Table Info

Table 11.

Study evaluating SSM by VCTE and HCC recurrence in patients with mixed etiology

Author & year	Region	Patients (n)	Mean age (years)	F-U months	Etiology of liver disease (%)	Recurrent HCC	Proposed cut off (TE) (kPa)	AUROC	Sens (%)	Spec (%)	PPV	NPV	LR+	LR–
Marasco et al., 2019 [66]	Italy	157	62	24	HCV 56 HBV 19.8 EtOH 21 Others 3.2	66 (early) 27 (late)	SSM > 70	-	-	-	-	-	-	-

SSM: spleen stiffness measurement; VCTE: vibration-controlled transient elastography

Supplementary materials

The supplementary materials for this article are available at: https://www.explorationpub.com/uploads/Article/file/100555_sup_1.pdf.

Declarations

Author contributions

AF: Investigation, Writing—original draft. MF: Conceptualization, Investigation, Writing—original draft, Writing—review & editing, Supervision. All authors read and approved the submitted version.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

The primary data for this review were sourced online from databases listed in the methods.

Funding

Not applicable.

Copyright

References

Llovet JM, Kelley RK, Villanueva A, Singal AG, Pikarsky E, Roayaie S, et al. Hepatocellular carcinoma. Nat Rev Dis Primers. 2021;7:6. English. Erratum in: Nat Rev Dis Primers. 2024;10:10. [DOI] [PubMed]

Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, et al. Diagnosis, Staging, and Management of Hepatocellular Carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68:723–50. [DOI] [PubMed]

European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236. Erratum in: J Hepatol. 2019;70:817. [DOI] [PubMed]

Colecchia A, Marasco G, Taddia M, Montrone L, Eusebi LH, Mandolesi D, et al. Liver and spleen stiffness and other noninvasive methods to assess portal hypertension in cirrhotic patients: a review of the literature. Eur J Gastroenterol Hepatol. 2015;27:992–1001. [DOI] [PubMed]

Colecchia A, Ravaioli F, Marasco G, Colli A, Dajti E, Biase ARD, et al. A combined model based on spleen stiffness measurement and Baveno VI criteria to rule out high-risk varices in advanced chronic liver disease. J Hepatol. 2018;69:308–17. [DOI] [PubMed]

Ravaioli F, Colecchia A, Dajti E, Marasco G, Alemanni LV, Tamè M, et al. Spleen stiffness mirrors changes in portal hypertension after successful interferon-free therapy in chronic-hepatitis C virus patients. World J Hepatol. 2018;10:731–42. [DOI] [PubMed] [PMC]

Tawada A, Kanda T, Yokosuka O. Current and future directions for treating hepatitis B virus infection. World J Hepatol. 2015;7:1541–52. [DOI] [PubMed] [PMC]

Chu C, Liaw Y. Hepatitis B virus-related cirrhosis: natural history and treatment. Semin Liver Dis. 2006;26:142–52. [DOI] [PubMed]

Fung J, Lai C, But D, Wong D, Cheung T, Yuen M. Prevalence of fibrosis and cirrhosis in chronic hepatitis B: implications for treatment and management. Am J Gastroenterol. 2008;103:1421–6. [DOI] [PubMed]

10.

Seo YS, Kim MN, Kim SU, Kim SG, Um SH, Han K, et al. Risk Assessment of Hepatocellular Carcinoma Using Transient Elastography Vs. Liver Biopsy in Chronic Hepatitis B Patients Receiving Antiviral Therapy. Medicine (Baltimore). 2016;95:e2985. [DOI] [PubMed] [PMC]

11.

Chon YE, Jung ES, Park JY, Kim DY, Ahn SH, Han K, et al. The accuracy of noninvasive methods in predicting the development of hepatocellular carcinoma and hepatic decompensation in patients with chronic hepatitis B. J Clin Gastroenterol. 2012;46:518–25. [DOI] [PubMed]

12.

Wang J, Hu T, Chen C, Hung C, Yen Y, Chang K, et al. Liver stiffness measurement at complete virological response in hepatoma prediction for HBV-related cirrhosis patient with potent antiviral agent. Kaohsiung J Med Sci. 2019;35:708–14. [DOI] [PubMed]

13.

Jung KS, Kim SU, Ahn SH, Park YN, Kim DY, Park JY, et al. Risk assessment of hepatitis B virus-related hepatocellular carcinoma development using liver stiffness measurement (FibroScan). Hepatology. 2011;53:885–94. [DOI] [PubMed]

14.

