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Imaging and prognostic characterization of fat-containing hepatocellular carcinoma subtypes

  • Abdominal Radiology
  • Published:
La radiologia medica

Abstract

Purpose

Steatohepatitic hepatocellular carcinoma (SH-HCC) is characterized by intratumoral fat with > 50% inflammatory changes. However, intratumoral fat (with or without inflammation) can also be found in not-otherwise specified HCC (NOS-HCC). We compared the imaging features and outcome of resected HCC containing fat on pathology including SH-HCC (> 50% steatohepatitic component), NOS-HCC with < 50% steatohepatitic component (SH-NOS-HCC), and fatty NOS-HCC (no steatohepatitic component).

Material and methods

From September 2012 to June 2021, 94 patients underwent hepatic resection for fat-containing HCC on pathology. Imaging features and categories were assessed using LIRADS v2018. Fat quantification was performed on chemical-shift MRI. Recurrence-free and overall survival were estimated.

Results

Twenty-one patients (26%) had nonalcoholic steatohepatitis (NASH). The median intra-tumoral fat fraction was 8%, with differences between SH-HCC and SH-NOS-HCC (9.5% vs. 5% p = 0.03). There was no difference in major LI-RADS features between all groups; most tumors were classified as LR-4/5. A mosaic architecture on MRI was rare (7%) in SH-HCC, a fat in mass on CT was more frequently depicted (48%) in SH-HCC. A combination of NASH with no mosaic architecture on MRI or NASH with fat in mass on CT yielded excellent specificity for diagnosing SH-HCC (97.6% and 97.7%, respectively). The median recurrence-free and overall survival were 58 and 87 months, with no difference between groups (p = 0.18 and p = 0.69).

Conclusion

In patients with NASH, an SH-HCC may be suspected in L4/LR-5 observations with no mosaic architecture at MRI or with fat in mass on CT. Oncological outcomes appear similar between fat-containing HCC subtypes.

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References

  1. Cancer (IARC) TIA for R on Global Cancer Observatory. https://gco.iarc.fr/. Accessed 18 Apr 2022

  2. WHO Classification of Tumours. Digestive System Tumours. Fifth Edition—WHO. Accessed 20 Apr 2020

  3. 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. https://doi.org/10.1016/j.jhep.2017.05.014

    Article  CAS  PubMed  Google Scholar 

  4. Ziol M, Poté N, Amaddeo G et al (2018) Macrotrabecular-massive hepatocellular carcinoma: a distinctive histological subtype with clinical relevance. Hepatology 68:103–112. https://doi.org/10.1002/hep.29762

    Article  PubMed  Google Scholar 

  5. Salomao M, Yu WM, Brown RS, Emond JC (2010) Steatohepatitic hepatocellular carcinoma (SH-HCC). Am J Surg Pathol 34:7

    Article  Google Scholar 

  6. Shafizadeh N, Kakar S (2013) Hepatocellular carcinoma. Surg Pathol Clin 6:367–384. https://doi.org/10.1016/j.path.2013.03.007

    Article  PubMed  Google Scholar 

  7. Shibahara J, Ando S, Sakamoto Y et al (2014) Hepatocellular carcinoma with steatohepatitic features: a clinicopathological study of Japanese patients. Histopathology 64:951–962. https://doi.org/10.1111/his.12343

    Article  PubMed  Google Scholar 

  8. Salomao M, Remotti H, Vaughan R et al (2012) The steatohepatitic variant of hepatocellular carcinoma and its association with underlying steatohepatitis. Hum Pathol 43:737–746. https://doi.org/10.1016/j.humpath.2011.07.005

    Article  PubMed  Google Scholar 

  9. Taniai M, Hashimoto E, Tobari M et al (2018) Clinicopathological investigation of steatohepatitic hepatocellular carcinoma: a multicenter study using immunohistochemical analysis of adenoma-related markers: clinicopathological investigation of steatohepatitic hepatocellular carcinoma. Hepatol Res 48:947–955. https://doi.org/10.1111/hepr.13203

    Article  CAS  PubMed  Google Scholar 

  10. Jain D, Nayak NC, Kumaran V, Saigal S (2013) Steatohepatitic hepatocellular carcinoma, a morphologic indicator of associated metabolic risk factors: a study from India. Arch Pathol Lab Med 137:961–966. https://doi.org/10.5858/arpa.2012-0048-OA

    Article  PubMed  Google Scholar 

  11. Olofson AM, Gonzalo DH, Chang M, Liu X (2018) Steatohepatitic variant of hepatocellular carcinoma: a focused review. Gastroenterol Res 11:391–396. https://doi.org/10.14740/gr1110

