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MRI features and research progress of proliferative hepatocellular carcinoma
LÜ Yuanyuan  YU Changjiang  ZHU Shaocheng 

Cite this article as: LÜ Y Y, YU C J, ZHU S C. MRI features and research progress of proliferative hepatocellular carcinoma[J]. Chin J Magn Reson Imaging, 2023, 14(6): 161-165. DOI:10.12015/issn.1674-8034.2023.06.029.


[Abstract] Pathological subtypes of hepatocellular carcinoma are closely related to specific gene mutations and carcinogenic pathways. Studies have proposed an aggressive subtype: proliferative hepatocellular carcinoma, which usually has poor cell differentiation, high alpha-fetoprotein level and frequent microvascular invasion. Compared with non-proliferative hepatocellular carcinoma, this subtype has a high recurrence rate and a poor prognosis. MRI can noninvasively predict proliferative hepatocellular carcinoma. This paper reviews the MRI characteristics of proliferative hepatocellular carcinoma and the research progress of MRI based imaging omics and deep learning in the diagnosis of proliferative hepatocellular carcinoma, and discuss the challenges to provide theoretical basis for radiologists to identify proliferative hepatocellular carcinoma and to realize the early diagnosis and prognosis evaluation of proliferative hepatocellular carcinoma in clinical application.
[Keywords] proliferative hepatocellular carcinoma；cytokeratin 19；macrotrabecular-massive hepatocellular carcinoma；diagnosis；radiomics；magnetic resonance imaging

LÜ Yuanyuan1, 2   YU Changjiang1, 2   ZHU Shaocheng1, 2*  

1 Department of Medical Imaging, Zhengzhou University People's Hospital, Zhengzhou 450003, China

2 Department of Medical Imaging, Henan Provincial People's Hospital, Zhengzhou 450003, China

Corresponding author: Zhu SC, E-mail: zsc2686@163.com

Conflicts of interest   None.

ACKNOWLEDGMENTS Special Project of Key R&D and Promotion in Henan Province (Scientific and Technological Research) (No. 212102310729).
Received  2023-01-18
Accepted  2023-05-18
DOI: 10.12015/issn.1674-8034.2023.06.029
Cite this article as: LÜ Y Y, YU C J, ZHU S C. MRI features and research progress of proliferative hepatocellular carcinoma[J]. Chin J Magn Reson Imaging, 2023, 14(6): 161-165. DOI:10.12015/issn.1674-8034.2023.06.029.