Kim SU, Lee JH, Kim DY, Ahn SH, Jung KS, Choi EH, et al. Prediction of liver-related events using fibroscan in chronic hepatitis B patients showing advanced liver fibrosis. PLoS One. 2012;7:e36676. [DOI] [PubMed] [PMC]

15.

Kim DY, Song KJ, Kim SU, Yoo EJ, Park JY, Ahn SH, et al. Transient elastography-based risk estimation of hepatitis B virus-related occurrence of hepatocellular carcinoma: development and validation of a predictive model. Onco Targets Ther. 2013;6:1463–9. [DOI] [PubMed] [PMC]

16.

Wong GL, Chan HL, Wong CK, Leung C, Chan CY, Ho PP, et al. Liver stiffness-based optimization of hepatocellular carcinoma risk score in patients with chronic hepatitis B. J Hepatol. 2014;60:339–45. [DOI] [PubMed]

17.

Kim MN, Kim SU, Kim BK, Park JY, Kim DY, Ahn SH, et al. Increased risk of hepatocellular carcinoma in chronic hepatitis B patients with transient elastography-defined subclinical cirrhosis. Hepatology. 2015;61:1851–9. [DOI] [PubMed]

18.

Bihari C, Rastogi A, Sen B, Bhadoria AS, Maiwall R, Sarin SK. Quantitative fibrosis estimation by image analysis predicts development of decompensation, composite events and defines event-free survival in chronic hepatitis B patients. Hum Pathol. 2016;55:63–71. [DOI] [PubMed]

19.

Jeon MY, Lee HW, Kim SU, Heo JY, Han S, Kim BK, et al. Subcirrhotic liver stiffness by FibroScan correlates with lower risk of hepatocellular carcinoma in patients with HBV-related cirrhosis. Hepatol Int. 2017;11:268–76. [DOI] [PubMed]

20.

Li Z, Hu C, Yu P, Gu X, Zhang J, Li H, et al. The development of hepatocarcinoma after long-term antivirus treatment of Chinese patients with chronic hepatitis B virus infection: Incidence, long-term outcomes and predictive factors. Clin Res Hepatol Gastroenterol. 2017;41:311–18. [DOI] [PubMed]

21.

Izumi T, Sho T, Morikawa K, Shigesawa T, Suzuki K, Nakamura A, et al. Assessing the risk of hepatocellular carcinoma by combining liver stiffness and the controlled attenuation parameter. Hepatol Res. 2019;49:1207–17. [DOI] [PubMed]

22.

Lee HW, Lee HW, Lee JS, Roh YH, Lee H, Kim SU, et al. The Prognostic Role of On-Treatment Liver Stiffness for Hepatocellular Carcinoma Development in Patients with Chronic Hepatitis B. J Hepatocell Carcinoma. 2021;8:467–76. [DOI] [PubMed] [PMC]

23.

Ghany MG, Kleiner DE, Alter H, Doo E, Khokar F, Promrat K, et al. Progression of fibrosis in chronic hepatitis C. Gastroenterology. 2003;124:97–104. [DOI] [PubMed]

24.

Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet. 1997;349:825–32. [DOI] [PubMed]

25.

Goto K, Suarez AAR, Wrensch F, Baumert TF, Lupberger J. Hepatitis C Virus and Hepatocellular Carcinoma: When the Host Loses Its Grip. Int J Mol Sci. 2020;21:3057. [DOI] [PubMed] [PMC]

26.

Ioannou GN, Green PK, Beste LA, Mun EJ, Kerr KF, Berry K. Development of models estimating the risk of hepatocellular carcinoma after antiviral treatment for hepatitis C. J Hepatol. 2018;69:1088–98. [DOI] [PubMed] [PMC]

27.

Wang H, Hung C, Lu S, Chen C, Lee C, Hu T, et al. Liver stiffness measurement as an alternative to fibrotic stage in risk assessment of hepatocellular carcinoma incidence for chronic hepatitis C patients. Liver Int. 2013;33:756–61. [DOI] [PubMed]

28.

Nakagomi R, Tateishi R, Masuzaki R, Soroida Y, Iwai T, Kondo M, et al. Liver stiffness measurements in chronic hepatitis C: Treatment evaluation and risk assessment. J Gastroenterol Hepatol. 2019;34:921–28. [DOI] [PubMed]

29.

Masuzaki R, Tateishi R, Yoshida H, Yoshida H, Sato S, Kato N, et al. Risk assessment of hepatocellular carcinoma in chronic hepatitis C patients by transient elastography. J Clin Gastroenterol. 2008;42:839–43. [DOI] [PubMed]

30.

