Skip to main content

Advertisement

Log in

Dynamic Contrast-Enhanced Ultrasound Radiomics for Hepatocellular Carcinoma Recurrence Prediction After Thermal Ablation

  • Research Article
  • Published:
Molecular Imaging and Biology Aims and scope Submit manuscript

Abstract

Purpose

To develop a radiomics model based on dynamic contrast-enhanced ultrasound (CEUS) to predict early and late recurrence in patients with a single HCC lesion ≤ 5 cm in diameter after thermal ablation.

Procedures

We enrolled patients who underwent thermal ablation for HCC in our hospital from April 2004 to April 2017. Radiomics based on two branch convolution recurrent network was utilized to analyze preoperative dynamic CEUS image of HCC lesions to establish CEUS model, in comparison to the conventional ultrasound (US), clinical, and combined models. Clinical follow-up of HCC recurrence after ablation were taken as reference standard to evaluate the predicted performance of CEUS model and other models.

Results

We finally analyzed 318 patients (training cohort: test cohort = 255:63). The combined model showed better performance for early recurrence than CUES (in training cohort, AUC, 0.89 vs. 0.84, P < 0.001; in test cohort, AUC, 0.84 vs. 0.83, P = 0.272), US (P < 0.001), or clinical model (P < 0.001). For late recurrence prediction, the combined model showed the best performance than the CEUS (C-index, in training cohort, 0.77 vs. 0.76, P = 0.009; in test cohort, 0.77 vs. 0.68, P < 0.001), US (P < 0.001), or clinical model (P < 0.001).

Conclusions

The CEUS model based on dynamic CEUS radiomics performed well in predicting early HCC recurrence after ablation. The combined model combining CEUS, US radiomics, and clinical factors could stratify the high risk of late recurrence.

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

References

  1. J F, I S, R D, S E, C M, M R, DM P, D F, cancer BFJIjo: Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. 2015, 136(5):E359–386

  2. Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology (Baltimore, Md) 53(3):1020–1022

    Article  Google Scholar 

  3. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol 2018, 69(1):182–236

  4. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012, 56(4):908–943

  5. Benson AB 3rd, D'Angelica MI, Abbott DE, Abrams TA, Alberts SR, Saenz DA, Are C, Brown DB, Chang DT, Covey AM et al (2017) NCCN Guidelines insights: Hepatobiliary cancers, version 1.2017. J Natl Compr Cancer Network 15(5):563–573

    Article  Google Scholar 

  6. Hirokawa F, Hayashi M, Miyamoto Y, Asakuma M, Shimizu T, Komeda K, Inoue Y, Uchiyama K (2014) Outcomes and predictors of microvascular invasion of solitary hepatocellular carcinoma. Hepatol Res 44(8):846–853

    Article  CAS  Google Scholar 

  7. Renzulli M, Brocchi S, Cucchetti A, Mazzotti F, Mosconi C, Sportoletti C, Brandi G, Pinna AD, Golfieri R (2016) Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology 279(2):432–442

    Article  Google Scholar 

  8. Pawlik TM, Gleisner AL, Anders RA, Assumpcao L, Maley W, Choti MA (2007) Preoperative assessment of hepatocellular carcinoma tumor grade using needle biopsy: implications for transplant eligibility. Ann Surg 245(3):435–442

    Article  Google Scholar 

  9. Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, Bussink J, Monshouwer R, Haibe-Kains B, Rietveld D et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006

    Article  CAS  Google Scholar 

  10. Limkin EJ, Sun R, Dercle L, Zacharaki EI, Robert C, Reuze S, Schernberg A, Paragios N, Deutsch E, Ferte C (2017) Promises and challenges for the implementation of computational medical imaging (radiomics) in oncology. Ann Oncol 28(6):1191–1206

    Article  CAS  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. Yuan C, Wang Z, Gu D, Tian J, Zhao P, Wei J, Yang X, Hao X, Dong D, He N, Sun Y, Gao W, Feng J (2019) Prediction early recurrence of hepatocellular carcinoma eligible for curative ablation using a Radiomics nomogram. Cancer Imaging 19(1):21

    Article  Google Scholar 

  13. Zheng BH, Liu LZ, Zhang ZZ, Shi JY, Dong LQ, Tian LY, Ding ZB, Ji Y, Rao SX, Zhou J, Fan J, Wang XY, Gao Q (2018) Radiomics score: a potential prognostic imaging feature for postoperative survival of solitary HCC patients. BMC Cancer 18(1):1148

