Log in

Prognostic significance of MRI features in patients with solitary large hepatocellular carcinoma following surgical resection

  • Hepatobiliary-Pancreas
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

To assess the prognostic impact of preoperative MRI features on outcomes for single large hepatocellular carcinoma (HCC) (≥ 8 cm) after surgical resection.

Material and methods

This retrospective study included 151 patients (mean age: 59.2 years; 126 men) with a single large HCC who underwent gadoxetic acid-enhanced MRI and surgical resection between 2008 and 2020. Clinical variables, including tumor markers and MRI features (tumor size, tumor margin, and the proportion of hypovascular component on hepatic arterial phase (AP) (≥ 50% vs. < 50% tumor volume) were evaluated. Cox proportional hazards model analyzed overall survival (OS), recurrence-free survival (RFS), and associated factors.

Results

Among 151 HCCs, 37.8% and 62.2% HCCs were classified as ≥ 50% and < 50% AP hypovascular groups, respectively. The 5- and 10-year OS and RFS rates in all patients were 62.0%, 52.6% and 41.4%, 38.5%, respectively. Multivariable analysis revealed that ≥ 50% AP hypovascular group (hazard ratio [HR] 1.7, p = 0.048), tumor size (HR 1.1, p = 0.006), and alpha-fetoprotein ≥ 400 ng/mL (HR 2.6, p = 0.001) correlated with poorer OS. ≥ 50% AP hypovascular group (HR 1.9, p = 0.003), tumor size (HR 1.1, p = 0.023), and non-smooth tumor margin (HR 2.1, p = 0.009) were linked to poorer RFS. One-year RFS rates were lower in the ≥ 50% AP hypovascular group than in the < 50% AP hypovascular group (47.4% vs 66.9%, p = 0.019).

Conclusion

MRI with ≥ 50% AP hypovascular component and larger tumor size were significant factors associated with poorer OS and RFS after resection of single large HCC (≥ 8 cm). These patients require careful multidisciplinary management to determine optimal treatment strategies.

Clinical relevance statement

Preoperative MRI showing a ≥ 50% arterial phase hypovascular component and larger tumor size can predict worse outcomes after resection of single large hepatocellular carcinomas (≥ 8 cm), underscoring the need for tailored, multidisciplinary treatment strategies.

Key Points

  • MRI features offer insights into the postoperative prognosis for large hepatocellular carcinoma.

  • Hypovascular component on arterial phase ≥ 50% and tumor size predicted poorer overall survival and recurrence-free survival.

  • These findings can assist in prioritizing aggressive and multidisciplinary approaches for patients at risk for poor outcomes.

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

Similar content being viewed by others

Abbreviations

AFP:

Alpha-fetoprotein

ALBI:

Albumin-bilirubin

APHE:

Arterial phase hyperenhancement

BCLC:

Barcelona clinic liver cancer

CI:

Confidence interval

HCC:

Hepatocellular carcinoma

HR:

Hazard ratio

MTM:

Macrotrabecular-massive

NHHN:

Nonhypervascular hypointense nodule

OS:

Overall survival

PIVKA-II:

Protein induced by vitamin K absence-II

RFS:

Recurrence-free survival

TARE:

Transarterial radioembolization

References

  1. Reig M, Forner A, Rimola J et al (2022) BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol 76:681–693

    Article  PubMed  Google Scholar 

  2. Portolani N, Coniglio A, Ghidoni S et al (2006) Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann Surg 243:229–235

    Article  PubMed  PubMed Central  Google Scholar 

  3. **ng H, Zhang WG, Cescon M et al (2020) Defining and predicting early recurrence after liver resection of hepatocellular carcinoma: a multi-institutional study. HPB (Oxford) 22:677–689

    Article  PubMed  Google Scholar 

  4. Imamura H, Matsuyama Y, Tanaka E et al (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207

    Article  PubMed  Google Scholar 

  5. Shah SA, Greig PD, Gallinger S et al (2006) Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg 202:275–283

    Article  PubMed  Google Scholar 

  6. Takeishi K, Maeda T, Tsujita E et al (2015) Predictors of intrahepatic multiple recurrences after curative hepatectomy for hepatocellular carcinoma. Anticancer Res 35:3061–3066

    PubMed  Google Scholar 

  7. Joo I, Lee JM (2016) Recent advances in the imaging diagnosis of hepatocellular carcinoma: value of gadoxetic acid-enhanced MRI. Liver Cancer 5:67–87

