Abstract
Purpose
To investigate the potential of radiomics analysis of dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) in preoperatively predicting microvascular invasion (MVI) in patients with combined hepatocellular-cholangiocarcinoma (cHCC-CC) before surgery.
Methods
A cohort of 91 patients with histologically confirmed cHCC-CC who underwent preoperative liver DCE-MRI were enrolled and divided into a training cohort (27 MVI-positive and 37 MVI-negative) and a validation cohort (11 MVI-positive and 16 MVI-negative). Clinical characteristics and MR features of the patients were evaluated. Radiomics features were extracted from DCE-MRI, and a radiomics signature was built using the least absolute shrinkage and selection operator (LASSO) algorithm in the training cohort. Prediction performance of the developed radiomics signature was evaluated by utilizing the receiver operating characteristic (ROC) analysis.
Results
Larger tumor size and higher Radscore were associated with the presence of MVI in the training cohort (p = 0.026 and < 0.001, respectively), and theses findings were also confirmed in the validation cohort (p = 0.040 and 0.001, respectively). The developed radiomics signature, composed of 4 stable radiomics features, showed high prediction performance in both the training cohort (AUC = 0.866, 95% CI 0.757–0.938, p < 0.001) and validation cohort (AUC = 0.841, 95% CI 0.650–0.952, p < 0.001).
Conclusions
The radiomics signature developed from DCE-MRI can be a reliable imaging biomarker to preoperatively predict MVI in cHCC-CC.
Similar content being viewed by others
Abbreviations
- AFP:
-
Alpha fetoprotein
- AUC:
-
Area under curve
- CA19-9:
-
Cancer antigen19-9
- CEA:
-
Carcinoembryonic antigen
- cHCC-CC:
-
Combined hepatocellular-cholangiocarcinoma
- HCC:
-
Hepatocellular carcinoma
- ICC:
-
Intrahepatic cholangiocarcinoma
- IMCC:
-
Mass-forming intrahepatic cholangiocarcinoma
- LASSO:
-
Least absolute shrinkage and selection operator
- MRI:
-
Magnetic resonance imaging
- MVI:
-
Microvascular invasion
- ROC:
-
Receiver operating characteristic curve
- AP:
-
Arterial phase
- PP:
-
Portal phase
- DP:
-
Delayed phase
References
Beaufrère A, Calderaro J, Paradis V (2021) Combined hepatocellular-cholangiocarcinoma: An update. J Hepatol 74:1212-1224. https://doi.org/10.1016/j.jhep.2021.01.035
Weber SM, Ribero D, O'Reilly EM, Kokudo N, Miyazaki M, Pawlik TM (2015) Intrahepatic cholangiocarcinoma: expert consensus statement. HPB (Oxford) 17:669-680. https://doi.org/10.1111/hpb.12441
Ogasawara S, Akiba J, Nakayama M, Nakashima O, Torimura T, Yano H (2015) Epithelial cell adhesion molecule-positive human hepatic neoplastic cells: development of combined hepatocellular-cholangiocarcinoma in mice. J Gastroenterol Hepatol 30:413-420. https://doi.org/10.1111/jgh.12692
Sciarra A, Park YN, Sempoux C (2020) Updates in the diagnosis of combined hepatocellular-cholangiocarcinoma. Hum Pathol 96:48-55. https://doi.org/10.1016/j.humpath.2019.11.001
Tang Y, Wang L, Teng F, Zhang T, Zhao Y, Chen Z (2021) The clinical characteristics and prognostic factors of combined Hepatocellular Carcinoma and Cholangiocarcinoma, Hepatocellular Carcinoma and Intrahepatic Cholangiocarcinoma after Surgical Resection: A propensity score matching analysis. Int J Med Sci 18:187-198. https://doi.org/10.7150/ijms.50883
Erstad DJ, Tanabe KK (2019) Prognostic and Therapeutic Implications of Microvascular Invasion in Hepatocellular Carcinoma. Ann Surg Oncol 26:1474-1493. https://doi.org/10.1245/s10434-019-07227-9
Chen Y, Liu H, Zhang J et al (2021) Prognostic value and predication model of microvascular invasion in patients with intrahepatic cholangiocarcinoma: a multicenter study from China. BMC Cancer 21:1299. https://doi.org/10.1186/s12885-021-09035-5
Shao C, Chen J, Chen J, Shi J, Huang L, Qiu Y (2017) Histological classification of microvascular invasion to predict prognosis in intrahepatic cholangiocarcinoma. Int J Clin Exp Pathol 10:7674-7681.