    Article  Google Scholar 

  14. Hui TCH, Chuah TK, Low HM, Tan CH (2018) Predicting early recurrence of hepatocellular carcinoma with texture analysis of preoperative MRI: a radiomics study. Clin Radiol 73(12):1056.e1011–1056.e1016

    Article  Google Scholar 

  15. Ahmed M, Solbiati L, Brace CL, Breen DJ, Callstrom MR, Charboneau JW, Chen MH, Choi BI, de Baere T, Dodd GD 3rd et al (2014) Image-guided tumor ablation: standardization of terminology and reporting criteria--a 10-year update. Radiology 273(1):241–260

    Article  Google Scholar 

  16. Alzaraa A, Gravante G, Chung WY, Al-Leswas D, Morgan B, Dennison A, Lloyd D (2013) Contrast-enhanced ultrasound in the preoperative, intraoperative and postoperative assessment of liver lesions. Hepatol Res 43(8):809–819

    Article  Google Scholar 

  17. Liu F, Liu D, Wang K, Xie X, Su L, Kuang M, Huang G, Peng B, Wang Y, Zhou H: Deep learning radiomics based on contrast-enhanced ultrasound might optimize curative treatments for very early or early stage HCC patients. 2019

  18. Ma QP, Xu EJ, Zeng QJ, Su ZZ, Tan L, Chen JX, Zheng RQ, Li K (2019) Intraprocedural computed tomography/magnetic resonance-contrast-enhanced ultrasound fusion imaging improved thermal ablation effect of hepatocellular carcinoma: comparison with conventional ultrasound. Hepatol Res 49(7):799–809

    PubMed  Google Scholar 

  19. J B, M S, Hepatology J: Management of hepatocellular carcinoma. 2005, 42(5):1208–1236

  20. B P, report BAJG: Diagnosis of cirrhosis and portal hypertension: imaging, non-invasive markers of fibrosis and liver biopsy. 2017, 5(2):79–89

  21. JJM vG, A F, C P, A H, N A, V N, RGH B-T, JC F-R, S P, research AHJC: Computational radiomics system to decode the radiographic phenotype. 2017, 77(21):e104-e107

  22. hepatology JZgzbzzZgzCjo: [Diagnosis, management, and treatment of hepatocellular carcinoma (V2017)]. 2017, 25(12):886–895

  23. Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, Labow DM, Llovet JM, Schwartz ME (2009) A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology 137(3):850–855

    Article  Google Scholar 

  24. Miyata R, Tanimoto A, Wakabayashi G, Shimazu M, Nakatsuka S, Mukai M, Kitajima M (2006) Accuracy of preoperative prediction of microinvasion of portal vein in hepatocellular carcinoma using superparamagnetic iron oxide-enhanced magnetic resonance imaging and computed tomography during hepatic angiography. J Gastroenterol 41(10):987–995

    Article  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. Liang JD, Ping XO, Tseng YJ, Huang GT, Lai F, Yang PM (2014) Recurrence predictive models for patients with hepatocellular carcinoma after radiofrequency ablation using support vector machines with feature selection methods. Comput Methods Prog Biomed 117(3):425–434

    Article  Google Scholar 

  28. Wu CF, Wu YJ, Liang PC, Wu CH, Peng SF, Chiu HW (2017) Disease-free survival assessment by artificial neural networks for hepatocellular carcinoma patients after radiofrequency ablation. J Formosan Med Assoc 116(10):765–773

    Article  Google Scholar 

  29. Rennert J, Georgieva M, Schreyer AG, Jung W, Ross C, Stroszczynski C, Jung EM (2011) Image fusion of contrast enhanced ultrasound (CEUS) with computed tomography (CT) or magnetic resonance imaging (MRI) using volume navigation for detection, characterization and planning of therapeutic interventions of liver tumors. Clin Hemorheol Microcirc 49(1–4):67–81

    Article  CAS  Google Scholar 

  30. Strobel D, Bernatik T, Blank W, Schuler A, Greis C, Dietrich CF, Seitz K (2011) Diagnostic accuracy of CEUS in the differential diagnosis of small (</= 20 mm) and subcentimetric (</= 10 mm) focal liver lesions in comparison with histology. Results of the DEGUM multicenter trial. Ultraschall Medizin (Stuttgart, Germany : 1980) 32(6):593–597

    Article  CAS  Google Scholar 

  31. Schoenleber SJ, Kurtz DM, Talwalkar JA, Roberts LR, Gores GJ (2009) Prognostic role of vascular endothelial growth factor in hepatocellular carcinoma: systematic review and meta-analysis. Br J Cancer 100(9):1385–1392

