Skip to main content

Advertisement

Log in

A predictive model integrating deep and radiomics features based on gadobenate dimeglumine-enhanced MRI for postoperative early recurrence of hepatocellular carcinoma

  • Abdominal Radiology
  • Published:
La radiologia medica Aims and scope Submit manuscript

Abstract

Purpose

Hepatocellular carcinoma (HCC) is the most common liver cancer worldwide, and early recurrence of HCC after curative hepatic resection is indicative of poor prognoses. We aim to develop a predictive model for postoperative early recurrence of HCC based on deep and radiomics features from multi-phasic magnetic resonance imaging (MRI).

Materials and methods

A total of 472 HCC patients were included and divided into the training (n = 378) and validation (n = 94) cohorts in the retrospective study. We separately extracted radiomics features and deep features from eight phases of gadoxetic acid-enhanced MRI and utilized the least absolute shrinkage and selection operator logistic regression algorithm for feature selection and model construction. We integrated the selected two types of features into a combined model and established a radiomics model as well as a deep learning (DL) model for comparison.

Results

In the training and validation cohorts, the combined model demonstrated better performance for stratifying patients at high risk of early recurrence (AUC of 0.911 and 0.840, accuracy of 0.779 and 0.777, sensitivity of 0.927 and 0.769, specificity 0.720 and 0.779) than the radiomics model (AUC of 0.740 and 0.780) and the DL model (AUC of 0.887 and 0.813).

Conclusion

The combined model integrating deep and radiomics features from multi-phasic MRI is efficient for noninvasively stratifying patients at high risk of early HCC recurrence after resection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AUC:

Area under the receiver operating characteristic curve

BCLC:

Barcelona Clinic Liver Cancer

CNN:

Convolutional neural network

DCA:

Decision curve analysis

DCNN:

Deep convolutional neural network

DL:

Deep learning

FC:

Fully connected

HCC:

Hepatocellular carcinoma

LASSO:

Least absolute shrinkage and selection operator

MRI:

Magnetic resonance imaging

NPV:

Negative predictive value

PPV:

Positive predictive value

RFS:

Recurrence-free survival

ROC:

Receiver operating characteristic

T2WI:

T2-weighted imaging

VOI:

Volume of interest

References

  1. Forner A, Reig M, Bruix J (2018) Hepatocellular carcinoma. Lancet 391(10127):1301–1314. https://doi.org/10.1016/S0140-6736(18)30010-2

    Article  PubMed  Google Scholar 

  2. Cheng Z, Yang P, Qu S, Zhou J, Yang J, Yang X, Xia Y, Li J, Wang K, Yan Z, Wu D, Zhang B, Huser N, Shen F (2015) Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HPB (Oxford) 17(5):422–427. https://doi.org/10.1111/hpb.12367

    Article  Google Scholar 

  3. Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S (2015) Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg 261(5):947–955. https://doi.org/10.1097/SLA.0000000000000710

    Article  PubMed  Google Scholar 

  4. Choi GH, Kim DH, Kang CM, Kim KS, Choi JS, Lee WJ, Kim BR (2008) Prognostic factors and optimal treatment strategy for intrahepatic nodular recurrence after curative resection of hepatocellular carcinoma. Ann Surg Oncol 15(2):618–629. https://doi.org/10.1245/s10434-007-9671-6

    Article  PubMed  Google Scholar 

  5. Bruix J, Takayama T, Mazzaferro V, Chau GY, Yang J, Kudo M, Cai J, Poon RT, Han KH, Tak WY, Lee HC, Song T, Roayaie S, Bolondi L, Lee KS, Makuuchi M, Souza F, Berre MA, Meinhardt G, Llovet JM, investigators S (2015) Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol 16 (13):1344–1354. doi:https://doi.org/10.1016/S1470-2045(15)00198-9

  6. Dioguardi Burgio M, Ronot M, Fuks D, Dondero F, Cauchy F, Gaujoux S, Dokmak S, Paradis V, Durand F, Belghiti J, Vilgrain V (2015) Follow-up Imaging After Liver Transplantation Should Take Into Consideration Primary Hepatocellular Carcinoma Characteristics. Transplantation 99(8):1613–1618. https://doi.org/10.1097/TP.0000000000000659

    Article  CAS  PubMed  Google Scholar 

  7. Liu D, Fong DY, Chan AC, Poon RT, Khong PL (2015) Hepatocellular carcinoma: surveillance CT schedule after hepatectomy based on risk stratification. Radiology 274(1):133–140. https://doi.org/10.1148/radiol.14132343

    Article  PubMed  Google Scholar 

  8. Hao S, Fan P, Chen S, Tu C, Wan C (2017) Distinct recurrence risk factors for intrahepatic metastasis and multicenter occurrence after surgery in patients with hepatocellular carcinoma. J Gastrointest Surg 21(2):312–320. https://doi.org/10.1007/s11605-016-3311-z

