DOI QR코드

DOI QR Code

Prognostication of Hepatocellular Carcinoma Using Artificial Intelligence

  • Subin Heo (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Hyo Jung Park (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Seung Soo Lee (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2024.01.18
  • Accepted : 2024.03.31
  • Published : 2024.06.01

Abstract

Hepatocellular carcinoma (HCC) is a biologically heterogeneous tumor characterized by varying degrees of aggressiveness. The current treatment strategy for HCC is predominantly determined by the overall tumor burden, and does not address the diverse prognoses of patients with HCC owing to its heterogeneity. Therefore, the prognostication of HCC using imaging data is crucial for optimizing patient management. Although some radiologic features have been demonstrated to be indicative of the biologic behavior of HCC, traditional radiologic methods for HCC prognostication are based on visually-assessed prognostic findings, and are limited by subjectivity and inter-observer variability. Consequently, artificial intelligence has emerged as a promising method for image-based prognostication of HCC. Unlike traditional radiologic image analysis, artificial intelligence based on radiomics or deep learning utilizes numerous image-derived quantitative features, potentially offering an objective, detailed, and comprehensive analysis of the tumor phenotypes. Artificial intelligence, particularly radiomics has displayed potential in a variety of applications, including the prediction of microvascular invasion, recurrence risk after locoregional treatment, and response to systemic therapy. This review highlights the potential value of artificial intelligence in the prognostication of HCC as well as its limitations and future prospects.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (NRF-2020R1F1A1048826).