    Article  CAS  Google Scholar 

  12. Ando S, Shibahara J, Hayashi A, Fukayama M (2015) β-catenin alteration is rare in hepatocellular carcinoma with steatohepatitic features: immunohistochemical and mutational study. Virchows Arch 467:535–542. https://doi.org/10.1007/s00428-015-1836-2

    Article  CAS  PubMed  Google Scholar 

  13. Lee JS, Yoo JE, Kim H et al (2017) Tumor stroma with senescence-associated secretory phenotype in steatohepatitic hepatocellular carcinoma. PLoS ONE 12:e0171922. https://doi.org/10.1371/journal.pone.0171922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fujiwara N, Nakagawa H, Enooku K et al (2018) CPT2 downregulation adapts HCC to lipid-rich environment and promotes carcinogenesis via acylcarnitine accumulation in obesity. Gut 67:1493–1504. https://doi.org/10.1136/gutjnl-2017-315193

    Article  CAS  PubMed  Google Scholar 

  15. Cannella R, Dioguardi Burgio M, Beaufrère A et al (2021) Imaging features of histological subtypes of hepatocellular carcinoma: implication for LI-RADS. JHEP Rep 3:100380. https://doi.org/10.1016/j.jhepr.2021.100380

    Article  PubMed  PubMed Central  Google Scholar 

  16. Inui S, Kondo H, Tanahashi Y et al (2021) Steatohepatitic hepatocellular carcinoma: imaging findings with clinicopathological correlation. Clin Radiol 76:160.e15-160.e25. https://doi.org/10.1016/j.crad.2020.09.011

    Article  CAS  PubMed  Google Scholar 

  17. Mulé S (2023) MRI features associated with HCC histologic subtypes: a western American and European bicenter study. Eur Radiol 33:1342

    Article  PubMed  Google Scholar 

  18. Yamaoka K, Saitoh S, Kinowaki K et al (2022) Clinicopathological assessment of steatohepatitic hepatocellular carcinoma. Clin Res Hepatol Gastroenterol 46:101799. https://doi.org/10.1016/j.clinre.2021.101799

    Article  CAS  PubMed  Google Scholar 

  19. Park JH, Park YN, Kim M-J et al (2023) Steatotic hepatocellular carcinoma: association of MRI findings to underlying liver disease and clinicopathological characteristics. Liver Int 43:1332–1344. https://doi.org/10.1111/liv.15589

    Article  CAS  PubMed  Google Scholar 

  20. Kambadakone AR, Fung A, Gupta RT et al (2018) LI-RADS technical requirements for CT, MRI, and contrast-enhanced ultrasound. Abdom Radiol 43:56–74. https://doi.org/10.1007/s00261-017-1325-y

    Article  Google Scholar 

  21. CT/MRI LI-RADS v2018. https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/CT-MRI-LI-RADS-v2018. Accessed 18 Apr 2022

  22. Chiang H-J, Lin L-H, Li C-W et al (2014) Magnetic resonance fat quantification in living donor liver transplantation. Transplant Proc 46:666–668. https://doi.org/10.1016/j.transproceed.2013.11.050

    Article  PubMed  Google Scholar 

  23. Kim HJ, Cho HJ, Kim B et al (2019) Accuracy and precision of proton density fat fraction measurement across field strengths and scan intervals: a phantom and human study. J Magn Reson Imaging JMRI 50:305–314. https://doi.org/10.1002/jmri.26575

    Article  PubMed  Google Scholar 

  24. Idilman IS, Tuzun A, Savas B et al (2015) Quantification of liver, pancreas, kidney, and vertebral body MRI-PDFF in non-alcoholic fatty liver disease. Abdom Imaging 40:1512–1519. https://doi.org/10.1007/s00261-015-0385-0

    Article  PubMed  Google Scholar 

  25. Hui SCN, So H-K, Chan DFY et al (2018) Validation of water-fat MRI and proton MRS in assessment of hepatic fat and the heterogeneous distribution of hepatic fat and iron in subjects with non-alcoholic fatty liver disease. Eur J Radiol 107:7–13. https://doi.org/10.1016/j.ejrad.2018.08.008

    Article  PubMed  Google Scholar 

  26. Hussain HK, Chenevert TL, Londy FJ et al (2005) Hepatic fat fraction: MR imaging for quantitative measurement and display—early experience. Radiology 237:1048–1055. https://doi.org/10.1148/radiol.2373041639

    Article  PubMed  Google Scholar 

  27. Trapani L, Beaufrère A, Hobeika C et al (2023) Pathological overview of steatohepatitic hepatocellular carcinoma in a surgical series. Histopathology 83:526–537. https://doi.org/10.1111/his.14941

