LI<b>-</b>RADS in the diagnosis and treatment of hepatocellular carcinoma: current and future perspectives_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 JIANG Hanyu , CHEN Weixia

1. Department of Radiology, West China Hospital, Chengdu 610041, P. R. China;

Corresponding author：

JIANG Hanyu, Email: hanyu_jiang@foxmail.com

Keywords：

hepatocellular carcinoma; Liver Imaging Reporting and Data System; diagnosis; prognosis

DOI：

10.7507/1007-9424.202401064

Video：

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Primary liver cancer is the sixth most common malignancy and the third leading cause of cancer-related death worldwide, and hepatocellular carcinoma (HCC) constitutes the majority of primary liver cancer cases. The Liver Imaging Reporting and Data System (LI-RADS) was introduced to standardize the lexicon, acquisition, interpretation, reporting, and data collection of imaging results in patients at increased risk for HCC. LI-RADS allows effective categorization of focal liver lesions, and has been applied in the full clinical spectrum of HCC from diagnosis, biological behavior characterization, prognosis prediction, to treatment response assessment. This review aimed to summarize the recent applications of CT/MRI LI-RADS in the diagnosis, biological behavior characterization and prognosis prediction of HCC, discuss current challenges and shed light on potential future directions.

Citation： JIANG Hanyu, CHEN Weixia. LI-RADS in the diagnosis and treatment of hepatocellular carcinoma: current and future perspectives. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(3): 272-277. doi: 10.7507/1007-9424.202401064 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Zhou J, Sun H, Wang Z, et al. Guidelines for the Diagnosis and Treatment of Primary Liver Cancer (2022 Edition). Liver Cancer, 2023, 12(5): 405-444.
3.	Singal AG, Llovet JM, Yarchoan M, et al. AASLD Practice Guidance on prevention, diagnosis, and treatment of hepatocellular carcinoma. Hepatology, 2023, 78(6): 1922-1965.
4.	European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol, 2018, 69(1): 182-236.
5.	Reig M, Forner A, Rimola J, et al. BCLC strategy for prognosis prediction and treatment recommendation: The 2022 update. J Hepatol, 2022, 76(3): 681-693.
6.	Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6.
7.	Chernyak V, Fowler KJ, Kamaya A, et al. Liver Imaging Reporting and Data System (LI-RADS) Version 2018: Imaging of hepatocellular carcinoma in at-risk patients. Radiology, 2018, 289(3): 816-830.
8.	van der Pol CB, Lim CS, Sirlin CB, et al. Accuracy of the Liver Imaging Reporting and Data System in computed tomography and magnetic resonance image analysis of hepatocellular carcinoma or overall malignancy—A systematic review. Gastroenterology, 2019, 156(4): 976-986.
9.	Kim DH, Choi SH, Park SH, et al. Meta-analysis of the accuracy of Liver Imaging Reporting and Data System category 4 or 5 for diagnosing hepatocellular carcinoma. Gut, 2019, 68(9): 1719-1721.
10.	van der Pol CB, McInnes MDF, Salameh JP, et al. CT/MRI and CEUS LI-RADS major features association with hepatocellular carcinoma: individual patient data meta-analysis. Radiology, 2022, 302(2): 326-335.
11.	Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology, 2018, 68(2): 723-750.
12.	Ronot M, Fouque O, Esvan M, et al. Comparison of the accuracy of AASLD and LI-RADS criteria for the non-invasive diagnosis of HCC smaller than 3 cm. J Hepatol, 2018, 68(4): 715-723.
