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Imaging features of hepatocellular carcinoma in nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: a systematic review and meta-analysis

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Abstract

Purpose

To investigate the imaging features of hepatocellular carcinoma (HCC) in patients with non-alcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH) through a systematic review and meta-analysis.

Methods

MEDLINE, EMBASE, and the Cochrane Library database were searched for studies providing data on imaging features of HCC in NAFLD and NASH between January 1, 2011 and July 19, 2021. Random effects models were used to calculate the pooled percentages of the three major features of arterial-phase hyperenhancement (APHE), washout, and enhancing capsule. Sensitivity analysis and subgroup analysis were performed according to underlying liver disease (NASH vs. NAFLD) and imaging modality (CT vs. MRI).

Results

Five studies (170 patients with 193 HCCs) were included in the analysis. The pooled percentages of APHE, washout, and enhancing capsule were 94.0% (95% confidence interval [CI] 89.1–96.7%), 72.7% (95% CI 63.3–80.4%), and 57.5% (95% CI 45.1–69.1%), respectively. The percentages of these three major features did not significantly differ between NAFLD and NASH (p ≥ 0.21). MRI showed similar pooled percentages of APHE (94.3% vs. 93.4%, p = 0.82) and washout (70.4% vs. 77.2%, p = 0.38) to CT, but a higher pooled percentage of enhancing capsule (67.1% vs. 44.7%, p = 0.02).

Conclusion

HCC in patients with NAFLD and NASH had a similar frequency of APHE to HCC with other etiology. However, it showed a relatively low frequency of washout and enhancing capsule.

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References

  1. Fitzmaurice C, Abate D, Abbasi N, Abbastabar H, Abd-Allah F, Abdel-Rahman O, et al. (2019) Global, Regional, and National Cancer Incidence, Mortality, Years of Life Lost, Years Lived With Disability, and Disability-Adjusted Life-Years for 29 Cancer Groups, 1990 to 2017: A Systematic Analysis for the Global Burden of Disease Study. JAMA oncology 5:1749-1768. https://doi.org/10.1001/jamaoncol.2019.2996

    Article  PubMed  PubMed Central  Google Scholar 

  2. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. (2016) Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology (Baltimore, Md) 64:73-84. https://doi.org/10.1002/hep.28431

    Article  Google Scholar 

  3. Siegel AB, Zhu AX. (2009) Metabolic syndrome and hepatocellular carcinoma: two growing epidemics with a potential link. Cancer 115:5651-5661. https://doi.org/10.1002/cncr.24687

    Article  PubMed  Google Scholar 

  4. Tilg H, Moschen AR, Roden M. (2017) NAFLD and diabetes mellitus. Nature reviews Gastroenterology & hepatology 14:32-42. https://doi.org/10.1038/nrgastro.2016.147

    Article  CAS  Google Scholar 

  5. Sherif ZA, Saeed A, Ghavimi S, Nouraie SM, Laiyemo AO, Brim H, et al. (2016) Global Epidemiology of Nonalcoholic Fatty Liver Disease and Perspectives on US Minority Populations. Digestive diseases and sciences 61:1214-1225. https://doi.org/10.1007/s10620-016-4143-0

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ascha MS, Hanouneh IA, Lopez R, Tamimi TA, Feldstein AF, Zein NN. (2010) The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis. Hepatology (Baltimore, Md) 51:1972-1978. https://doi.org/10.1002/hep.23527

    Article  Google Scholar 

  7. Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, et al. (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology (Baltimore, Md) 67:358-380. https://doi.org/10.1002/hep.29086

    Article  Google Scholar 

  8. American College of Radiology (2018). Liver imaging reporting and data system version 2018.: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS (2018). Accessed August 21 2021.

  9. Al-Sharhan F, Dohan A, Barat M, Feddal A, Terris B, Pol S, et al. (2019) MRI presentation of hepatocellular carcinoma in non-alcoholic steatohepatitis (NASH). Eur J Radiol 119:108648. https://doi.org/10.1016/j.ejrad.2019.108648

    Article  PubMed  Google Scholar 

  10. Barat M, Nguyen TTL, Hollande C, Coty JB, Hoeffel C, Terris B, et al. (2021) LI-RADS v2018 major criteria: Do hepatocellular carcinomas in non-alcoholic steatohepatitis differ from those in virus-induced chronic liver disease on MRI? Eur J Radiol 138:109651. https://doi.org/10.1016/j.ejrad.2021.109651

    Article  PubMed  Google Scholar 

  11. Garg I, Thompson SM, Sheedy SP, Mounajjed T, Khandelwal A, Ehman EC, et al. (2019) CT of hepatocellular carcinoma in non-alcoholic fatty liver disease: imaging characteristics and inter-rater agreement. Hepatoma Research 2019. https://doi.org/10.20517/2394-5079.2019.009

    Article  Google Scholar 

  12. Iannaccone R, Piacentini F, Murakami T, Paradis V, Belghiti J, Hori M, et al. (2007) Hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: helical CT and MR imaging findings with clinical-pathologic comparison. Radiology 243:422-430.

