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Risk stratification of solitary hepatocellular carcinoma ≤ 5 cm without microvascular invasion: prognostic values of MR imaging features based on LI-RADS and clinical parameters

  • Hepatobiliary-Pancreas
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Abstract

Objectives

To estimate the potential of preoperative MR imaging features and clinical parameters in the risk stratification of patients with solitary hepatocellular carcinoma (HCC) ≤ 5 cm without microvascular invasion (MVI) after hepatectomy.

Methods

The study enrolled 166 patients with histopathological confirmed MVI-negative HCC retrospectively. The MR imaging features were evaluated by two radiologists independently. The risk factors associated with recurrence-free survival (RFS) were identified by univariate Cox regression analysis and the least absolute shrinkage and selection operator Cox regression analysis. A predictive nomogram was developed based on these risk factors, and the performance was tested in the validation cohort. The RFS was analyzed by using the Kaplan–Meier survival curves and log-rank test.

Results

Among the 166 patients with solitary MVI-negative HCC, 86 patients presented with postoperative recurrence. Multivariate Cox regression analysis indicated that cirrhosis, tumor size, hepatitis, albumin, arterial phase hyperenhancement (APHE), washout, and mosaic architecture were risk factors associated with poor RFS and then incorporated into the nomogram. The nomogram achieved good performance with C-index values of 0.713 and 0.707 in the development and validation cohorts, respectively. Furthermore, patients were stratified into high- and low-risk subgroups, and significant prognostic differences were found between the different subgroups in both cohorts (p < 0.001 and p = 0.024, respectively).

Conclusion

The nomogram incorporated preoperative MR imaging features, and clinical parameters can be a simple and reliable tool for predicting RFS and achieving risk stratification in patients with solitary MVI-negative HCC.

Key Points

• Application of preoperative MR imaging features and clinical parameters can effectively predict RFS in patients with solitary MVI-negative HCC.

• Risk factors including cirrhosis, tumor size, hepatitis, albumin, APHE, washout, and mosaic architecture were associated with worse prognosis in patients with solitary MVI-negative HCC.

• Based on the nomogram incorporating these risk factors, the MVI-negative HCC patients could be stratified into two subgroups with significant different prognoses.

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Abbreviations

ALBI:

Albumin-bilirubin

APHE:

Arterial phase hyperenhancement

BCLC:

Barcelona Clinic Liver Cancer

CI:

Confidence intervals

HR:

Hazard ratios

HCC:

Hepatocellular carcinoma

LI-RADS:

Liver Imaging Reporting and Data System

MRI:

Magnetic resonance imaging

MVI:

Microvascular invasion

RFS:

Recurrence-free survival

References

  1. Sung H, Ferlay J, Siegel RL et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    Article  PubMed  Google Scholar 

  2. Marrero JA, Kulik LM, Sirlin CB et al (2018) Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the Study of Liver Diseases. Hepatology 68:723–750

    Article  PubMed  Google Scholar 

  3. Lei Z, Li J, Wu D et al (2016) Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the Milan criteria. JAMA Surg 151:356–363

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  PubMed Central  Google Scholar 

  5. Jiang H, Wei J, Fu F et al (2022) Predicting microvascular invasion in hepatocellular carcinoma: a dual-institution study on gadoxetate disodium-enhanced MRI. Liver Int 42:1158–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lin WP, **ng KL, Fu JC et al (2021) Development and validation of a model including distinct vascular patterns to estimate survival in hepatocellular carcinoma. JAMA Netw Open 4:e2125055

    Article  PubMed  PubMed Central  Google Scholar 

  7. Yao LQ, Chen ZL, Feng ZH et al (2022) Clinical features of recurrence after hepatic resection for early-stage hepatocellular carcinoma and long-term survival outcomes of patients with recurrence: a multi-institutional analysis. Ann Surg Oncol. https://doi.org/10.1245/s10434-022-11454-y

    Article  PubMed  PubMed Central  Google Scholar 

  8. Zhang L, Hu J, Hou J, Jiang X, Guo L, Tian L (2021) Radiomics-based model using gadoxetic acid disodium-enhanced MR images: associations with recurrence-free survival of patients with hepatocellular carcinoma treated by surgical resection. Abdom Radiol (NY) 46:3845–3854