    Article  PubMed  Google Scholar 

  9. Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Tahara M, Kakisaka T, Tsuruga Y, Todo S, Taketomi A (2012) Analysis of the risk factors for early death due to disease recurrence or progression within 1 year after hepatectomy in patients with hepatocellular carcinoma. World J Surg Oncol 10:107. https://doi.org/10.1186/1477-7819-10-107

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zhou J, Sun HC, Wang Z, Cong WM, Wang JH, Zeng MS, Yang JM, Bie P, Liu LX, Wen TF, Han GH, Wang MQ, Liu RB, Lu LG, Ren ZG, Chen MS, Zeng ZC, Liang P, Liang CH, Chen M, Yan FH, Wang WP, Ji Y, Cheng WW, Dai CL, Jia WD, Li YM, Li YX, Liang J, Liu TS, Lv GY, Mao YL, Ren WX, Shi HC, Wang WT, Wang XY, Xing BC, Xu JM, Yang JY, Yang YF, Ye SL, Yin ZY, Zhang BH, Zhang SJ, Zhou WP, Zhu JY, Liu R, Shi YH, Xiao YS, Dai Z, Teng GJ, Cai JQ, Wang WL, Dong JH, Li Q, Shen F, Qin SK, Fan J (2018) Guidelines for Diagnosis and Treatment of Primary Liver Cancer in China (2017 Edition). Liver Cancer 7 (3):235–260. doi:https://doi.org/10.1159/000488035

  11. Kumar V, Gu Y, Basu S, Berglund A, Eschrich SA, Schabath MB, Forster K, Aerts HJ, Dekker A, Fenstermacher D, Goldgof DB, Hall LO, Lambin P, Balagurunathan Y, Gatenby RA, Gillies RJ (2012) Radiomics: the process and the challenges. Magn Reson Imaging 30(9):1234–1248. https://doi.org/10.1016/j.mri.2012.06.010

    Article  PubMed  PubMed Central  Google Scholar 

  12. Zhou Y, He L, Huang Y, Chen S, Wu P, Ye W, Liu Z, Liang C (2017) CT-based radiomics signature: a potential biomarker for preoperative prediction of early recurrence in hepatocellular carcinoma. Abdom Radiol (NY) 42(6):1695–1704. https://doi.org/10.1007/s00261-017-1072-0

    Article  Google Scholar 

  13. Kim S, Shin J, Kim DY, Choi GH, Kim MJ, Choi JY (2019) Radiomics on gadoxetic acid-enhanced magnetic resonance imaging for prediction of postoperative early and late recurrence of single hepatocellular carcinoma. Clin Cancer Res 25(13):3847–3855. https://doi.org/10.1158/1078-0432.CCR-18-2861

    Article  CAS  PubMed  Google Scholar 

  14. Zhang Z, Jiang H, Chen J, Wei Y, Cao L, Ye Z, Li X, Ma L, Song B (2019) Hepatocellular carcinoma: radiomics nomogram on gadoxetic acid-enhanced MR imaging for early postoperative recurrence prediction. Cancer Imaging 19(1):22. https://doi.org/10.1186/s40644-019-0209-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wen L, Weng S, Yan C, Ye R, Zhu Y, Zhou L, Gao L, Li Y (2021) A Radiomics nomogram for preoperative prediction of early recurrence of small hepatocellular carcinoma after surgical resection or radiofrequency ablation. Front Oncol 11:657039. https://doi.org/10.3389/fonc.2021.657039

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zhao Y, Wu J, Zhang Q, Hua Z, Qi W, Wang N, Lin T, Sheng L, Cui D, Liu J, Song Q, Li X, Wu T, Guo Y, Cui J, Liu A (2021) Radiomics analysis based on multiparametric MRI for predicting early recurrence in hepatocellular carcinoma after partial hepatectomy. J Magn Reson Imaging 53(4):1066–1079. https://doi.org/10.1002/jmri.27424

    Article  PubMed  Google Scholar 

  17. Shan QY, Hu HT, Feng ST, Peng ZP, Chen SL, Zhou Q, Li X, Xie XY, Lu MD, Wang W, Kuang M (2019) CT-based peritumoral radiomics signatures to predict early recurrence in hepatocellular carcinoma after curative tumor resection or ablation. Cancer Imaging 19(1):11. https://doi.org/10.1186/s40644-019-0197-5

    Article  PubMed  PubMed Central  Google Scholar 

  18. Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, Bussink J, Monshouwer R, Haibe-Kains B, Rietveld D, Hoebers F, Rietbergen MM, Leemans CR, Dekker A, Quackenbush J, Gillies RJ, Lambin P (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006. https://doi.org/10.1038/ncomms5006

    Article  CAS  PubMed  Google Scholar 

  19. LeCun Y, Bengio Y, Hinton G (2015) Deep learning. Nature 521(7553):436–444. https://doi.org/10.1038/nature14539

    Article  CAS  PubMed  Google Scholar 

  20. Le Berre C, Sandborn WJ, Aridhi S, Devignes MD, Fournier L, Smail-Tabbone M, Danese S, Peyrin-Biroulet L (2020) Application of Artificial Intelligence to Gastroenterology and Hepatology. Gastroenterology 158 (1):76–94. doi:https://doi.org/10.1053/j.gastro.2019.08.058