13.	Onyirioha K, Joshi S, Burkholder D, et al. Clinical outcomes of patients with suspicious (LI-RADS 4) liver observations. Clin Gastroenterol Hepatol, 2023, 21(6): 1649-1651.
14.	Arvind A, Joshi S, Zaki T, et al. Risk of hepatocellular carcinoma in patients with indeterminate (LI-RADS 3) liver observations. Clin Gastroenterol Hepatol, 2023, 21(4): 1091-1093.
15.	Terzi E, Iavarone M, Pompili M, et al. Contrast ultrasound LI-RADS LR-5 identifies hepatocellular carcinoma in cirrhosis in a multicenter restropective study of 1 006 nodules. J Hepatol, 2018, 68(3): 485-492.
16.	Min JH, Kim JM, Kim YK, et al. Magnetic resonance imaging with extracellular contrast detects hepatocellular carcinoma with greater accuracy than with gadoxetic acid or computed tomography. Clin Gastroenterol Hepatol, 2020, 18(9): 2091-2100.
17.	Min JH, Kim JM, Kim YK, et al. Prospective intraindividual comparison of magnetic resonance imaging with gadoxetic acid and extracellular contrast for diagnosis of hepatocellular carcinomas using the Liver Imaging Reporting and Data System. Hepatology, 2018, 68(6): 2254-2266.
18.	Yoon JH, Lee JM, Lee YJ, et al. Added value of sequentially performed gadoxetic acid-enhanced liver MRI for the diagnosis of small (10-19 mm) or atypical hepatic observations at contrast-enhanced CT: A prospective comparison. J Magn Reson Imaging, 2019, 49(2): 574-587.
19.	Moctezuma-Velázquez C, Lewis S, Lee K, et al. Non-invasive imaging criteria for the diagnosis of hepatocellular carcinoma in non-cirrhotic patients with chronic hepatitis B. JHEP Rep, 2021, 3(6): 100364.
20.	Kim BR, Lee JM, Lee DH, et al. Diagnostic performance of gadoxetic acid-enhanced liver MR imaging versus multidetector CT in the Detection of dysplastic nodules and early hepatocellular carcinoma. Radiology, 2017, 285(1): 134-146.
21.	Korean Liver Cancer Association (KLCA) and National Cancer Center (NCC) Korea. 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma. J Liver Cancer, 2023, 23(1): 1-120.
22.	Rimola J, Sapena V, Brancatelli G, et al. Reliability of extracellular contrast versus gadoxetic acid in assessing small liver lesions using liver imaging reporting and data system v. 2018 and European association for the study of the liver criteria. Hepatology, 2022, 76(5): 1318-1328.
23.	Hong CW, Chernyak V, Choi JY, et al. A multicenter assessment of interreader reliability of LI-RADS version 2018 for MRI and CT. Radiology, 2023, 307(5): e222855.
24.	Jiang H, Song B, Qin Y, et al. Data-driven modification of the LI-RADS major feature system on gadoxetate disodium-enhanced MRI: Toward better sensitivity and simplicity. J Magn Reson Imaging, 2022, 55(2): 493-506.
25.	Jiang H, Song B, Qin Y, et al. Modifying LI-RADS on gadoxetate disodium-enhanced MRI: A secondary analysis of a prospective observational study. J Magn Reson Imaging, 2022, 56(2): 399-412.
26.	Goins SM, Jiang H, van der Pol CB, et al. Individual participant data meta-analysis of LR-5 in LI-RADS version 2018 versus revised LI-RADS for hepatocellular carcinoma diagnosis. Radiology, 2023, 309(3): e231656.
27.	Goins SM, Jiang H, van der Pol CB, et al. Comparative performance of 2018 LI-RADS versus modified LIRADS (mLI-RADS): An individual participant data meta-analysis. J Magn Reson Imaging, 2023 Dec 1. doi: 10.1002/jmri.29167. Online ahead of print.
28.	Kwag M, Choi SH, Choi SJ, et al. Simplified LI-RADS for hepatocellular carcinoma diagnosis at gadoxetic acid-enhanced MRI. Radiology, 2022, 305(3): 614-622.
29.	Ronot M, Chernyak V, Burgoyne A, et al. Imaging to predict prognosis in hepatocellular carcinoma: current and future perspectives. Radiology, 2023, 307(3): e221429.