    Article  CAS  PubMed  Google Scholar 

  8. Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology 273:30–50

    Article  PubMed  Google Scholar 

  9. Kim YY, Park MS, Aljoqiman KS, Choi JY, Kim MJ (2019) Gadoxetic acid-enhanced magnetic resonance imaging: hepatocellular carcinoma and mimickers. Clin Mol Hepatol 25:223–233

    Article  PubMed  PubMed Central  Google Scholar 

  10. European Association for the Study of the Liver (2018) EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol 69:182–236

  11. Choi SY, Kim SH, Park CK et al (2018) Imaging features of gadoxetic acid-enhanced and diffusion-weighted MR imaging for identifying cytokeratin 19-positive hepatocellular carcinoma: a retrospective observational study. Radiology 286:897–908

    Article  PubMed  Google Scholar 

  12. Rhee H, Cho ES, Nahm JH et al (2021) Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol 74:109–121

    Article  CAS  PubMed  Google Scholar 

  13. Cha H, Choi J-Y, Park YN et al (2023) Comparison of imaging findings of macrotrabecular-massive hepatocellular carcinoma using CT and gadoxetic acid–enhanced MRI. Eur Radiol 33:1364–1377

    Article  CAS  PubMed  Google Scholar 

  14. Poon RT-P, Fan ST, Wong J (2002) Selection criteria for hepatic resection in patients with large hepatocellular carcinoma larger than 10 cm in diameter1 1No competing interests declared. J Am Coll Surg 194:592–602

    Article  PubMed  Google Scholar 

  15. ** YJ, Lee JW, Choi YJ et al (2014) Surgery versus transarterial chemoembolization for solitary large hepatocellular carcinoma of BCLC stage A. J Gastrointest Surg 18:555–561

    Article  PubMed  Google Scholar 

  16. Zhong JH, Pan LH, Wang YY et al (2017) Optimizing stage of single large hepatocellular carcinoma: a study with subgroup analysis by tumor diameter. Medicine (Baltimore) 96:e6608

    Article  PubMed  Google Scholar 

  17. Toyoda H, Kumada T, Tada T et al (2013) Non-hypervascular hypointense nodules detected by Gd-EOB-DTPA-enhanced MRI are a risk factor for recurrence of HCC after hepatectomy. J Hepatol 58:1174–1180

    Article  PubMed  Google Scholar 

  18. Lee S, Kim SH, Lee JE, Sinn DH, Park CK (2017) Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. J Hepatol 67:526–534

    Article  CAS  PubMed  Google Scholar 

  19. Kim H, Park MS, Choi JY et al (2009) Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol 19:1744–1751

    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. 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 

  22. Shimada M, Rikimaru T, Hamatsu T et al (2001) The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg 182:177–182

    Article  CAS  PubMed  Google Scholar 

  23. Wei T, Zhang XF, Bagante F et al (2021) Tumor necrosis impacts prognosis of patients undergoing curative-intent hepatocellular carcinoma. Ann Surg Oncol 28:797–805

    Article  PubMed  Google Scholar 

  24. Takano M, Shimada K, Fujii T et al (2016) Keratin 19 as a key molecule in progression of human hepatocellular carcinomas through invasion and angiogenesis. BMC Cancer 16:903

    Article  PubMed  PubMed Central  Google Scholar 

  25. Cox DR (1975) Partial likelihood. Biometrika 62:269–276

    Article  Google Scholar 

  26. Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509

    Article  Google Scholar 

  27. Korean Liver Cancer Association (KLCA) and National Cancer Center (NCC) Korea (2022) 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma. Korean J Radiol 23:1126–1240

    Article  Google Scholar 

  28. Yamashita Y, Taketomi A, Shirabe K et al (2011) Outcomes of hepatic resection for huge hepatocellular carcinoma (≥10 cm in diameter). J Surg Oncol 104:292–298

    Article  PubMed  Google Scholar 

  29. Shah SA, Wei AC, Cleary SP et al (2007) Prognosis and results after resection of very large (>or = 10 cm) hepatocellular carcinoma. J Gastrointest Surg 11:589–595

    Article  PubMed  Google Scholar 

  30. Pandey D, Lee KH, Wai CT, Wagholikar G, Tan KC (2007) Long term outcome and prognostic factors for large hepatocellular carcinoma (10 cm or more) after surgical resection. Ann Surg Oncol 14:2817–2823