    Article  PubMed  Google Scholar 

  9. Shen J, Wen J, Li C et al (2018) The prognostic value of microvascular invasion in early-intermediate stage hepatocelluar carcinoma: a propensity score matching analysis. BMC Cancer 18:278

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wang H, Wu MC, Cong WM (2019) Microvascular invasion predicts a poor prognosis of solitary hepatocellular carcinoma up to 2 cm based on propensity score matching analysis. Hepatol Res 49:344–354

    Article  CAS  PubMed  Google Scholar 

  11. 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 276:433–443

    Article  PubMed  Google Scholar 

  12. Zhang J, Liu X, Zhang H et al (2019) Texture analysis based on preoperative magnetic resonance imaging (MRI) and conventional MRI features for predicting the early recurrence of single hepatocellular carcinoma after hepatectomy. Acad Radiol 26:1164–1173

    Article  PubMed  Google Scholar 

  13. Ahn SJ, Kim JH, Park SJ, Kim ST, Han JK (2019) Hepatocellular carcinoma: preoperative gadoxetic acid-enhanced MR imaging can predict early recurrence after curative resection using image features and texture analysis. Abdom Radiol (NY) 44:539–548

    Article  PubMed  Google Scholar 

  14. Shinkawa H, Tanaka S, Kabata D et al (2021) The prognostic impact of tumor differentiation on recurrence and survival after resection of hepatocellular carcinoma is dependent on tumor size. Liver Cancer 10:461–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Dai CY, Lin CY, Tsai PC et al (2018) Impact of tumor size on the prognosis of hepatocellular carcinoma in patients who underwent liver resection. J Chin Med Assoc 81:155–163

    Article  PubMed  Google Scholar 

  16. Zhang L, Kuang S, Chen J et al (2019) The role of preoperative dynamic contrast-enhanced 3.0-T MR imaging in predicting early recurrence in patients with early-stage hepatocellular carcinomas after curative resection. Front Oncol 9:1336

  17. Wei H, Jiang H, Qin Y et al (2022) Comparison of a preoperative MR-based recurrence risk score versus the postoperative score and four clinical staging systems in hepatocellular carcinoma: a retrospective cohort study. Eur Radiol 32:7578–7589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chernyak V, Fowler KJ, Kamaya A et al (2018) Liver Imaging Reporting and Data System (LI-RADS) Version 2018: imaging of hepatocellular carcinoma in at-risk patients. Radiology 289:816–830

    Article  PubMed  Google Scholar 

  19. Johnson PJ, Berhane S, Kagebayashi C et al (2015) Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol 33:550–558

    Article  PubMed  Google Scholar 

  20. Ariizumi S, Kitagawa K, Kotera Y et al (2011) A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci 18:575–585

    Article  PubMed  Google Scholar 

  21. Wei Y, Pei W, Qin Y, Su D, Liao H (2021) Preoperative MR imaging for predicting early recurrence of solitary hepatocellular carcinoma without microvascular invasion. Eur J Radiol 138:109663

    Article  PubMed  Google Scholar 

  22. Lee S, Kim SH, Hwang JA, Lee JE, Ha SY (2019) Pre-operative ADC predicts early recurrence of HCC after curative resection. Eur Radiol 29:1003–1012

    Article  PubMed  Google Scholar 

  23. Hong SK, ** XL, Suh S et al (2022) Different risk factors for early and late recurrence after curative resection of hepatocellular carcinoma. World J Surg 46:197–206

    Article  PubMed  Google Scholar 

  24. Moon JY, Min JH, Kim YK et al (2021) Prognosis after curative resection of single hepatocellular carcinoma with a focus on LI-RADS targetoid appearance on preoperative gadoxetic acid-enhanced MRI. Korean J Radiol 22:1786–1796