30.	Wei H, Yang T, Chen J, et al. Prognostic implications of CT/MRI LI-RADS in hepatocellular carcinoma: State of the art and future directions. Liver Int, 2022, 42(10): 2131-2144.
31.	Kang HJ, Kim H, Lee DH, et al. Gadoxetate-enhanced MRI features of proliferative hepatocellular carcinoma are prognostic after surgery. Radiology, 2021, 300(3): 572-582.
32.	Bao Y, Li JX, Zhou P, et al. Identifying proliferative hepatocellular carcinoma at pretreatment CT: implications for therapeutic outcomes after transarterial chemoembolization. Radiology, 2023, 308(2): e230457.
33.	Mulé S, Galletto Pregliasco A, Tenenhaus A, et al. Multiphase liver MRI for identifying the macrotrabecular-massive subtype of hepatocellular carcinoma. Radiology, 2020, 295(3): 562-571.
34.	Rhee H, Cho ES, Nahm JH, et al. Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol, 2021, 74(1): 109-121.
35.	Feng Z, Li H, Zhao H, et al. Preoperative CT for characterization of aggressive macrotrabecular-massive subtype and vessels that encapsulate tumor clusters pattern in hepatocellular carcinoma. Radiology, 2021, 300(1): 219-229.
36.	Cannella R, Dioguardi Burgio M, Beaufrère A, et al. Imaging features of histological subtypes of hepatocellular carcinoma: Implication for LI-RADS. JHEP Rep, 2021, 3(6): 100380.
37.	Choi SY, Kim SH, Park CK, et al. Imaging features of gadoxetic acid-enhanced and diffusion-weighted MR imaging for identifying cytokeratin 19-positive hepatocellular carcinoma: A retrospective observational study. Radiology, 2018, 286(3): 897-908.
38.	Hong SB, Choi SH, Kim SY, et al. MRI features for predicting microvascular invasion of hepatocellular carcinoma: A systematic review and meta-analysis. Liver Cancer, 2021, 10(2): 94-106.
39.	Lee S, Kang TW, Song KD, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg, 2021, 273(3): 564-571.
40.	Paisant A, Vilgrain V, Riou J, et al. Comparison of extracellular and hepatobiliary MR contrast agents for the diagnosis of small HCCs. J Hepatol, 2020, 72(5): 937-945.
41.	Jiang H, Wei H, Yang T, et al. VICT2 trait: prognostic alternative to peritumoral hepatobiliary phase hypointensity in HCC. Radiology, 2023, 307(2): e221835.
42.	Min JH, Lee MW, Park HS, et al. Interobserver variability and diagnostic performance of gadoxetic acid-enhanced MRI for Predicting microvascular invasion in hepatocellular carcinoma. Radiology, 2020, 297(3): 573-581.
43.	Jiang H, Yang C, Chen Y, et al. Development of a Model including MRI features for predicting advanced-stage recurrence of hepatocellular carcinoma after liver resection. Radiology, 2023, 309(2): e230527.
44.	Jiang H, Qin Y, Wei H, et al. Prognostic MRI features to predict postresection survivals for very early to intermediate stage hepatocellular carcinoma. Eur Radiol, 2023 Oct 23. doi: 10.1007/s00330-023-10279-x. Online ahead of print.
45.	Wei H, Fu F, Jiang H, et al. Development and validation of the OSASH score to predict overall survival of hepatocellular carcinoma after surgical resection: a dual-institutional study. Eur Radiol, 2023, 33(11): 7631-7645.
46.	Wei H, Jiang H, Qin Y, et al. Comparison of a preoperative MR-based recurrence risk score versus the postoperative score and four clinical staging systems in hepatocellular carcinoma: a retrospective cohort study. Eur Radiol, 2022, 32(11): 7578-7589.
47.	Wei H, Jiang H, Zheng T, et al. LI-RADS category 5 hepatocellular carcinoma: preoperative gadoxetic acid-enhanced MRI for early recurrence risk stratification after curative resection. Eur Radiol, 2021, 31(4): 2289-2302.