[1]
SUNG H, FERLAY J, SIEGEL R L, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2021, 71(3): 209-249. DOI: 10.3322/caac.21660.
[2]
Global Burden of Disease Cancer Collaboration, FITZMAURICE C, ABATE D, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study[J]. JAMA Oncol, 2019, 5(12): 1749-1768. DOI: 10.1001/jamaoncol.2019.2996.
[3]
CALDERARO J, ZIOL M, PARADIS V, et al. Molecular and histological correlations in liver cancer[J]. J Hepatol, 2019, 71(3): 616-630. DOI: 10.1016/j.jhep.2019.06.001.
[4]
NAGTEGAAL I D, ODZE R D, KLIMSTRA D, et al. The 2019 WHO classification of tumours of the digestive system[J]. Histopathology, 2020, 76(2): 182-188. DOI: 10.1111/his.13975.
[5]
NAULT J C, GALLE P R, MARQUARDT J U. The role of molecular enrichment on future therapies in hepatocellular carcinoma[J]. J Hepatol, 2018, 69(1): 237-247. DOI: 10.1016/j.jhep.2018.02.016.
[6]
ZUCMAN-ROSSI J, VILLANUEVA A, NAULT J C, et al. Genetic landscape and biomarkers of hepatocellular carcinoma[J/OL]. Gastroenterology, 2015, 149(5): 1226-1239.e4 [2023-05-02]. https://www.gastrojournal.org/article/S0016-5085(15)00869-0/fulltext. DOI: 10.1053/j.gastro.2015.05.061.
[7]
NAULT J C, MARTIN Y, CARUSO S, et al. Clinical impact of genomic diversity from early to advanced hepatocellular carcinoma[J]. Hepatology, 2020, 71(1): 164-182. DOI: 10.1002/hep.30811.
[8]
KRINSKY G, SHANBHOGUE K. Proliferative versus nonproliferative hepatocellular carcinoma: clinical and imaging implications[J]. Radiology, 2021, 300(3): 583-585. DOI: 10.1148/radiol.2021211316.
[9]
SHIM J H, HAN S, SHIN Y M, et al. Prognostic performance of preoperative gadoxetic acid-enhanced MRI in resectable hepatocellular carcinoma[J]. J Magn Reson Imaging, 2015, 41(4): 1115-1123. DOI: 10.1002/jmri.24660.
[10]
KANG H J, KIM H, LEE D H, et al. Gadoxetate-enhanced MRI features of proliferative hepatocellular carcinoma are prognostic after surgery[J]. Radiology, 2021, 300(3): 572-582. DOI: 10.1148/radiol.2021204352.
[11]
TANG W Q, XUE J, LUO L, et al. Kangxianruangan Granule-containing serum mediated inhibition of hepatic oval cell differentiation into hepatocellular carcinoma cells via the Wnt-1/β-catenin signaling pathway[J/OL]. Mol Med Rep, 2022, 25(2): 55 [2023-01-31]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8711029/. DOI: 10.3892/mmr.2021.12571.
[12]
CHOI S Y, KIM S H, PARK C K, et al. Imaging features of gadoxetic acid-enhanced and diffusion-weighted MR imaging for identifying cytokeratin 19-positive hepatocellular carcinoma: a retrospective observational study[J]. Radiology, 2018, 286(3): 897-908. DOI: 10.1148/radiol.2017162846.
[13]
MULÉ S, GALLETTO PREGLIASCO A, TENENHAUS A, et al. Multiphase liver MRI for identifying the macrotrabecular-massive subtype of hepatocellular carcinoma[J]. Radiology, 2020, 295(3): 562-571. DOI: 10.1148/radiol.2020192230.
[14]
CALDERARO J, COUCHY G, IMBEAUD S, et al. Histological subtypes of hepatocellular carcinoma are related to gene mutations and molecular tumour classification[J]. J Hepatol, 2017, 67(4): 727-738. DOI: 10.1016/j.jhep.2017.05.014.
[15]
JEONG H T, KIM M J, KIM Y E, et al. MRI features of hepatocellular carcinoma expressing progenitor cell markers[J]. Liver Int, 2012, 32(3): 430-440. DOI: 10.1111/j.1478-3231.2011.02640.x.
[16]
MURAKATA A, TANAKA S, MOGUSHI K, et al. Gene expression signature of the gross morphology in hepatocellular carcinoma[J]. Ann Surg, 2011, 253(1): 94-100. DOI: 10.1097/SLA.0b013e3181f9bc00.
[17]
CHEN J B, ZHOU J, KUANG S C, et al. Liver imaging reporting and data system category 5: MRI predictors of microvascular invasion and recurrence after hepatectomy for hepatocellular carcinoma[J]. AJR Am J Roentgenol, 2019, 213(4): 821-830. DOI: 10.2214/AJR.19.21168.
[18]
ZHU Y J, FENG B, WANG B Z, et al. Value of gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid enhanced magnetic resonance imaging and diffusion-weighted MR imaging in predicting microvascular invasion in hepatocellular carcinoma and the prognostic significance[J]. Chin J Oncol, 2021, 43(3): 312-317. DOI: 10.3760/cma.j.cn112152-20191009-00652.
[19]
LIN B, ZHOU Z P. Research progress of Liver Imaging Reporting and Data System in the diagnosis of hepatocellular carcinoma[J]. Int J Med Radiol, 2020, 43(6): 686-692. DOI: 10.19300/j.2020.Z18143.