    Article  PubMed  Google Scholar 

  28. Kleiner DE, Brunt EM, Natta MV et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321. https://doi.org/10.1002/hep.20701

    Article  PubMed  Google Scholar 

  29. Bedossa P, Poitou C, Veyrie N et al (2012) Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients. Hepatology 56:1751–1759. https://doi.org/10.1002/hep.25889

    Article  PubMed  Google Scholar 

  30. Aykutlu U, Argon A, Orman M et al (2021) Steatotic and steatohepatitic hepatocellular carcinomas: features in a series with predominantly viral etiology. Am J Surg Pathol 45:1252–1263. https://doi.org/10.1097/PAS.0000000000001714

    Article  PubMed  Google Scholar 

  31. Kupczyk PA, Kurt D, Endler C et al (2023) MRI proton density fat fraction for estimation of tumor grade in steatotic hepatocellular carcinoma. Eur Radiol 33:8974–8985. https://doi.org/10.1007/s00330-023-09864-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Liu X, Ni X, Li Y et al (2022) Diagnostic performance of LI-RADS version 2018 for primary liver cancer in patients with liver cirrhosis on enhanced MRI. Front Oncol 12:934045. https://doi.org/10.3389/fonc.2022.934045

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kim Y-Y, An C, Kim S, Kim M-J (2018) Diagnostic accuracy of prospective application of the Liver Imaging Reporting and Data System (LI-RADS) in gadoxetate-enhanced MRI. Eur Radiol 28:2038–2046. https://doi.org/10.1007/s00330-017-5188-y

    Article  PubMed  Google Scholar 

  34. An C, Park S, Chung YE et al (2017) Curative resection of single primary hepatic malignancy: liver imaging reporting and data system category LR-M portends a worse prognosis. Am J Roentgenol 209:576–583. https://doi.org/10.2214/AJR.16.17478

    Article  Google Scholar 

  35. Auer TA, Halskov S, Fehrenbach U et al (2023) Gd-EOB MRI for HCC subtype differentiation in a western population according to the 5th edition of the World Health Organization classification. Eur Radiol 33:6902–6915. https://doi.org/10.1007/s00330-023-09669-y

    Article  PubMed  PubMed Central  Google Scholar 

  36. Chen K, Xu Y, Dong Y et al (2023) Contrast-enhanced imaging features and clinicopathological investigation of steatohepatitic hepatocellular carcinoma. Diagnostics 13:1337. https://doi.org/10.3390/diagnostics13071337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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Authors and Affiliations

  1. Department of Radiology, Hôpital Beaujon, AP-HP.Nord, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Alexandre Faure, Marco Dioguardi Burgio, Riccardo Sartoris, Valérie Vilgrain & Maxime Ronot

  2. UMR1149, Centre de Recherche Sur L’inflammation, Université Paris Cité, 75018, Paris, France

    Marco Dioguardi Burgio, Aurélie Beaufrère, Valérie Vilgrain & Maxime Ronot

  3. Section of Radiology, Department of Biomedicine, Neuroscience and Advanced Diagnostics (BiND), University of Palermo, Palermo, Italy

    Roberto Cannella

  4. Department of Digestive Oncology, Hôpital Beaujon, AP-HP.Nord, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Mohamed Bouattour

  5. Department of HPB Surgery and Liver Transplantation, Hôpital Beaujon, AP-HP, 92110, Clichy, France

    Christian Hobeika & Francois Cauchy

  6. Department of Pathology, FHU MOSAIC, Hôpital Beaujon, AP-HP.Nord, 100 Boulevard du Général Leclerc, 92110, Clichy, France

    Loïc Trapani & Aurélie Beaufrère

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  1. Alexandre Faure
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Alexandre Faure, Marco Dioguardi Burgio, Roberto Cannella. The first draft of the manuscript was written by Alexandre Faure, Marco Dioguardi Burgio and Maxime Ronot and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.”

Corresponding author

Correspondence to Marco Dioguardi Burgio.

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The authors have no relevant financial or non-financial interests to disclose.

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This study was performed in line with the principles of the Declaration of Helsinki. Local IRB (CERIM) approved this retrospective study and waiver of written informed consent was obtained due to de retrospective approach.

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Faure, A., Dioguardi Burgio, M., Cannella, R. et al. Imaging and prognostic characterization of fat-containing hepatocellular carcinoma subtypes. Radiol med 129, 687–701 (2024). https://doi.org/10.1007/s11547-024-01807-w

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  • DOI: https://doi.org/10.1007/s11547-024-01807-w

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