  21. Song D, Wang Y, Wang W, Wang Y, Cai J, Zhu K, Lv M, Gao Q, Zhou J, Fan J, Rao S, Wang M, Wang X (2021) 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. https://doi.org/10.1007/s00432-021-03617-3

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ning Z, Luo J, Li Y, Han S, Feng Q, Xu Y, Chen W, Chen T, Zhang Y (2019) Pattern classification for gastrointestinal stromal tumors by integration of radiomics and deep convolutional features. IEEE J Biomed Health Inform 23(3):1181–1191. https://doi.org/10.1109/JBHI.2018.2841992

    Article  PubMed  Google Scholar 

  23. Huang B, Tian J, Zhang H, Luo Z, Qin J, Huang C, He X, Luo Y, Zhou Y, Dan G, Chen H, Feng S, Yuan C (2020) Deep semantic segmentation feature-based radiomics for the classification tasks in medical image analysis. IEEE J Biomed Health Inform. doi:https://doi.org/10.1109/JBHI.2020.3043236

  24. Paul R, Hawkins SH, Schabath MB, Gillies RJ, Hall LO, Goldgof DB (2018) Predicting malignant nodules by fusing deep features with classical radiomics features. J Med Imaging (Bellingham) 5(1):011021. https://doi.org/10.1117/1.JMI.5.1.011021

    Article  Google Scholar 

  25. European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L (2018) EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 69 (1):182-236. doi:https://doi.org/10.1016/j.jhep.2018.03.019

  26. Chernyak V, Fowler KJ, Kamaya A, Kielar AZ, Elsayes KM, Bashir MR, Kono Y, Do RK, Mitchell DG, Singal AG, Tang A, Sirlin CB (2018) Liver imaging reporting and data system (LI-RADS) version 2018: imaging of hepatocellular carcinoma in at-risk patients. Radiology 289(3):816–830. https://doi.org/10.1148/radiol.2018181494

    Article  PubMed  Google Scholar 

  27. Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, Roberts LR, Heimbach JK (2018) Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American association for the study of liver diseases. Hepatology 68(2):723–750. https://doi.org/10.1002/hep.29913

    Article  PubMed  Google Scholar 

  28. van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V, Beets-Tan RGH, Fillion-Robin JC, Pieper S, Aerts H (2017) Computational radiomics system to decode the radiographic phenotype. Cancer Res 77(21):e104–e107. https://doi.org/10.1158/0008-5472.CAN-17-0339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sauerbrei W, Royston P, Binder H (2007) Selection of important variables and determination of functional form for continuous predictors in multivariable model building. Stat Med 26(30):5512–5528. https://doi.org/10.1002/sim.3148

    Article  PubMed  Google Scholar 

  30. An C, Kim DW, Park YN, Chung YE, Rhee H, Kim MJ (2015) Single hepatocellular carcinoma: preoperative MR imaging to predict early recurrence after curative resection. Radiology 276(2):433–443. https://doi.org/10.1148/radiol.15142394

    Article  PubMed  Google Scholar 

  31. Ding HF, Zhang XF, Bagante F, Ratti F, Marques HP, Soubrane O, Lam V, Poultsides GA, Popescu I, Alexandrescu S, Martel G, Workneh A, Guglielmi A, Hugh T, Aldrighetti L, Lv Y, Pawlik TM (2021) Prediction of tumor recurrence by alpha-fetoprotein model after curative resection for hepatocellular carcinoma. Eur J Surg Oncol 47 (3 Pt B):660–666. doi:https://doi.org/10.1016/j.ejso.2020.10.017

Download references

Acknowledgements

Funding was provided by National Natural Science Foundation of China (Grant Nos. 81227901, 81527805, 81571661), Chinese Academy of Sciences (Grant No. GJJSTD20170004), National Key Research and Development Program of China (Grant No.2017YFC0108804), The Shanghai Sailing Program (Grant No. 19YF1408100), Fudan University Medical-Industrial Integration Project (Grant No. XM03211196) and The China International Medical Foundation (Grant No. Z-2014-07-2003-04).

Funding

This study was funded by National Natural Science Foundation of China (No. 81227901, 81527805, 81571661), Chinese Academy of Sciences (No. GJJSTD20170004), The National Key Research and Development Program of China (No. 2017YFC0108804), The Shanghai Sailing Program (No. 19YF1408100), The China International Medical Foundation (No. Z-2014-07-2003-04), and Fudan University Medical-Industrial Integration Project (No. XM03211196).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sheng-xiang Rao or Manning Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

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.

Supplementary file1 (DOCX 122 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, W., Wang, W., Song, D. et al. A predictive model integrating deep and radiomics features based on gadobenate dimeglumine-enhanced MRI for postoperative early recurrence of hepatocellular carcinoma. Radiol med 127, 259–271 (2022). https://doi.org/10.1007/s11547-021-01445-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11547-021-01445-6

Keywords

Navigation