    Article  PubMed  Google Scholar 

  31. Vitale A, Burra P, Frigo AC et al (2015) Survival benefit of liver resection for patients with hepatocellular carcinoma across different Barcelona Clinic Liver Cancer stages: a multicentre study. J Hepatol 62:617–624

    Article  PubMed  Google Scholar 

  32. Hong SK, Lee KW, Lee S et al (2022) Impact of tumor size on hepatectomy outcomes in hepatocellular carcinoma: a nationwide propensity score matching analysis. Ann Surg Treat Res 102:193–204

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kim J, Kim JY, Lee JH et al (2022) Long-term outcomes of transarterial radioembolization for large single hepatocellular carcinoma: a comparison to resection. J Nucl Med 63:1215–1222

    Article  CAS  PubMed  Google Scholar 

  34. Gu K-w, Kim YK, Min JH, Ha SY, Jeong WK (2017) Imaging features of hepatic sarcomatous carcinoma on computed tomography and gadoxetic acid-enhanced magnetic resonance imaging. Abdom Radiol (NY) 42:1424–1433

    Article  PubMed  Google Scholar 

  35. Low HM, Lee JM, Tan CH (2023) Prognosis prediction of hepatocellular carcinoma based on magnetic resonance imaging features. Korean J Radiol 24:660–667

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ling YH, Chen JW, Wen SH et al (2020) Tumor necrosis as a poor prognostic predictor on postoperative survival of patients with solitary small hepatocellular carcinoma. BMC Cancer 20:607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zhang J, Zhang Q, Lou Y et al (2018) Hypoxia-inducible factor-1alpha/interleukin-1beta signaling enhances hepatoma epithelial-mesenchymal transition through macrophages in a hypoxic-inflammatory microenvironment. Hepatology 67:1872–1889

    Article  CAS  PubMed  Google Scholar 

  38. Rhee H, Chung T, Yoo JE et al (2020) Gross type of hepatocellular carcinoma reflects the tumor hypoxia, fibrosis, and stemness-related marker expression. Hepatol Int 14:239–248

    Article  PubMed  Google Scholar 

  39. Jain RK (2014) Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell 26:605–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Calderaro J, Couchy G, Imbeaud S et al (2017) Histological subtypes of hepatocellular carcinoma are related to gene mutations and molecular tumour classification. J Hepatol 67:727–738

    Article  CAS  PubMed  Google Scholar 

  41. Ziol M, Poté N, Amaddeo G et al (2018) Macrotrabecular-massive hepatocellular carcinoma: a distinctive histological subtype with clinical relevance. Hepatology 68:103–112

    Article  PubMed  Google Scholar 

  42. Mulé S, Pregliasco AG, Tenenhaus A et al (2020) Multiphase liver MRI for identifying the macrotrabecular-massive subtype of hepatocellular carcinoma. Radiology 295:562–571

    Article  PubMed  Google Scholar 

  43. Tan PS, Nakagawa S, Goossens N et al (2016) Clinicopathological indices to predict hepatocellular carcinoma molecular classification. Liver Int 36:108–118

    Article  CAS  PubMed  Google Scholar 

  44. Li Q, Wei Y, Zhang T et al (2023) Predictive models and early postoperative recurrence evaluation for hepatocellular carcinoma based on gadoxetic acid-enhanced MR imaging. Insights Imaging 14:4

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kim SJ, Kim JM (2022) Prediction models of hepatocellular carcinoma recurrence after liver transplantation: a comprehensive review. Clin Mol Hepatol 28:739–753

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kudo M, Kitano M, Sakurai T, Nishida N (2015) General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the Liver Cancer Study Group of Japan. Dig Dis 33:765–770

    Article  PubMed  Google Scholar 

Download references

Funding

The authors state that this work has not received any funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ji Hye Min.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Ji Hye Min in Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

Sun-Young Baek, one of the authors, has significant statistical expertise.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

The Institutional Review Board of the Samsung Medical Center (IRB number: 2023-04-085) approved this study.

Study subjects or cohorts overlap

No study subjects or cohorts overlap.

Methodology

  • Retrospective

  • Observational

  • Performed at one institution

Additional information

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

Supplementary information

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gu, K., Min, J.H., Lee, J.H. et al. Prognostic significance of MRI features in patients with solitary large hepatocellular carcinoma following surgical resection. Eur Radiol (2024). https://doi.org/10.1007/s00330-024-10780-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00330-024-10780-x

Keywords

Navigation