    Article  CAS  Google Scholar 

  32. Huang KW, Yang SY, Yu CY, Chieh JJ, Yang CC, Horng HE, Hong CY, Yang HC, Wu CC (2011) Exploration of the relationship between the tumor burden and the concentration of vascular endothelial growth factor in liver-cancer-bearing animals using immunomagnetic reduction assay. J Biomed Nanotechnol 7(4):535–541

    Article  CAS  Google Scholar 

  33. K S, J S, H T, K T, K A, Y K, H I, Liver MFJLiojotIAftSot: Computer-aided diagnosis for estimating the malignancy grade of hepatocellular carcinoma using contrast-enhanced ultrasound: an ROC observer study. 2016, 36(7):1026–1032

  34. Gao Y, Zheng DY, Cui Z, Ma Y, Liu YZ, Zhang W (2015) Predictive value of quantitative contrast-enhanced ultrasound in hepatocellular carcinoma recurrence after ablation. World J Gastroenterol 21(36):10418–10426

    Article  CAS  Google Scholar 

  35. Tian H, Wang Q (2016) Quantitative analysis of microcirculation blood perfusion in patients with hepatocellular carcinoma before and after transcatheter arterial chemoembolisation using contrast-enhanced ultrasound. Eur J Cancer (Oxford, England : 1990) 68:82–89

    Article  Google Scholar 

  36. Zhuang PH, Xu L, Gao L, Lu W, Ruan LT, Yang J (2017) Correlations of microvascular blood flow of contrast-enhanced ultrasound and HGF/c-met signaling pathway with clinicopathological features and prognosis of patients with hepatocellular carcinoma. OncoTargets Ther 10:847–857

    Article  CAS  Google Scholar 

  37. Floriani I, Torri V, Rulli E, Garavaglia D, Compagnoni A, Salvolini L, Giovagnoni A (2010) Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging 31(1):19–31

    Article  Google Scholar 

  38. Welzel TM, Graubard BI, Zeuzem S, El-Serag HB, Davila JA, McGlynn KA (2011) Metabolic syndrome increases the risk of primary liver cancer in the United States: a study in the SEER-Medicare database. Hepatology (Baltimore, Md) 54(2):463–471

    Article  Google Scholar 

  39. M K, K U, Y O, M H, Y I, K A, K N, M K, T K, N I et al: B-mode ultrasonography versus contrast-enhanced ultrasonography for surveillance of hepatocellular carcinoma: a prospective multicenter randomized controlled trial. 2019, 8(4):271–280

  40. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38(2):200–207

    Article  Google Scholar 

  41. Poon RT (2009) Differentiating early and late recurrences after resection of HCC in cirrhotic patients: implications on surveillance, prevention, and treatment strategies. Ann Surg Oncol 16(4):792–794

    Article  Google Scholar 

  42. Hayashi M, Shimizu T, Hirokawa F, Inoue Y, Komeda K, Asakuma M, Miyamoto Y, Takeshita A, Shibayama Y, Tanigawa N (2011) Clinicopathological risk factors for recurrence within one year after initial hepatectomy for hepatocellular carcinoma. Am Surg 77(5):572–578

    Article  Google Scholar 

  43. Ziol M, Sutton A, Calderaro J, Barget N, Aout M, Leroy V, Blanc JF, Sturm N, Bioulac-Sage P, Nahon P, Nault JC, Charnaux N, N’Kontchou G, Trinchet JC, Delehedde M, Seror O, Beaugrand M, Vicaut E, Ganne-Carrié N (2013) ESM-1 expression in stromal cells is predictive of recurrence after radiofrequency ablation in early hepatocellular carcinoma. J Hepatol 59(6):1264–1270

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Key Research and Development Program of China under Grant No. 2017YFC0112000, National Natural Science Foundation of China (No. 81827802), the Science and Technology Planning Project of Guangzhou, China under Grant No. 201704020164 and Chinese Academy of Sciences (KFJ-STS-ZDTP-059 and YJKYYQ20180048).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Wang Kun, Rong-Qin Zheng or Jei Tian.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 1408 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, QP., He, Xl., Li, K. et al. Dynamic Contrast-Enhanced Ultrasound Radiomics for Hepatocellular Carcinoma Recurrence Prediction After Thermal Ablation. Mol Imaging Biol 23, 572–585 (2021). https://doi.org/10.1007/s11307-021-01578-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11307-021-01578-0

Key words

Navigation