    Article  Google Scholar 

  13. Thompson SM, Garg I, Ehman EC, Sheedy SP, Bookwalter CA, Carter RE, et al. (2018) Non-alcoholic fatty liver disease-associated hepatocellular carcinoma: effect of hepatic steatosis on major hepatocellular carcinoma features at MRI. The British journal of radiology 91:20180345.

    Article  Google Scholar 

  14. Moher D, Liberati A, Tetzlaff J, Altman DG. (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336-341.

    Article  Google Scholar 

  15. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Annals of internal medicine 155:529-536.

    Article  Google Scholar 

  16. DerSimonian R, Laird N. (1986) Meta-analysis in clinical trials. Controlled clinical trials 7:177-188.

    Article  CAS  Google Scholar 

  17. Higgins JP, Thompson SG, Deeks JJ, Altman DG. (2003) Measuring inconsistency in meta-analyses. BMJ 327:557-560.

    Article  Google Scholar 

  18. Vandenbroucke JP. (1998) Bias in meta-analysis detected by a simple, graphical test. Experts' views are still needed. BMJ 316:469.

    CAS  PubMed  Google Scholar 

  19. Tang A, Bashir MR, Corwin MT, Cruite I, Dietrich CF, Do RKG, et al. (2018) Evidence Supporting LI-RADS Major Features for CT- and MR Imaging-based Diagnosis of Hepatocellular Carcinoma: A Systematic Review. Radiology 286:29-48. https://doi.org/10.1148/radiol.2017170554

    Article  PubMed  Google Scholar 

  20. Dunst D, Ream JM, Khalef V, Hajdu CH, Rosenkrantz AB. (2016) Comparison of MRI features of pathologically proven hepatocellular carcinoma between patients with hepatitis B and hepatitis C infection. Clinical imaging 40:352-356. https://doi.org/10.1016/j.clinimag.2016.01.014

    Article  PubMed  Google Scholar 

  21. Shao S, Liang Y, Kuang S, Chen J, Shan Q, Yang H, et al. (2020) Diagnostic performance of LI-RADS version 2018 in differentiating hepatocellular carcinoma from other hepatic malignancies in patients with hepatitis B virus infection. Bosnian journal of basic medical sciences 20:401-410. https://doi.org/10.17305/bjbms.2019.4576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Cannella R, Burgio MD, Beaufrère A, Trapani L, Paradis V, Hobeika C, et al. (2021) Imaging features of histological subtypes of hepatocellular carcinoma: implication for LI-RADS. JHEP Reports:100380.

  23. Cannella R, Ronot M, Sartoris R, Cauchy F, Hobeika C, Beaufrere A, et al. (2021) Enhancing capsule in hepatocellular carcinoma: intra-individual comparison between CT and MRI with extracellular contrast agent. Diagnostic and interventional imaging. https://doi.org/10.1016/j.diii.2021.06.004

    Article  PubMed  Google Scholar 

  24. Joo I, Lee JM, Lee DH, Ahn SJ, Lee ES, Han JK. (2017) Liver imaging reporting and data system v2014 categorization of hepatocellular carcinoma on gadoxetic acid-enhanced MRI: Comparison with multiphasic multidetector computed tomography. Journal of magnetic resonance imaging : JMRI 45:731-740. https://doi.org/10.1002/jmri.25406

    Article  PubMed  Google Scholar 

  25. Cho ES, Choi JY. (2015) MRI features of hepatocellular carcinoma related to biologic behavior. Korean journal of radiology 16:449-464. https://doi.org/10.3348/kjr.2015.16.3.449

    Article  PubMed  PubMed Central  Google Scholar 

  26. van den Bos IC, Hussain SM, Dwarkasing RS, Hop WC, Zondervan PE, de Man RA, et al. (2007) MR imaging of hepatocellular carcinoma: relationship between lesion size and imaging findings, including signal intensity and dynamic enhancement patterns. Journal of magnetic resonance imaging : JMRI 26:1548-1555. https://doi.org/10.1002/jmri.21046

    Article  PubMed  Google Scholar 

  27. Forner A, Vilana R, Ayuso C, Bianchi L, Solé M, Ayuso JR, et al. (2008) Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology (Baltimore, Md) 47:97-104. https://doi.org/10.1002/hep.21966

    Article  Google Scholar 

  28. Lee YJ, Lee JM, Lee JS, Lee HY, Park BH, Kim YH, et al. (2015) Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology 275:97-109. https://doi.org/10.1148/radiol.14140690

    Article  PubMed  Google Scholar 

  29. Salomao M, Yu WM, Brown RS, Jr., Emond JC, Lefkowitch JH. (2010) Steatohepatitic hepatocellular carcinoma (SH-HCC): a distinctive histological variant of HCC in hepatitis C virus-related cirrhosis with associated NAFLD/NASH. The American journal of surgical pathology 34:1630-1636. https://doi.org/10.1097/PAS.0b013e3181f31caa

    Article  PubMed  Google Scholar 

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Park, E.J., Son, J.H. & Choi, S.H. Imaging features of hepatocellular carcinoma in nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: a systematic review and meta-analysis. Abdom Radiol 47, 2089–2098 (2022). https://doi.org/10.1007/s00261-022-03499-0

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