Masuzaki R, Tateishi R, Yoshida H, Goto E, Sato T, Ohki T, et al. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. Hepatology. 2009;49:1954–61. [DOI] [PubMed]

31.

Calvaruso V, Bronte F, Simone F, Bavetta MG, Conte E, Craxì A, et al. P.11.9 Liver stiffness at baseline predicts decompensation and hepatocellular carcinoma in patients with compensated HCV cirrhosis. Dig Liver Dis. 2013;45:S167–8. [DOI]

32.

Feier D, Platon ML, Stefanescu H, Badea R. Transient elastography for the detection of hepatocellular carcinoma in viral C liver cirrhosis. Is there something else than increased liver stiffness? J Gastrointestin Liver Dis. 2013;22:283–9. [PubMed]

33.

Narita Y, Genda T, Tsuzura H, Sato S, Kanemitsu Y, Ishikawa S, et al. Prediction of liver stiffness hepatocellular carcinoma in chronic hepatitis C patients on interferon-based anti-viral therapy. J Gastroenterol Hepatol. 2014;29:137–43. [DOI] [PubMed]

34.

Wang J, Yen Y, Yao C, Hung C, Chen C, Hu T, et al. Liver stiffness-based score in hepatoma risk assessment for chronic hepatitis C patients after successful antiviral therapy. Liver Int. 2016;36:1793–9. [DOI] [PubMed]

35.

D’ambrosio R, Degasperi E, Iavarone M, Sangiovanni A, Aghemo A, Soffredini R, et al. Incidence and predictors of de novo hepatocellular carcinoma in HCV cirrhotic patients treated with direct-acting antivirals: a single-center prospective 3 year study. J Hepatol. 2018;68:S529. [DOI]

36.

Degasperi E, D’Ambrosio R, Iavarone M, Sangiovanni A, Aghemo A, Soffredini R, et al. Factors Associated With Increased Risk of De Novo or Recurrent Hepatocellular Carcinoma in Patients With Cirrhosis Treated With Direct-Acting Antivirals for HCV Infection. Clin Gastroenterol Hepatol. 2019;17:1183–91.e7. [DOI] [PubMed]

37.

Pons M, Rodríguez-Tajes S, Esteban JI, Mariño Z, Vargas V, Lens S, et al. Non-invasive prediction of liver-related events in patients with HCV-associated compensated advanced chronic liver disease after oral antivirals. J Hepatol. 2020;72:472–80. [DOI] [PubMed]

38.

Rinaldi L, Guarino M, Perrella A, Pafundi PC, Valente G, Fontanella L, et al. Role of Liver Stiffness Measurement in Predicting HCC Occurrence in Direct-Acting Antivirals Setting: A Real-Life Experience. Dig Dis Sci. 2019;64:3013–9. [DOI] [PubMed]

39.

Kumada T, Toyoda H, Yasuda S, Sone Y, Ogawa S, Takeshima K, et al. Prediction of Hepatocellular Carcinoma by Liver Stiffness Measurements Using Magnetic Resonance Elastography After Eradicating Hepatitis C Virus. Clin Transl Gastroenterol. 2021;12:e00337. [DOI] [PubMed] [PMC]

40.

Tamaki N, Higuchi M, Kurosaki M, Kirino S, Osawa L, Watakabe K, et al. Risk assessment of hepatocellular carcinoma development by magnetic resonance elastography in chronic hepatitis C patients who achieved sustained virological responses by direct-acting antivirals. J Viral Hepat. 2019;26:893–9. [DOI] [PubMed]

41.

Kumada T, Toyoda H, Yasuda S, Ogawa S, Gotoh T, Tada T, et al. Combined ultrasound and magnetic resonance elastography predict hepatocellular carcinoma after hepatitis C virus eradication. Hepatol Res. 2022;52:957–67. [DOI] [PubMed]

42.

Gyotoku Y, Shirahashi R, Suda T, Tamano M. Role of liver stiffness measurements in patients who develop hepatocellular carcinoma after clearance of the hepatitis C virus. J Med Ultrason (2001). 2022;49:253–9. [DOI] [PubMed] [PMC]

43.

Hamada K, Saitoh S, Nishino N, Fukushima D, Horikawa Y, Nishida S, et al. Shear wave elastography predicts hepatocellular carcinoma risk in hepatitis C patients after sustained virological response. PLoS One. 2018;13:e0195173. [DOI] [PubMed] [PMC]

44.