[20]
RHEE H, AN C, KIM H Y, et al. Hepatocellular carcinoma with irregular rim-like arterial phase hyperenhancement: more aggressive pathologic features[J]. Liver Cancer, 2019, 8(1): 24-40. DOI: 10.1159/000488540.
[21]
LU M T, QU Q, XU L, et al. Prediction for aggressiveness and postoperative recurrence of hepatocellular carcinoma using gadoxetic acid-enhanced magnetic resonance imaging[J]. Acad Radiol, 2023, 30(5): 841-852. DOI: 10.1016/j.acra.2022.12.018.
[22]
HUANG Z D, XIANG Y, MENG X S, et al. MRI features of hepatocellular carcinomas with different fibrotic stroma and their relationships with findings of delayed contrast-enhancement[J]. Chin J Radiol, 2017, 51(3): 183-187. DOI: 10.3760/cma.j.issn.1005?1201.2017.03.006.
[23]
HU X X, WANG W T, YANG L, et al. MR features based on LI-RADS identify cytokeratin 19 status of hepatocellular carcinomas[J]. Eur J Radiol, 2019, 113: 7-14. DOI: 10.1016/j.ejrad.2019.01.036.
[24]
SEO N, KIM M J, RHEE H. Hepatic sarcomatoid carcinoma: magnetic resonance imaging evaluation by using the liver imaging reporting and data system[J].Eur Radiol, 2019, 29(7): 3761-3771. DOI: 10.1007/s00330-019-06052-8.
[25]
LIAO S H, SU T H, JENG Y M, et al. Clinical manifestations and outcomes of patients with sarcomatoid hepatocellular carcinoma[J]. Hepatology, 2019, 69(1): 209-221. DOI: 10.1002/hep.30162.
[26]
YOON J K, CHOI J Y, RHEE H, et al. MRI features of histologic subtypes of hepatocellular carcinoma: correlation with histologic, genetic, and molecular biologic classification[J]. Eur Radiol, 2022, 32(8): 5119-5133. DOI: 10.1007/s00330-022-08643-4.
[27]
CHOI S Y, KIM Y K, MIN J H, et al. Added value of ancillary imaging features for differentiating scirrhous hepatocellular carcinoma from intrahepatic cholangiocarcinoma on gadoxetic acid-enhanced MR imaging[J]. Eur Radiol, 2018, 28(6): 2549-2560. DOI: 10.1007/s00330-017-5196-y.
[28]
HUANG S C, LIAO S H, SU T H, et al. Clinical manifestations and outcomes of patients with scirrhous hepatocellular carcinoma[J].Hepatol Int, 2021, 15(2): 472-481. DOI: 10.1007/s12072-021-10146-1.
[29]
WANG F Q, NUMATA K, NIHONMATSU H, et al. Intraprocedurally EOB-MRI/US fusion imaging focusing on hepatobiliary phase findings can help to reduce the recurrence of hepatocellular carcinoma after radiofrequency ablation[J]. Int J Hyperthermia, 2020, 37(1): 1149-1158. DOI: 10.1080/02656736.2020.1825837.
[30]
KITAO A, MATSUI O, YONEDA N, et al. The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: correlation with gadoxetic acid enhanced MR imaging[J]. Eur Radiol, 2011, 21(10): 2056-2066. DOI: 10.1007/s00330-011-2165-8.
[31]
CHOI J W, LEE J M, KIM S J, et al. Hepatocellular carcinoma: imaging patterns on gadoxetic acid-enhanced MR Images and their value as an imaging biomarker[J]. Radiology, 2013, 267(3): 776-786. DOI: 10.1148/radiol.13120775.
[32]
ZHU Y J, FENG B, WANG B Z, et al. Value of gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid enhanced magnetic resonance imaging and diffusion-weighted MR imaging in predicting microvascular invasion in hepatocellular carcinoma and the prognostic significance[J]. Chin J Oncol, 2021, 43(3): 312-317. DOI: 10.3760/cma.j.cn112152-20191009-00652.
[33]
HU H Y, QI S, ZENG S L, et al. Importance of microvascular invasion risk and tumor size on recurrence and survival of hepatocellular carcinoma after anatomical resection and non-anatomical resection[J/OL]. Front Oncol, 2021, 11: 621622 [2023-01-31]. https://www.frontiersin.org/articles/10.3389/fonc.2021.621622/full. DOI: 10.3389/fonc.2021.621622.
[34]
SHIMADA S, KAMIYAMA T, KAKISAKA T, et al. Impact of gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced magnetic resonance imaging on the prognosis of hepatocellular carcinoma after surgery[J]. JGH Open, 2021, 5(1): 41-49. DOI: 10.1002/jgh3.12444.
[35]
JIANG H Y, CHEN J, XIA C C, et al. Noninvasive imaging of hepatocellular carcinoma: from diagnosis to prognosis[J]. World J Gastroenterol, 2018, 24(22): 2348-2362. DOI: 10.3748/wjg.v24.i22.2348.
[36]
KIM J G, JIANG K M, MIN G S, et al. Questionable correlation of the apparent diffusion coefficient with the histological grade and microvascular invasion in small hepatocellular carcinoma[J/OL]. Clin Radiol, 2019, 74(5): 406.e19-406.e27 [2023-01-31]. https://linkinghub.elsevier.com/retrieve/pii/S0009-9260(19)30081-9. DOI: 10.1016/j.crad.2019.01.019.