References

  1. European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182-236  https://doi.org/10.1016/j.jhep.2018.03.019
  2. Ronot M, Chernyak V, Burgoyne A, Chang J, Jiang H, Bashir M, et al. Imaging to predict prognosis in hepatocellular carcinoma: current and future perspectives. Radiology 2023;307:e221429 
  3. Renne SL, Woo HY, Allegra S, Rudini N, Yano H, Donadon M, et al. Vessels encapsulating tumor clusters (VETC) is a powerful predictor of aggressive hepatocellular carcinoma. Hepatology 2020;71:183-195  https://doi.org/10.1002/hep.30814
  4. Calderaro J, Ziol M, Paradis V, Zucman-Rossi J. Molecular and histological correlations in liver cancer. J Hepatol 2019;71:616-630  https://doi.org/10.1016/j.jhep.2019.06.001
  5. Lee S, Kim SH, Lee JE, Sinn DH, Park CK. Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. J Hepatol 2017;67:526-534  https://doi.org/10.1016/j.jhep.2017.04.024
  6. Cho ES, Choi JY. MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol 2015;16:449-464  https://doi.org/10.3348/kjr.2015.16.3.449
  7. Low HM, Lee JM, Tan CH. Prognosis prediction of hepatocellular carcinoma based on magnetic resonance imaging features. Korean J Radiol 2023;24:660-667  https://doi.org/10.3348/kjr.2023.0168
  8. Choi SH, Lee SS, Park SH, Kim KM, Yu E, Park Y, et al. LI-RADS classification and prognosis of primary liver cancers at gadoxetic acid-enhanced MRI. Radiology 2019;290:388-397  https://doi.org/10.1148/radiol.2018181290
  9. Davenport MS, Khalatbari S, Liu PS, Maturen KE, Kaza RK, Wasnik AP, et al. Repeatability of diagnostic features and scoring systems for hepatocellular carcinoma by using MR imaging. Radiology 2014;272:132-142  https://doi.org/10.1148/radiol.14131963
  10. Park HJ, Park B, Lee SS. Radiomics and deep learning: hepatic applications. Korean J Radiol 2020;21:387-401  https://doi.org/10.3348/kjr.2019.0752
  11. Park JE, Park SY, Kim HJ, Kim HS. Reproducibility and generalizability in radiomics modeling: possible strategies in radiologic and statistical perspectives. Korean J Radiol 2019;20:1124-1137  https://doi.org/10.3348/kjr.2018.0070
  12. Bo Z, Chen B, Zhao Z, He Q, Mao Y, Yang Y, et al. Prediction of response to lenvatinib monotherapy for unresectable hepatocellular carcinoma by machine learning radiomics: a multicenter cohort study. Clin Cancer Res 2023;29:1730-1740 
  13. Chen S, Feng S, Wei J, Liu F, Li B, Li X, et al. Pretreatment prediction of immunoscore in hepatocellular cancer: a radiomics-based clinical model based on Gd-EOB-DTPA-enhanced MRI imaging. Eur Radiol 2019;29:4177-4187  https://doi.org/10.1007/s00330-018-5986-x
  14. Feng Z, Li H, Liu Q, Duan J, Zhou W, Yu X, et al. CT radiomics to predict macrotrabecular-massive subtype and immune status in hepatocellular carcinoma. Radiology 2023;307:e221291 
  15. Guo D, Gu D, Wang H, Wei J, Wang Z, Hao X, et al. Radiomics analysis enables recurrence prediction for hepatocellular carcinoma after liver transplantation. Eur J Radiol 2019;117:33-40  https://doi.org/10.1016/j.ejrad.2019.05.010
  16. Ji GW, Zhu FP, Xu Q, Wang K, Wu MY, Tang WW, et al. Radiomic features at contrast-enhanced CT predict recurrence in early stage hepatocellular carcinoma: a multi-institutional study. Radiology 2020;294:568-579  https://doi.org/10.1148/radiol.2020191470
  17. Kim S, Shin J, Kim DY, Choi GH, Kim MJ, Choi JY. Radiomics on gadoxetic acid-enhanced magnetic resonance imaging for prediction of postoperative early and late recurrence of single hepatocellular carcinoma. Clin Cancer Res 2019;25:3847-3855  https://doi.org/10.1158/1078-0432.CCR-18-2861
  18. Peng J, Lu F, Huang J, Zhang J, Gong W, Hu Y, et al. Development and validation of a pyradiomics signature to predict initial treatment response and prognosis during transarterial chemoembolization in hepatocellular carcinoma. Front Oncol 2022;12:853254 
  19. Tao YY, Shi Y, Gong XQ, Li L, Li ZM, Yang L, et al. Radiomic analysis based on magnetic resonance imaging for predicting PD-L2 expression in hepatocellular carcinoma. Cancers (Basel) 2023;15:365 
  20. Wang W, Gu D, Wei J, Ding Y, Yang L, Zhu K, et al. A radiomics-based biomarker for cytokeratin 19 status of hepatocellular carcinoma with gadoxetic acid-enhanced MRI. Eur Radiol 2020;30:3004-3014  https://doi.org/10.1007/s00330-019-06585-y
  21. Xia TY, Zhou ZH, Meng XP, Zha JH, Yu Q, Wang WL, et al. Predicting microvascular invasion in hepatocellular carcinoma using CT-based radiomics model. Radiology 2023;307:e222729 
  22. Xu X, Zhang HL, Liu QP, Sun SW, Zhang J, Zhu FP, et al. Radiomic analysis of contrast-enhanced CT predicts microvascular invasion and outcome in hepatocellular carcinoma. J Hepatol 2019;70:1133-1144  https://doi.org/10.1016/j.jhep.2019.02.023
  23. Yu Y, Fan Y, Wang X, Zhu M, Hu M, Shi C, et al. Gd-EOB-DTPA-enhanced MRI radiomics to predict vessels encapsulating tumor clusters (VETC) and patient prognosis in hepatocellular carcinoma. Eur Radiol 2022;32:959-970  https://doi.org/10.1007/s00330-021-08250-9
  24. Yuan C, Wang Z, Gu D, Tian J, Zhao P, Wei J, et al. Prediction early recurrence of hepatocellular carcinoma eligible for curative ablation using a radiomics nomogram. Cancer Imaging 2019;19:21 
  25. Liu F, Liu D, Wang K, Xie X, Su L, Kuang M, et al. Deep learning radiomics based on contrast-enhanced ultrasound might optimize curative treatments for very-early or early-stage hepatocellular carcinoma patients. Liver Cancer 2020;9:397-413  https://doi.org/10.1159/000505694
