. Journal of clinical epidemiology. 2005;58:882-93. https://doi.org/10.1016/j.jclinepi.2005.01.016
Bolog N, Pfammatter T, Müllhaupt B, Andreisek G, Weishaupt D. Double-contrast magnetic resonance imaging of hepatocellular carcinoma after transarterial chemoembolization. Abdominal imaging. 2008;33:313-23. https://doi.org/10.1007/s00261-007-9244-y
Goshima S, Kanematsu M, Kondo H, Yokoyama R, Tsuge Y, Shiratori Y, Onozuka M, Moriyama N. Evaluating local hepatocellular carcinoma recurrence post-transcatheter arterial chemoembolization: is diffusion-weighted MRI reliable as an indicator? Journal of magnetic resonance imaging : JMRI. 2008;27:834-9. https://doi.org/10.1002/jmri.21316
Jin W, Qing D, Yun-Jing X, Bin S. Dynamic contrast-enhanced VIBE sequence at 3.0T MR:assessment of therapeutic effect of transcatheter arterial chemoembolization for hepatocellucer carcinoma. Chinese Journal of Interventional Imaging and Therapy. 2008;5:115–8. https://doi.org/10.1672/chin.jIntervim.2008.02.015
Yu JS, Kim JH, Chung JJ, Kim KW. Added value of diffusion-weighted imaging in the MRI assessment of perilesional tumor recurrence after chemoembolization of hepatocellular carcinomas. Journal of magnetic resonance imaging : JMRI. 2009;30:153-60. https://doi.org/10.1002/jmri.21818
Kalb B, Chamsuddin A, Nazzal L, Sharma P, Martin DR. Chemoembolization follow-up of hepatocellular carcinoma with MR imaging: usefulness of evaluating enhancement features on one-month posttherapy MR imaging for predicting residual disease. Journal of vascular and interventional radiology : JVIR. 2010;21:1396-404. https://doi.org/10.1016/j.jvir.2010.05.015
Osama RM, Abdelmaksoud AHK, El Tatawy SAM, Nabeel MM, Metwally LIA. Role of dynamic contrast-enhanced and diffusion weighted MRI in evaluation of necrosis of hepatocellular carcinoma after chemoembolization. Egyptian Journal of Radiology and Nuclear Medicine. 2013;44:737–46. https://doi.org/10.1016/j.ejrnm.2013.09.012
Ebeed AE, Romeih EH, Refat MM, Yossef MH. Role of dynamic contrast-enhanced and diffusion weighted MRI in evaluation of hepatocellular carcinoma after chemoembolization. Egyptian Journal of Radiology and Nuclear Medicine. 2017;48. https://doi.org/10.1016/j.ejrnm.2017.06.006
Saleh TY, Bahig S, Shebrya N, Ahmed AY. Value of dynamic and DWI MRI in evaluation of HCC viability after TACE via LI-RADS v2018 diagnostic algorithm. Egyptian Journal of Radiology and Nuclear Medicine. 2019;50. https://doi.org/10.1186/s43055-019-0120-x
Chaudhry M, McGinty KA, Mervak B, Lerebours R, Li C, Shropshire E, Ronald J, Commander L, Hertel J, Luo S, Bashir MR, Burke LMB. The LI-RADS Version 2018 MRI Treatment Response Algorithm: Evaluation of Ablated Hepatocellular Carcinoma. Radiology. 2020;294:320-6. https://doi.org/10.1148/radiol.2019191581
Abdelrahman AS, Ekladious MEY, Badran EM, Madkour SS. Liver imaging reporting and data system (LI-RADS) v2018: Reliability and agreement for assessing hepatocellular carcinoma locoregional treatment response. Diagnostic and interventional imaging. 2022;103:524-34. https://doi.org/10.1016/j.diii.2022.06.007
Watanabe H, Kanematsu M, Goshima S, Yoshida M, Kawada H, Kondo H, Moriyama N. Is gadoxetate disodium-enhanced MRI useful for detecting local recurrence of hepatocellular carcinoma after radiofrequency ablation therapy? AJR American journal of roentgenology. 2012;198:589-95. https://doi.org/10.2214/ajr.11.6844
Rimola J, Forner A, Sapena V, Llarch N, Darnell A, Díaz A, García-Criado A, Bianchi L, Vilana R, Díaz-González Á, Ayuso C, Bruix J, Reig M. Performance of gadoxetic acid MRI and diffusion-weighted imaging for the diagnosis of early recurrence of hepatocellular carcinoma. European radiology. 2020;30:186-94. https://doi.org/10.1007/s00330-019-06351-0
Liu HF, Xu YS, Liu Z, Che KY, Sheng Y, Ding JL, Zhang JG, Lei JQ, Xing W. Value of Gd-EOB-DTPA-Enhanced MRI and Diffusion-Weighted Imaging in Detecting Residual Hepatocellular Carcinoma After Drug-Eluting Bead Transarterial Chemoembolization. Academic radiology. 2021;28:790-8. https://doi.org/10.1016/j.acra.2020.04.003
He Q, Yang J, Jin Y. Development and Validation of TACE Refractoriness-Related Diagnostic and Prognostic Scores and Characterization of Tumor Microenvironment Infiltration in Hepatocellular Carcinoma. Frontiers in immunology. 2022;13:869993. https://doi.org/10.3389/fimmu.2022.869993