[37]
LV X L, CHEN M J, KONG C L, et al. Construction of a novel radiomics nomogram for the prediction of aggressive intrasegmental recurrence of HCC after radiofrequency ablation[J/OL]. Eur J Radiol, 2021, 144: 109955 [2023-01-31]. https://linkinghub.elsevier.com/retrieve/pii/S0720-048X(21)00436-8. DOI: 10.1016/j.ejrad.2021.109955.
[38]
CHEN Y Y, CAI H S, YANG Y H, et al. Preoperative prediction of the expression of CK19 in hepatocellular carcinoma by Gd-EOB-DTPA enhanced MRI[J]. J Sun Yat Sen Univ Med Sci, 2019, 40(6): 866-874. DOI: 10.1259/bjr.20180017.
[39]
CHEN J, XIA C C, DUAN T, et al. Macrotrabecular-massive hepatocellular carcinoma: imaging identification and prediction based on gadoxetic acid-enhanced magnetic resonance imaging[J]. Eur Radiol, 2021, 31(10): 7696-7704. DOI: 10.1007/s00330-021-07898-7.
[40]
NIENDORF E, SPILSETH B, WANG X, et al. Contrast enhanced MRI in the diagnosis of HCC[J]. Diagnostics, 2015, 5(3): 383-398. DOI: 10.3390/diagnostics5030383.
[41]
LI X M, CAI P, CHENG L, et al. Clinical value of gadolinium ethoxybenzyl diethylanetriaminepentaacetic acid enhanced MRI in the preoperative diagnosis of macrotrabecular-massive hepatocellular carcinoma[J]. Chin J Dig Surg, 2021, 20(11): 1218-1226. DOI: 10.3760/cma.j.cn115610-20210809-00385.
[42]
CALDERARO J, MEUNIER L, NGUYEN C T, et al. ESM1 as a marker of macrotrabecular-massive hepatocellular carcinoma[J]. Clin Cancer Res, 2019, 25(19): 5859-5865. DOI: 10.1158/1078-0432.CCR-19-0859.
[43]
VILLA E, CRITELLI R, LEI B, et al. Neoangiogenesis-related genes are hallmarks of fast-growing hepatocellular carcinomas and worst survival. Results from a prospective study[J]. Gut, 2016, 65(5): 861-869. DOI: 10.1136/gutjnl-2014-308483.
[44]
LOY L M, LOW H M, CHOI J Y, et al. Variant hepatocellular carcinoma subtypes according to the 2019 WHO classification: an imaging-focused review[J]. AJR Am J Roentgenol, 2022, 219(2): 212-223. DOI: 10.2214/AJR.21.26982.
[45]
GONG X Q, TAO Y Y, WU Y K, et al. Progress of MRI radiomics in hepatocellular carcinoma[J/OL]. Front Oncol, 2021, 11: 698373 [2023-01-31]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8488263/. DOI: 10.3389/fonc.2021.698373.
[46]
LV K, CAO X, DU P, et al. Radiomics for the detection of microvascular invasion in hepatocellular carcinoma[J]. World J Gastroenterol, 2022, 28(20): 2176-2183. DOI: 10.3748/wjg.v28.i20.2176.
[47]
CHEN J, WU Z R, XIA C C, et al. Noninvasive prediction of HCC with progenitor phenotype based on gadoxetic acid-enhanced MRI[J]. Eur Radiol, 2020, 30(2): 1232-1242. DOI: 10.1007/s00330-019-06414-2.
[48]
WANG W T, GU D S, WEI J W, et al. A radiomics-based biomarker for cytokeratin 19 status of hepatocellular carcinoma with gadoxetic acid-enhanced MRI[J]. Eur Radiol, 2020, 30(5): 3004-3014. DOI: 10.1007/s00330-019-06585-y.
[49]
YANG F, WAN Y D, XU L, et al. MRI-radiomics prediction for cytokeratin 19-positive hepatocellular carcinoma: a multicenter study[J/OL]. Front Oncol, 2021, 11: 672126 [2023-01-31]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8406635/. DOI: 10.3389/fonc.2021.672126.
[50]
ZHU Y M, WENG S P, LI Y M, et al. A radiomics nomogram based on contrast-enhanced MRI for preoperative prediction of macrotrabecular- massive hepatocellular carcinoma[J]. Abdom Radiol (NY), 2021, 46(7): 3139-3148. DOI: 10.1007/s00261-021-02989-x.
[51]
CHEN Y Y, CHEN J, ZHANG Y, et al. Preoperative prediction of cytokeratin 19 expression for hepatocellular carcinoma with deep learning radiomics based on gadoxetic acid-enhanced magnetic resonance imaging[J]. J Hepatocell Carcinoma, 2021, 8: 795-808. DOI: 10.2147/JHC.S313879.
[52]
OESTMANN P M, WANG C J, SAVIC L J, et al. Deep learning-assisted differentiation of pathologically proven atypical and typical hepatocellular carcinoma (HCC) versus non-HCC on contrast-enhanced MRI of the liver[J]. Eur Radiol, 2021, 31(7): 4981-4990. DOI: 10.1007/s00330-020-07559-1.
[53]
CALDERARO J, SERAPHIN T P, LUEDDE T, et al. Artificial intelligence for the prevention and clinical management of hepatocellular carcinoma[J]. J Hepatol, 2022, 76(6): 1348-1361. DOI: 10.1016/j.jhep.2022.01.014.

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