Wang X, Wang W, Ma X et al (2020) Combined hepatocellular-cholangiocarcinoma: which preoperative clinical data and conventional MRI characteristics have value for the prediction of microvascular invasion and clinical significance? Eur Radiol 30:5337-5347. https://doi.org/10.1007/s00330-020-06861-2
Wang T, Yang X, Tang H et al (2020) Integrated nomograms to predict overall survival and recurrence-free survival in patients with combined hepatocellular cholangiocarcinoma (cHCC) after liver resection. Aging (Albany NY) 12:15334-15358. https://doi.org/10.18632/aging.103577
Wang Y, Zhou CW, Zhu GQ et al (2021) A multidimensional nomogram combining imaging features and clinical factors to predict the invasiveness and metastasis of combined hepatocellular cholangiocarcinoma. Ann Transl Med 9:1518. https://doi.org/10.21037/atm-21-2500
Yip SS, Aerts HJ (2016) Applications and limitations of radiomics. Phys Med Biol 61:R150-166. https://doi.org/10.1088/0031-9155/61/13/r150
Wei J, Jiang H, Gu D et al (2020) Radiomics in liver diseases: Current progress and future opportunities. Liver Int 40:2050-2063. https://doi.org/10.1111/liv.14555
Jeong WK, Jamshidi N, Felker ER, Raman SS, Lu DS (2019) Radiomics and radiogenomics of primary liver cancers. Clin Mol Hepatol 25:21-29. https://doi.org/10.3350/cmh.2018.1007
Dreher C, Linde P, Boda-Heggemann J, Baessler B (2020) Radiomics for liver tumours. Strahlenther Onkol 196:888-899. https://doi.org/10.1007/s00066-020-01615-x
Yang L, Gu D, Wei J et al (2019) A Radiomics Nomogram for Preoperative Prediction of Microvascular Invasion in Hepatocellular Carcinoma. Liver Cancer 8:373-386. https://doi.org/10.1159/000494099
Ma X, Wei J, Gu D et al (2019) Preoperative radiomics nomogram for microvascular invasion prediction in hepatocellular carcinoma using contrast-enhanced CT. Eur Radiol 29:3595-3605. https://doi.org/10.1007/s00330-018-5985-y
Zhou Y, Zhou G, Zhang J, Xu C, Wang X, Xu P (2021) Radiomics signature on dynamic contrast-enhanced MR images: a potential imaging biomarker for prediction of microvascular invasion in mass-forming intrahepatic cholangiocarcinoma. Eur Radiol 31:6846-6855. https://doi.org/10.1007/s00330-021-07793-1
Cong WM, Bu H, Chen J et al (2016) Practice guidelines for the pathological diagnosis of primary liver cancer: 2015 update. World J Gastroenterol 22:9279-9287. https://doi.org/10.3748/wjg.v22.i42.9279
Hu HT, Wang Z, Kuang M, Wang W (2018) Need for normalization: the non-standard reference standard for microvascular invasion diagnosis in hepatocellular carcinoma. World J Surg Oncol 16:50. https://doi.org/10.1186/s12957-018-1347-0
Zhang X, Li J, Shen F, Lau WY (2018) Significance of presence of microvascular invasion in specimens obtained after surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol 33:347-354. https://doi.org/10.1111/jgh.13843
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159-174.