  26. Song D, Wang Y, Wang W, Wang Y, Cai J, Zhu K, et al. Using deep learning to predict microvascular invasion in hepatocellular carcinoma based on dynamic contrast-enhanced MRI combined with clinical parameters. J Cancer Res Clin Oncol 2021;147:3757-3767  https://doi.org/10.1007/s00432-021-03617-3
  27. Xu Z, An C, Shi F, Ren H, Li Y, Chen S, et al. Automatic prediction of hepatic arterial infusion chemotherapy response in advanced hepatocellular carcinoma with deep learning radiomic nomogram. Eur Radiol 2023;33:9038-9051 
  28. Zhang L, Xia W, Yan ZP, Sun JH, Zhong BY, Hou ZH, et al. Deep learning predicts overall survival of patients with unresectable hepatocellular carcinoma treated by transarterial chemoembolization plus sorafenib. Front Oncol 2020;10:593292 
  29. Zhang Y, Lv X, Qiu J, Zhang B, Zhang L, Fang J, et al. Deep learning with 3D convolutional neural network for noninvasive prediction of microvascular invasion in hepatocellular carcinoma. J Magn Reson Imaging 2021;54:134-143  https://doi.org/10.1002/jmri.27538
  30. Zhang Y, Wei Q, Huang Y, Yao Z, Yan C, Zou X, et al. Deep learning of liver contrast-enhanced ultrasound to predict microvascular invasion and prognosis in hepatocellular carcinoma. Front Oncol 2022;12:878061 
  31. Ji GW, Zhu FP, Xu Q, Wang K, Wu MY, Tang WW, et al. Machine-learning analysis of contrast-enhanced CT radiomics predicts recurrence of hepatocellular carcinoma after resection: a multi-institutional study. EBioMedicine 2019;50:156-165  https://doi.org/10.1016/j.ebiom.2019.10.057
  32. Ning P, Gao F, Hai J, Wu M, Chen J, Zhu S, et al. Application of CT radiomics in prediction of early recurrence in hepatocellular carcinoma. Abdom Radiol (NY) 2020;45:64-72  https://doi.org/10.1007/s00261-019-02198-7
  33. Kong C, Zhao Z, Chen W, Lv X, Shu G, Ye M, et al. Prediction of tumor response via a pretreatment MRI radiomics-based nomogram in HCC treated with TACE. Eur Radiol 2021;31:7500-7511  https://doi.org/10.1007/s00330-021-07910-0
  34. Tian Y, Komolafe TE, Zheng J, Zhou G, Chen T, Zhou B, et al. Assessing PD-L1 expression level via preoperative MRI in HCC based on integrating deep learning and radiomics features. Diagnostics (Basel) 2021;11:1875 
  35. Hectors SJ, Lewis S, Besa C, King MJ, Said D, Putra J, et al. MRI radiomics features predict immuno-oncological characteristics of hepatocellular carcinoma. Eur Radiol 2020;30:3759-3769  https://doi.org/10.1007/s00330-020-06675-2
  36. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 2003;38:200-207  https://doi.org/10.1016/S0168-8278(02)00360-4
  37. Lee S, Kang TW, Song KD, Lee MW, Rhim H, Lim HK, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg 2021;273:564-571  https://doi.org/10.1097/SLA.0000000000003268
  38. Ma X, Wei J, Gu D, Zhu Y, Feng B, Liang M, et al. Preoperative radiomics nomogram for microvascular invasion prediction in hepatocellular carcinoma using contrast-enhanced CT. Eur Radiol 2019;29:3595-3605  https://doi.org/10.1007/s00330-018-5985-y
  39. Peng J, Zhang J, Zhang Q, Xu Y, Zhou J, Liu L. A radiomics nomogram for preoperative prediction of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma. Diagn Interv Radiol 2018;24:121-127  https://doi.org/10.5152/dir.2018.17467
  40. Yang L, Gu D, Wei J, Yang C, Rao S, Wang W, et al. A radiomics nomogram for preoperative prediction of microvascular invasion in hepatocellular carcinoma. Liver Cancer 2019;8:373-386  https://doi.org/10.1159/000494099
  41. Park HJ, Yoon JS, Lee SS, Suk HI, Park B, Sung YS, et al. Deep learning-based assessment of functional liver capacity using gadoxetic acid-enhanced hepatobiliary phase MRI. Korean J Radiol 2022;23:720-731  https://doi.org/10.3348/kjr.2021.0892
  42. Ahn Y, Yoon JS, Lee SS, Suk HI, Son JH, Sung YS, et al. Deep learning algorithm for automated segmentation and volume measurement of the liver and spleen using portal venous phase computed tomography images. Korean J Radiol 2020;21:987-997  https://doi.org/10.3348/kjr.2020.0237
  43. Bilic P, Christ P, Li HB, Vorontsov E, Ben-Cohen A, Kaissis G, et al. The liver tumor segmentation benchmark (LiTS). Med Image Anal 2023;84:102680 
  44. Berenguer R, Pastor-Juan MDR, Canales-Vazquez J, Castro-Garcia M, Villas MV, Mansilla Legorburo F, et al. Radiomics of CT features may be nonreproducible and redundant: influence of CT acquisition parameters. Radiology 2018;288:407-415  https://doi.org/10.1148/radiol.2018172361
  45. Zwanenburg A, Vallieres M, Abdalah MA, Aerts HJWL, Andrearczyk V, Apte A, et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology 2020;295:328-338  https://doi.org/10.1148/radiol.2020191145
  46. Orlhac F, Frouin F, Nioche C, Ayache N, Buvat I. Validation of a method to compensate multicenter effects affecting CT radiomics. Radiology 2019;291:53-59  https://doi.org/10.1148/radiol.2019182023
  47. Orlhac F, Lecler A, Savatovski J, Goya-Outi J, Nioche C, Charbonneau F, et al. How can we combat multicenter variability in MR radiomics? Validation of a correction procedure. Eur Radiol 2021;31:2272-2280  https://doi.org/10.1007/s00330-020-07284-9
  48. Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, van Timmeren J, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 2017;14:749-762 https://doi.org/10.1038/nrclinonc.2017.141