    Article  PubMed  PubMed Central  Google Scholar 

  25. Liu S, Xu Z, Fang Z et al (2021) The combination of age, international standardized ratio, albumin and gamma-glutamyl transpeptidase (AIAG), tumor size and alpha fetoprotein (AFP) stage as the prognostic model for hepatitis B-related hepatocellular carcinoma. Int J Gen Med 14:4291–4301

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cerny M, Chernyak V, Olivie D et al (2018) LI-RADS Version 2018 ancillary features at MRI. Radiographics 38:1973–2001

    Article  PubMed  Google Scholar 

  27. Yang H, Han P, Huang M et al (2022) The role of gadoxetic acid-enhanced MRI features for predicting microvascular invasion in patients with hepatocellular carcinoma. Abdom Radiol (NY) 47:948–956

    Article  PubMed  Google Scholar 

  28. Chen J, Zhou J, Kuang S et al (2019) Liver Imaging Reporting and Data System category 5: MRI predictors of microvascular invasion and recurrence after hepatectomy for hepatocellular carcinoma. AJR Am J Roentgenol 213:821–830

    Article  PubMed  Google Scholar 

  29. Kim BJ, Choi SH, Kim SY et al (2022) Liver Imaging Reporting and Data System categories: long-term imaging outcomes in a prospective surveillance cohort. Liver Int 42:1648–1657

    Article  PubMed  Google Scholar 

  30. Villanueva A (2019) Hepatocellular carcinoma. N Engl J Med 380:1450–1462

    Article  CAS  PubMed  Google Scholar 

  31. Wu Z, Tang H, Wang L et al (2022) Postoperative survival analysis of hepatocellular carcinoma patients with liver cirrhosis based on propensity score matching. BMC Surg 22:103

    Article  PubMed  PubMed Central  Google Scholar 

  32. Ding DY, Liu L, Li HL et al (2022) Development of preoperative prognostic models including radiological features for survival of singular nodular HCC patients. Hepatobiliary Pancreat Dis Int 22:72-80

  33. Huang J, Liu FC, Li L, Zhou WP, Jiang BG, Pan ZY (2020) Nomograms to predict the long-time prognosis in patients with alpha-fetoprotein negative hepatocellular carcinoma following radical resection. Cancer Med 9:2791–2802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Liang B, Yao S, Zhou J, Li Z, Liu T (2018) Liver resection versus radiofrequency ablation for hepatitis B virus-related small hepatocellular carcinoma. J Hepatocell Carcinoma 5:1–7

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wu N, Chen G, Hu H, Pang L, Chen Z (2015) Low pretherapeutic serum albumin as a risk factor for poor outcome in esophageal squamous cell carcinomas. Nutr Cancer 67:481-485

  36. Gupta D, Lis CG (2010) Pretreatment serum albumin as a predictor of cancer survival: a systematic review of the epidemiological literature. Nutr J 9:69

    Article  PubMed  PubMed Central  Google Scholar 

  37. Zhao Y, Huang F, Liu S et al (2022) Prediction of therapeutic response of unresectable hepatocellular carcinoma to hepatic arterial infusion chemotherapy based on pretherapeutic MRI radiomics and albumin-bilirubin score. J Cancer Res Clin Oncol. https://doi.org/10.1007/s00432-022-04467-3

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study is supported by the National Key Research and Development Program of China (No. 2020AAA0109503).

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Correspondence to **aohong Ma or **nming Zhao.

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The scientific guarantor of this publication is **nming Zhao.

Conflict of interest

One of the authors (Sicong Wang) is an employee of General Electric Healthcare China. The remaining authors declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

Sicong Wang kindly provided statistical advice for this manuscript.

One of the authors has significant statistical expertise.

No complex statistical methods were necessary for this paper.

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Written informed consent was waived by the institutional review board.

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Institutional review board approval was obtained.

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• performed at one institution

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Wang, L., Feng, B., Li, D. et al. Risk stratification of solitary hepatocellular carcinoma ≤ 5 cm without microvascular invasion: prognostic values of MR imaging features based on LI-RADS and clinical parameters. Eur Radiol 33, 3592–3603 (2023). https://doi.org/10.1007/s00330-023-09484-5

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