1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Zhou J, Sun H, Wang Z, et al. Guidelines for the Diagnosis and Treatment of Primary Liver Cancer (2022 Edition). Liver Cancer, 2023, 12(5): 405-444.
3. Singal AG, Llovet JM, Yarchoan M, et al. AASLD Practice Guidance on prevention, diagnosis, and treatment of hepatocellular carcinoma. Hepatology, 2023, 78(6): 1922-1965.
4. European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol, 2018, 69(1): 182-236.
5. Reig M, Forner A, Rimola J, et al. BCLC strategy for prognosis prediction and treatment recommendation: The 2022 update. J Hepatol, 2022, 76(3): 681-693.
6. Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6.
7. Chernyak V, Fowler KJ, Kamaya A, et al. Liver Imaging Reporting and Data System (LI-RADS) Version 2018: Imaging of hepatocellular carcinoma in at-risk patients. Radiology, 2018, 289(3): 816-830.
8. van der Pol CB, Lim CS, Sirlin CB, et al. Accuracy of the Liver Imaging Reporting and Data System in computed tomography and magnetic resonance image analysis of hepatocellular carcinoma or overall malignancy—A systematic review. Gastroenterology, 2019, 156(4): 976-986.
9. Kim DH, Choi SH, Park SH, et al. Meta-analysis of the accuracy of Liver Imaging Reporting and Data System category 4 or 5 for diagnosing hepatocellular carcinoma. Gut, 2019, 68(9): 1719-1721.
10. van der Pol CB, McInnes MDF, Salameh JP, et al. CT/MRI and CEUS LI-RADS major features association with hepatocellular carcinoma: individual patient data meta-analysis. Radiology, 2022, 302(2): 326-335.
11. Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology, 2018, 68(2): 723-750.
12. Ronot M, Fouque O, Esvan M, et al. Comparison of the accuracy of AASLD and LI-RADS criteria for the non-invasive diagnosis of HCC smaller than 3 cm. J Hepatol, 2018, 68(4): 715-723.
13. Onyirioha K, Joshi S, Burkholder D, et al. Clinical outcomes of patients with suspicious (LI-RADS 4) liver observations. Clin Gastroenterol Hepatol, 2023, 21(6): 1649-1651.
14. Arvind A, Joshi S, Zaki T, et al. Risk of hepatocellular carcinoma in patients with indeterminate (LI-RADS 3) liver observations. Clin Gastroenterol Hepatol, 2023, 21(4): 1091-1093.
15. Terzi E, Iavarone M, Pompili M, et al. Contrast ultrasound LI-RADS LR-5 identifies hepatocellular carcinoma in cirrhosis in a multicenter restropective study of 1 006 nodules. J Hepatol, 2018, 68(3): 485-492.
16. Min JH, Kim JM, Kim YK, et al. Magnetic resonance imaging with extracellular contrast detects hepatocellular carcinoma with greater accuracy than with gadoxetic acid or computed tomography. Clin Gastroenterol Hepatol, 2020, 18(9): 2091-2100.
17. Min JH, Kim JM, Kim YK, et al. Prospective intraindividual comparison of magnetic resonance imaging with gadoxetic acid and extracellular contrast for diagnosis of hepatocellular carcinomas using the Liver Imaging Reporting and Data System. Hepatology, 2018, 68(6): 2254-2266.
18. Yoon JH, Lee JM, Lee YJ, et al. Added value of sequentially performed gadoxetic acid-enhanced liver MRI for the diagnosis of small (10-19 mm) or atypical hepatic observations at contrast-enhanced CT: A prospective comparison. J Magn Reson Imaging, 2019, 49(2): 574-587.
19. Moctezuma-Velázquez C, Lewis S, Lee K, et al. Non-invasive imaging criteria for the diagnosis of hepatocellular carcinoma in non-cirrhotic patients with chronic hepatitis B. JHEP Rep, 2021, 3(6): 100364.
20. Kim BR, Lee JM, Lee DH, et al. Diagnostic performance of gadoxetic acid-enhanced liver MR imaging versus multidetector CT in the Detection of dysplastic nodules and early hepatocellular carcinoma. Radiology, 2017, 285(1): 134-146.
21. Korean Liver Cancer Association (KLCA) and National Cancer Center (NCC) Korea. 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma. J Liver Cancer, 2023, 23(1): 1-120.
22. Rimola J, Sapena V, Brancatelli G, et al. Reliability of extracellular contrast versus gadoxetic acid in assessing small liver lesions using liver imaging reporting and data system v. 2018 and European association for the study of the liver criteria. Hepatology, 2022, 76(5): 1318-1328.
23. Hong CW, Chernyak V, Choi JY, et al. A multicenter assessment of interreader reliability of LI-RADS version 2018 for MRI and CT. Radiology, 2023, 307(5): e222855.
24. Jiang H, Song B, Qin Y, et al. Data-driven modification of the LI-RADS major feature system on gadoxetate disodium-enhanced MRI: Toward better sensitivity and simplicity. J Magn Reson Imaging, 2022, 55(2): 493-506.
25. Jiang H, Song B, Qin Y, et al. Modifying LI-RADS on gadoxetate disodium-enhanced MRI: A secondary analysis of a prospective observational study. J Magn Reson Imaging, 2022, 56(2): 399-412.