Zhou HF, Han YQ, Lu J et al (2019) Radiomics Facilitates Candidate Selection for Irradiation Stents Among Patients With Unresectable Pancreatic Cancer. Front Oncol 9:973. https://doi.org/10.3389/fonc.2019.00973
Tibshirani R (2011) Regression shrinkage and selection via the lasso: a retrospective. Journal of the Royal Statistical Society Series B 73:273-282.
Chen Y, Lu Q, Zhu Y, Huang B, Dong Y, Wang W (2022) Prediction of Microvascular Invasion in Combined Hepatocellular-Cholangiocarcinoma Based on Pre-operative Clinical Data and Contrast-Enhanced Ultrasound Characteristics. Ultrasound Med Biol 48:1190-1201. https://doi.org/10.1016/j.ultrasmedbio.2022.02.014
Zhao H, Chen C, Gu S et al (2017) Anatomical versus non-anatomical resection for solitary hepatocellular carcinoma without macroscopic vascular invasion: A propensity score matching analysis. J Gastroenterol Hepatol 32:870-878. https://doi.org/10.1111/jgh.13603
Limkin EJ, Reuzé S, Carré A et al (2019) The complexity of tumor shape, spiculatedness, correlates with tumor radiomic shape features. Sci Rep 9:4329. https://doi.org/10.1038/s41598-019-40437-5
Cuocolo R, Stanzione A, Ponsiglione A et al (2019) Clinically significant prostate cancer detection on MRI: A radiomic shape features study. Eur J Radiol 116:144-149. https://doi.org/10.1016/j.ejrad.2019.05.006
Horvat N, Araujo-Filho JAB, Assuncao-Jr AN et al (2021) Radiomic analysis of MRI to Predict Sustained Complete Response after Radiofrequency Ablation in Patients with Hepatocellular Carcinoma - A Pilot Study. Clinics (Sao Paulo) 76:e2888. https://doi.org/10.6061/clinics/2021/e2888
Xiao D, Zhao Z, Liu J et al (2021) Diagnosis of Invasive Meningioma Based on Brain-Tumor Interface Radiomics Features on Brain MR Images: A Multicenter Study. Front Oncol 11:708040. https://doi.org/10.3389/fonc.2021.708040
Mechee MS, Hussain ZM, Salman ZI (2021) Wavelet Theory: Applications of the Wavelet. Wavelet Theory
Xu X, Zhang HL, Liu QP et al (2019) Radiomic analysis of contrast-enhanced CT predicts microvascular invasion and outcome in hepatocellular carcinoma. J Hepatol 70:1133-1144. https://doi.org/10.1016/j.jhep.2019.02.023
Tang TY, Li X, Zhang Q et al (2020) Development of a Novel Multiparametric MRI Radiomic Nomogram for Preoperative Evaluation of Early Recurrence in Resectable Pancreatic Cancer. J Magn Reson Imaging 52:231-245. https://doi.org/10.1002/jmri.27024
Zhou Y, Zhou G, Zhang J, Xu C, Zhu F, Xu P (2022) DCE-MRI based radiomics nomogram for preoperatively differentiating combined hepatocellular-cholangiocarcinoma from mass-forming intrahepatic cholangiocarcinoma. Eur Radiol 32:5004-5015.https://doi.org/10.1007/s00330-022-08548-2
Funding
This study was supported by Grants from the Shanghai 2022 "Science and Technology Innovation Action Plan" medical innovation research special project (Grant Number 22Y11910900).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study does not contain any studies with animals performed by any of the authors. For this type of study formal consent is not required.
Informed consent
The institutional review board approved this study and waived informed consent because of retrospective study.
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, G., Zhou, Y., Xu, X. et al. MRI-based radiomics signature: a potential imaging biomarker for prediction of microvascular invasion in combined hepatocellular-cholangiocarcinoma. Abdom Radiol 49, 49–59 (2024). https://doi.org/10.1007/s00261-023-04049-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00261-023-04049-y