Nam D, Chapiro J, Paradis V, Seraphin TP, Kather JN. Artificial intelligence in liver diseases: Improving diagnostics, prognostics and response prediction. JHEP reports : innovation in hepatology. 2022;4:100443. https://doi.org/10.1016/j.jhepr.2022.100443
Lee SW, Yen CL, Cheng YC, Shun Yang S, Lee TY. The radiological prognostic factors of transcatheter arterial chemoembolization to hepatocellular carcinoma. Medicine. 2022;101:e30875. https://doi.org/10.1097/md.0000000000030875
Yu MH, Kim JH, Yoon JH, Kim HC, Chung JW, Han JK, Choi BI. Small (≤1-cm) hepatocellular carcinoma: diagnostic performance and imaging features at gadoxetic acid-enhanced MR imaging. Radiology. 2014;271:748-60. https://doi.org/10.1148/radiol.14131996
Kudo M, Han KH, Ye SL, Zhou J, Huang YH, Lin SM, Wang CK, Ikeda M, Chan SL, Choo SP, Miyayama S, Cheng AL. A Changing Paradigm for the Treatment of Intermediate-Stage Hepatocellular Carcinoma: Asia-Pacific Primary Liver Cancer Expert Consensus Statements. Liver cancer. 2020;9:245-60. https://doi.org/10.1159/000507370
Chernyak V, Fowler KJ, Heiken JP, Sirlin CB. Use of gadoxetate disodium in patients with chronic liver disease and its implications for liver imaging reporting and data system (LI-RADS). Journal of magnetic resonance imaging : JMRI. 2019;49:1236-52. https://doi.org/10.1002/jmri.26540
Zhang W, Wang X, Miao Y, Hu C, Zhao W. Liver function correlates with liver-to-portal vein contrast ratio during the hepatobiliary phase with Gd-EOB-DTPA-enhanced MR at 3 Tesla. Abdominal radiology (New York). 2018;43:2262-9. https://doi.org/10.1007/s00261-018-1462-y
Min JH, Kim JM, Kim YK, Cha DI, Kang TW, Kim H, Choi GS, Choi SY, Ahn S. Magnetic Resonance Imaging With Extracellular Contrast Detects Hepatocellular Carcinoma With Greater Accuracy Than With Gadoxetic Acid or Computed Tomography. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. 2020;18:2091-100.e7. https://doi.org/10.1016/j.cgh.2019.12.010
Tamada T, Ito K, Sone T, Yamamoto A, Yoshida K, Kakuba K, Tanimoto D, Higashi H, Yamashita T. Dynamic contrast-enhanced magnetic resonance imaging of abdominal solid organ and major vessel: comparison of enhancement effect between Gd-EOB-DTPA and Gd-DTPA. Journal of magnetic resonance imaging : JMRI. 2009;29:636-40. https://doi.org/10.1002/jmri.21689
Motosugi U, Bannas P, Bookwalter CA, Sano K, Reeder SB. An Investigation of Transient Severe Motion Related to Gadoxetic Acid-enhanced MR Imaging. Radiology. 2016;279:93-102. https://doi.org/10.1148/radiol.2015150642
Motosugi U, Ichikawa T, Sou H, Sano K, Tominaga L, Muhi A, Araki T. Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging. Radiology. 2010;256:151-8. https://doi.org/10.1148/radiol.10091885
Brunsing RL, Chen DH, Schlein A, Wolfson T, Gamst A, Mamidipalli A, Vietti Violi N, Marks RM, Taouli B, Loomba R, Kono Y, Sirlin CB. Gadoxetate-enhanced Abbreviated MRI for Hepatocellular Carcinoma Surveillance: Preliminary Experience. Radiology Imaging cancer. 2019;1:e190010. https://doi.org/10.1148/rycan.2019190010
Marks RM, Ryan A, Heba ER, Tang A, Wolfson TJ, Gamst AC, Sirlin CB, Bashir MR. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. AJR American journal of roentgenology. 2015;204:527-35. https://doi.org/10.2214/ajr.14.12986
Funding
This work was supported by National Natural Science Foundation of China (NSFC, Grant Nos 82271978 and 81801669) and the Key Research and Development Program of Jiangsu Province (BE2020717).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Informed consent
Written informed consent was not required for this study because this is a systematic review. Institutional Review Board approval was not required because this is a systematic review.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhou, S., Wang, S., Xiang, J. et al. Diagnostic performance of MRI for residual or recurrent hepatocellular carcinoma after locoregional treatment according to contrast agent type: a systematic review and meta‑analysis. Abdom Radiol 49, 471–483 (2024). https://doi.org/10.1007/s00261-023-04143-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00261-023-04143-1