26. Goins SM, Jiang H, van der Pol CB, et al. Individual participant data meta-analysis of LR-5 in LI-RADS version 2018 versus revised LI-RADS for hepatocellular carcinoma diagnosis. Radiology, 2023, 309(3): e231656.
27. Goins SM, Jiang H, van der Pol CB, et al. Comparative performance of 2018 LI-RADS versus modified LIRADS (mLI-RADS): An individual participant data meta-analysis. J Magn Reson Imaging, 2023 Dec 1. doi: 10.1002/jmri.29167. Online ahead of print.
28. Kwag M, Choi SH, Choi SJ, et al. Simplified LI-RADS for hepatocellular carcinoma diagnosis at gadoxetic acid-enhanced MRI. Radiology, 2022, 305(3): 614-622.
29. Ronot M, Chernyak V, Burgoyne A, et al. Imaging to predict prognosis in hepatocellular carcinoma: current and future perspectives. Radiology, 2023, 307(3): e221429.
30. Wei H, Yang T, Chen J, et al. Prognostic implications of CT/MRI LI-RADS in hepatocellular carcinoma: State of the art and future directions. Liver Int, 2022, 42(10): 2131-2144.
31. Kang HJ, Kim H, Lee DH, et al. Gadoxetate-enhanced MRI features of proliferative hepatocellular carcinoma are prognostic after surgery. Radiology, 2021, 300(3): 572-582.
32. Bao Y, Li JX, Zhou P, et al. Identifying proliferative hepatocellular carcinoma at pretreatment CT: implications for therapeutic outcomes after transarterial chemoembolization. Radiology, 2023, 308(2): e230457.
33. Mulé S, Galletto Pregliasco A, Tenenhaus A, et al. Multiphase liver MRI for identifying the macrotrabecular-massive subtype of hepatocellular carcinoma. Radiology, 2020, 295(3): 562-571.
34. Rhee H, Cho ES, Nahm JH, et al. Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol, 2021, 74(1): 109-121.
35. Feng Z, Li H, Zhao H, et al. Preoperative CT for characterization of aggressive macrotrabecular-massive subtype and vessels that encapsulate tumor clusters pattern in hepatocellular carcinoma. Radiology, 2021, 300(1): 219-229.
36. Cannella R, Dioguardi Burgio M, Beaufrère A, et al. Imaging features of histological subtypes of hepatocellular carcinoma: Implication for LI-RADS. JHEP Rep, 2021, 3(6): 100380.
37. Choi SY, Kim SH, Park CK, et al. Imaging features of gadoxetic acid-enhanced and diffusion-weighted MR imaging for identifying cytokeratin 19-positive hepatocellular carcinoma: A retrospective observational study. Radiology, 2018, 286(3): 897-908.
38. Hong SB, Choi SH, Kim SY, et al. MRI features for predicting microvascular invasion of hepatocellular carcinoma: A systematic review and meta-analysis. Liver Cancer, 2021, 10(2): 94-106.
39. Lee S, Kang TW, Song KD, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg, 2021, 273(3): 564-571.
40. Paisant A, Vilgrain V, Riou J, et al. Comparison of extracellular and hepatobiliary MR contrast agents for the diagnosis of small HCCs. J Hepatol, 2020, 72(5): 937-945.
41. Jiang H, Wei H, Yang T, et al. VICT2 trait: prognostic alternative to peritumoral hepatobiliary phase hypointensity in HCC. Radiology, 2023, 307(2): e221835.
42. Min JH, Lee MW, Park HS, et al. Interobserver variability and diagnostic performance of gadoxetic acid-enhanced MRI for Predicting microvascular invasion in hepatocellular carcinoma. Radiology, 2020, 297(3): 573-581.
43. Jiang H, Yang C, Chen Y, et al. Development of a Model including MRI features for predicting advanced-stage recurrence of hepatocellular carcinoma after liver resection. Radiology, 2023, 309(2): e230527.
44. Jiang H, Qin Y, Wei H, et al. Prognostic MRI features to predict postresection survivals for very early to intermediate stage hepatocellular carcinoma. Eur Radiol, 2023 Oct 23. doi: 10.1007/s00330-023-10279-x. Online ahead of print.
45. Wei H, Fu F, Jiang H, et al. Development and validation of the OSASH score to predict overall survival of hepatocellular carcinoma after surgical resection: a dual-institutional study. Eur Radiol, 2023, 33(11): 7631-7645.
46. Wei H, Jiang H, Qin Y, et al. Comparison of a preoperative MR-based recurrence risk score versus the postoperative score and four clinical staging systems in hepatocellular carcinoma: a retrospective cohort study. Eur Radiol, 2022, 32(11): 7578-7589.
47. Wei H, Jiang H, Zheng T, et al. LI-RADS category 5 hepatocellular carcinoma: preoperative gadoxetic acid-enhanced MRI for early recurrence risk stratification after curative resection. Eur Radiol, 2021, 31(4): 2289-2302.

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LI-RADS in the diagnosis and treatment of hepatocellular carcinoma: current and future perspectives

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