Top

Published in:

10-01-2024 | Hepatocellular Carcinoma | Review

Diagnostic performance of MRI for residual or recurrent hepatocellular carcinoma after locoregional treatment according to contrast agent type: a systematic review and meta‑analysis

Authors: Shuwei Zhou, Siyu Wang, Jian Xiang, Zhongyu Han, Weilang Wang, Shuhang Zhang, Noble Chibuike Opara, Shenghong Ju, Ying Cui, Yuan-Cheng Wang

Published in: Abdominal Radiology | Issue 2/2024

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

Available only for authorised users

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.29086CrossRefPubMed

EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. Journal of hepatology. 2018;69:182-236. https://doi.org/10.1016/j.jhep.2018.03.019CrossRef

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/s41575-020-00395-0CrossRef

Kulik L, El-Serag HB. Epidemiology and Management of Hepatocellular Carcinoma. Gastroenterology. 2019;156:477-91.e1. https://doi.org/10.1053/j.gastro.2018.08.065CrossRefPubMed

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/s00330-022-08720-8CrossRefPubMed

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/10.1159/000489790CrossRefPubMed

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.29913CrossRefPubMed

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/s12072-017-9799-9CrossRefPubMed

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.2018181494CrossRefPubMed

10.

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

11.

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/s00261-019-01968-7CrossRefPubMed

12.

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/10.7326/0003-4819-151-4-200908180-00136CrossRefPubMed

13.

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.13731CrossRefPubMed

14.

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.2017.12.014CrossRefPubMed

15.

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/10.7326/0003-4819-155-8-201110180-00009CrossRefPubMed

16.

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.1040CrossRefPubMed

17.

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.2005.01.016CrossRefPubMed

18.

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-yCrossRefPubMed

19.

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.21316CrossRefPubMed

20.

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

21.

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.21818CrossRefPubMed

22.

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.2010.05.015CrossRefPubMed

23.

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.2013.09.012CrossRef

24.

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

25.

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

26.

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.2019191581CrossRefPubMed

27.

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.2022.06.007CrossRefPubMed

28.

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.11.6844CrossRefPubMed

29.

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/s00330-019-06351-0CrossRefPubMed

30.

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.2020.04.003CrossRefPubMed

31.

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.2022.869993CrossRefPubMedPubMedCentral

32.

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.2022.100443CrossRefPubMed

33.

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.0000000000030875CrossRefPubMedPubMedCentral

34.

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.14131996CrossRefPubMed

35.

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/10.1159/000507370CrossRefPubMedPubMedCentral

36.

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.26540CrossRefPubMed

37.

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-yCrossRefPubMed

38.

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.2019.12.010CrossRefPubMed

39.

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.21689CrossRefPubMed

40.

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.2015150642CrossRefPubMed

41.

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.10091885CrossRefPubMed

42.

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.2019190010CrossRefPubMedPubMedCentral

43.

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.14.12986CrossRefPubMed

Title: Diagnostic performance of MRI for residual or recurrent hepatocellular carcinoma after locoregional treatment according to contrast agent type: a systematic review and meta‑analysis
Authors: Shuwei Zhou
Siyu Wang
Jian Xiang
Zhongyu Han
Weilang Wang
Shuhang Zhang
Noble Chibuike Opara
Shenghong Ju
Ying Cui
Yuan-Cheng Wang
Publication date: 10-01-2024
Publisher: Springer US
Keywords: Hepatocellular Carcinoma
Hepatocellular Carcinoma
Magnetic Resonance Imaging
Magnetic Resonance Imaging
Published in: Abdominal Radiology / Issue 2/2024
Print ISSN: 2366-004X
Electronic ISSN: 2366-0058
DOI: https://doi.org/10.1007/s00261-023-04143-1

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Graphical abstract

Please log in to get access to this content

Other articles of this Issue 2/2024

Intravoxel incoherent motion diffusion-weighted imaging for evaluating the pancreatic perfusion in cirrhotic patients

A meta-analysis of the performance of ultrasound, hepatobiliary scintigraphy, CT and MRI in the diagnosis of acute cholecystitis

Image quality optimization: dynamic contrast-enhanced MRI of the abdomen at 3T using a continuously acquired radial golden-angle compressed sensing acquisition

A multi-parameter intrahepatic cholangiocarcinoma scoring system based on modified contrast-enhanced ultrasound LI-RADS M criteria for differentiating intrahepatic cholangiocarcinoma from hepatocellular carcinoma

Validity of an automated screening Dixon technique for quantifying hepatic steatosis in living liver donors

Feasibility and safety of bipolar radiofrequency track cautery during percutaneous image-guided abdominal biopsy procedures

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials