Skip to main content

Advertisement

Log in

Pre-operative Microvascular Invasion Prediction Using Multi-parametric Liver MRI Radiomics

  • Original Paper
  • Published:
Journal of Digital Imaging Aims and scope Submit manuscript

Abstract

Microvascular invasion (mVI) is the most significant independent predictor of recurrence for hepatocellular carcinoma (HCC), but its pre-operative assessment is challenging. In this study, we investigate the use of multi-parametric MRI radiomics to predict mVI status before surgery. We retrospectively collected pre-operative multi-parametric liver MRI scans for 99 patients who were diagnosed with HCC. These patients received surgery and pathology-confirmed diagnosis of mVI. We extracted radiomics features from manually segmented HCC regions and built machine learning classifiers to predict mVI status. We compared the performance of such classifiers when built on five MRI sequences used both individually and combined. We investigated the effects of using features extracted from the tumor region only, the peritumoral marginal region only, and the combination of the two. We used the area under the receiver operating characteristic curve (AUC) and accuracy as performance metrics. By combining features extracted from multiple MRI sequences, AUCs are 86.69%, 84.62%, and 84.19% when features are extracted from the tumor only, the peritumoral region only, and the combination of the two, respectively. For tumor-extracted features, the T2 sequence (AUC = 80.84%) and portal venous sequence (AUC = 79.22%) outperform other MRI sequences in single-sequence-based models and their combination yields the highest AUC of 86.69% for mVI status prediction. Our results show promise in predicting mVI from pre-operative liver MRI scans and indicate that information from multi-parametric MRI sequences is complementary in identifying mVI.

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

Similar content being viewed by others

Notes

  1. https://pyradiomics.readthedocs.io/en/latest/features.html, last accessed Jan. 7th, 2019

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018. https://doi.org/10.3322/caac.21492

  2. Petrick JL, Braunlin M, Laversanne M, Valery PC, Bray F, Mcglynn KA. International trends in liver cancer incidence, overall and by histologic subtype, 1978-2007. UICC Int J Cancer IJC. 2016;139:1534–1545. https://doi.org/10.1002/ijc.30211

    Article  CAS  Google Scholar 

  3. Petrick JL, Kelly SP, Altekruse SF, McGlynn KA, Rosenberg PS. Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol. 2016;34(15):1787–1794. https://doi.org/10.1200/JCO.2015.64.7412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Altekruse SF, McGlynn KA, Reichman ME. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol. 2009;27(9):1485–1491. https://doi.org/10.1200/JCO.2008.20.7753

    Article  PubMed  PubMed Central  Google Scholar 

  5. Greten TF, Papendorf F, Bleck JS, et al. Survival rate in patients with hepatocellular carcinoma: a retrospective analysis of 389 patients. Br J Cancer. 2005;92(10):1862–1868. https://doi.org/10.1038/sj.bjc.6602590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet. 2012;379(9822):1245–1255. https://doi.org/10.1016/S0140-6736(11)61347-0

    Article  PubMed  Google Scholar 

  7. Llovet J, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis. 1999;19(03):329–338. https://doi.org/10.1055/s-2007-1007122

    Article  CAS  PubMed  Google Scholar 

  8. Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68(2):723–750. https://doi.org/10.1002/hep.29913

    Article  PubMed  Google Scholar 

  9. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334(11):693–700. https://doi.org/10.1056/NEJM199603143341104

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  11. Halazun KJ, Najjar M, Abdelmessih RM, et al. Recurrence after liver transplantation for hepatocellular carcinoma. Ann Surg. 2017;265(3):557–564. https://doi.org/10.1097/SLA.0000000000001966

    Article  PubMed  Google Scholar 

  12. Escartin A, Sapisochin G, Bilbao I, et al. Recurrence of hepatocellular carcinoma after liver transplantation. Transplant Proc. 2007;39(7):2308–2310. https://doi.org/10.1016/J.TRANSPROCEED.2007.06.042

    Article  CAS  PubMed  Google Scholar 

  13. Mazzaferro V, Llovet JM, Miceli R, et al. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol. 2009;10(1):35–43. https://doi.org/10.1016/S1470-2045(08)70284-5

    Article  PubMed  Google Scholar 

  14. Pawlik TM, Gleisner AL, Anders RA, Assumpcao L, Maley W, Choti MA. Preoperative assessment of hepatocellular carcinoma tumor grade using needle biopsy: implications for transplant eligibility. Ann Surg. 2007;245(3):435–442. https://doi.org/10.1097/01.sla.0000250420.73854.ad

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sterling RK, Wright EC, Morgan TR, et al. Frequency of elevated hepatocellular carcinoma (HCC) biomarkers in patients with advanced hepatitis C. Am J Gastroenterol. 2012;107(1):64–74. https://doi.org/10.1038/ajg.2011.312

    Article  CAS  PubMed  Google Scholar 

  16. Gupta S, Bent S, Kohlwes J. Test characteristics of α-fetoprotein for detecting hepatocellular carcinoma in patients with hepatitis C: a systematic review and critical analysis. Ann Intern Med. 2003;139(1):46–50. http://annals.org/aim/fullarticle/716520. Accessed Dec 4, 2018.

    Article  CAS  Google Scholar 

  17. Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transplant. 2005;11(9):1086–1092. https://doi.org/10.1002/lt.20472

    Article  Google Scholar 

  18. Roayaie S, Frischer JS, Emre SH, et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters. Ann Surg. 2002;235(4):533–539. http://www.ncbi.nlm.nih.gov/pubmed/11923610. Accessed January 4, 2019.

    Article  Google Scholar 

  19. Ünal E, İdilman İS, Akata D, Özmen MN, Karçaaltıncaba M. Microvascular invasion in hepatocellular carcinoma. Diagnostic Interv Radiol. 2016;22(2):125–132. https://doi.org/10.5152/dir.2015.15125

    Article  Google Scholar 

  20. Renzulli M, Brocchi S, Cucchetti A, et al. Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology. 2016;279(2):432–442. https://doi.org/10.1148/radiol.2015150998

    Article  PubMed  Google Scholar 

  21. Chou C-T, Chen R-C, Lin W-C, Ko C-J, Chen C-B, Chen Y-L. Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. Am J Roentgenol. 2014;203(3):W253–W259. https://doi.org/10.2214/AJR.13.10595

    Article  Google Scholar 

  22. Yang C, Wang H, Sheng R, Ji Y, Rao S, Zeng M. Microvascular invasion in hepatocellular carcinoma: is it predictable with a new, preoperative application of diffusion-weighted imaging? Clin Imaging. 2017;41(2017):101–105. https://doi.org/10.1016/j.clinimag.2016.10.004

    Article  PubMed  Google Scholar 

  23. Lei Z, Li J, Wu D, et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus–related hepatocellular carcinoma within the Milan criteria. JAMA Surg. 2016;151(4):356. https://doi.org/10.1001/jamasurg.2015.4257

    Article  PubMed  Google Scholar 

  24. Kim H, Park MS, Choi JY, et al. Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol. 2009;19(7):1744–1751. https://doi.org/10.1007/s00330-009-1331-8

    Article  PubMed  Google Scholar 

  25. Kim KA, Kim M-J, Jeon HM, et al. Prediction of microvascular invasion of hepatocellular carcinoma: usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. J Magn Reson Imaging. 2012;35:629–634. https://doi.org/10.1002/jmri.22876

    Article  PubMed  Google Scholar 

  26. Bakr S, Echegaray S, Shah R, Kamaya A, Louie J. Noninvasive radiomics signature based on quantitative analysis of computed tomography images as a surrogate for microvascular invasion in hepatocellular carcinoma: a pilot study. J Med Imaging. 2017;4(04):1. https://doi.org/10.1117/1.JMI.4.4.041303

    Article  Google Scholar 

  27. Li H, Zhang J, Zheng Z, et al. Preoperative histogram analysis of intravoxel incoherent motion (IVIM) for predicting microvascular invasion in patients with single hepatocellular carcinoma. Eur J Radiol. 2018;105(January):65–71. https://doi.org/10.1016/j.ejrad.2018.05.032

    Article  PubMed  Google Scholar 

  28. Ahn SJ, Kim JH, Park SJ, Kim ST, Han JK. Hepatocellular carcinoma: preoperative gadoxetic acid–enhanced MR imaging can predict early recurrence after curative resection using image features and texture analysis. Abdominal Radiology. http://link.springer.com/10.1007/s00261-018-1768-9. Published September 18, 2018. Accessed Oct 18, 2018.

  29. Feng ST, Jia Y, Liao B, et al. Preoperative prediction of microvascular invasion in hepatocellular cancer: a radiomics model using Gd-EOB-DTPA-enhanced MRI. Eur Radiol. 2019;29(9):4648–4659. https://doi.org/10.1007/s00330-018-5935-8

    Article  PubMed  Google Scholar 

  30. Sumie S, Nakashima O, Okuda K, et al. The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol. 2014;21(3):1002–1009. https://doi.org/10.1245/s10434-013-3376-9

    Article  PubMed  Google Scholar 

  31. Semelka RC, Kelekis NL, Thomasson D, Brown MA, Laub GA. HASTE MR imaging: description of technique and preliminary results in the abdomen. Vol 6.; 1996. https://doi.org/10.1002/jmri.1880060420

  32. Runge VM, Wood ML, Kaufman DM, Kevin Nelson ML, Traill MR. FLASH: clinical three-dimensional magnetic resonance imaging. Vol 8.; 1988. https://pubs.rsna.org/doi/pdf/10.1148/radiographics.8.5.3227132. Accessed Jan 4, 2019.

  33. Rofsky NM, Lee VS, Laub G, et al. Abdominal MR imaging with a volumetric interpolated breath-hold examination. Radiology. 1999;212(3):876–884. https://doi.org/10.1148/radiology.212.3.r99se34876

    Article  CAS  PubMed  Google Scholar 

  34. Roayaie S, Blume IN, Thung SN, et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137(3):850–855. https://doi.org/10.1053/j.gastro.2009.06.003

    Article  PubMed  PubMed Central  Google Scholar 

  35. Van Griethuysen JJM, Fedorov A, Parmar C, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77(21):e104–e107. https://doi.org/10.1158/0008-5472.CAN-17-0339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tibshirani R. Regression shrinkage and selection via the lasso: a retrospective. J R Stat Soc Ser B (Statistical Methodol). 2011;73(3):273–282. https://doi.org/10.1111/j.1467-9868.2011.00771.x

    Article  Google Scholar 

  37. Tahmassebi A, Wengert GJ, Helbich TH, et al. Impact of machine learning with multiparametric magnetic resonance imaging of the breast for early prediction of response to neoadjuvant chemotherapy and survival outcomes in breast cancer patients. Invest Radiol. 2019;54(2):110–117. https://doi.org/10.1097/RLI.0000000000000518

    Article  PubMed  PubMed Central  Google Scholar 

  38. Edmondson HA, Steiner PE. Primary carcinoma of the liver.A study of 100 cases among 48,900 necropsies. Cancer. 1954;7(3):462–503. https://doi.org/10.1002/1097-0142(195405)7:3<462::AID-CNCR2820070308>3.0.CO;2-E

    Article  CAS  PubMed  Google Scholar 

  39. Chandarana H, Robinson E, Hajdu CH, Drozhinin L, Babb JS, Taouli B. Microvascular invasion in hepatocellular carcinoma: is it predictable with pretransplant MRI? Am J Roentgenol. 2011;196(5):1083–1089. https://doi.org/10.2214/AJR.10.4720

    Article  Google Scholar 

Download references

Funding

This work was supported by National Institutes of Health (NIH)/National Cancer Institute (NCI) grants (#1R01CA193603, #3R01CA193603-03S1, and #1R01CA218405), a Radiological Society of North America (RSNA) Research Scholar Grant (#RSCH1530), an Amazon AWS Machine Learning Research Award, and a University of Pittsburgh Physicians (UPP) Academic Foundation Award.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xinxiang Zhao or Shandong Wu.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nebbia, G., Zhang, Q., Arefan, D. et al. Pre-operative Microvascular Invasion Prediction Using Multi-parametric Liver MRI Radiomics. J Digit Imaging 33, 1376–1386 (2020). https://doi.org/10.1007/s10278-020-00353-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10278-020-00353-x

Keywords

Navigation