Dajti E, Marasco G, Ravaioli F, Colecchia L, Ferrarese A, Festi D, et al. Risk of hepatocellular carcinoma after HCV eradication: Determining the role of portal hypertension by measuring spleen stiffness. JHEP Rep. 2021;3:100289. [DOI] [PubMed] [PMC]

45.

Kuo YH, Lu SN, Hung CH, Kee KM, Chen CH, Hu TH, et al. Liver stiffness measurement in the risk assessment of hepatocellular carcinoma for patients with chronic hepatitis. Hepatol Int. 2010;4:700–6. [DOI] [PubMed] [PMC]

46.

Robic MA, Procopet B, Métivier S, Péron JM, Selves J, Vinel JP, et al. Liver stiffness accurately predicts portal hypertension related complications in patients with chronic liver disease: a prospective study. J Hepatol. 2011;55:1017–24. [DOI] [PubMed]

47.

Pérez-Latorre L, Sánchez-Conde M, Rincón D, Miralles P, Aldámiz-Echevarría T, Carrero A, et al. Prediction of liver complications in patients with hepatitis C virus-related cirrhosis with and without HIV coinfection: comparison of hepatic venous pressure gradient and transient elastography. Clin Infect Dis. 2014;58:713–8. [DOI] [PubMed]

48.

Nahon P, Kettaneh A, Lemoine M, Seror O, Barget N, Trinchet J, et al. Liver stiffness measurement in patients with cirrhosis and hepatocellular carcinoma: a case-control study. Eur J Gastroenterol Hepatol. 2009;21:214–9. [DOI] [PubMed]

49.

Akima T, Tamano M, Hiraishi H. Liver stiffness measured by transient elastography is a predictor of hepatocellular carcinoma development in viral hepatitis. Hepatol Res. 2011;41:965–70. [DOI] [PubMed]

50.

Klibansky DA, Mehta SH, Curry M, Nasser I, Challies T, Afdhal NH. Transient elastography for predicting clinical outcomes in patients with chronic liver disease. J Viral Hepat. 2012;19:e184–93. [DOI] [PubMed]

51.

Salmon D, Bani-Sadr F, Loko M, Stitou H, Gervais A, Durant J, et al. Insulin resistance is associated with a higher risk of hepatocellular carcinoma in cirrhotic HIV/HCV-co-infected patients: results from ANRS CO13 HEPAVIH. J Hepatol. 2012;56:862–8. [DOI] [PubMed]

52.

Poynard T, Vergniol J, Ngo Y, Foucher J, Munteanu M, Merrouche W, et al.; FibroFrance Study Group; Epic3 Study Group; Bordeaux HCV Study Group. Staging chronic hepatitis C in seven categories using fibrosis biomarker (FibroTest™) and transient elastography (FibroScan®). J Hepatol. 2014;60:706–14. [DOI] [PubMed]

53.

Adler M, Larocca L, Trovato FM, Marcinkowski H, Pasha Y, Taylor-Robinson SD. Evaluating the risk of hepatocellular carcinoma in patients with prominently elevated liver stiffness measurements by FibroScan: a multicentre study. HPB (Oxford). 2016;18:678–83. [DOI] [PubMed] [PMC]

54.

Lee DH, Lee JM, Chang W, Yoon J, Kim YJ, Lee J, et al. Prognostic Role of Liver Stiffness Measurements Using Magnetic Resonance Elastography in Patients with Compensated Chronic Liver Disease. Eur Radiol. 2018;28:3513–21. [DOI] [PubMed]

55.

Ichikawa S, Motosugi U, Enomoto N, Onishi H. Magnetic resonance elastography can predict development of hepatocellular carcinoma with longitudinally acquired two-point data. Eur Radiol. 2019;29:1013–21. [DOI] [PubMed]

56.

Anaparthy R, Talwalkar JA, Yin M, Roberts LR, Fidler JL, Ehman RL. Liver stiffness measurement by magnetic resonance elastography is not associated with developing hepatocellular carcinoma in subjects with compensated cirrhosis. Aliment Pharmacol Ther. 2011;34:83–91. [DOI] [PubMed] [PMC]

57.

Motosugi U, Ichikawa T, Koshiishi T, Sano K, Morisaka H, Ichikawa S, et al. Liver stiffness measured by magnetic resonance elastography as a risk factor for hepatocellular carcinoma: a preliminary case-control study. Eur Radiol. 2013;23:156–62. [DOI] [PubMed]

58.

Higuchi M, Tamaki N, Kurosaki M, Inada K, Kirino S, Yamashita K, et al. Longitudinal association of magnetic resonance elastography-associated liver stiffness with complications and mortality. Aliment Pharmacol Ther. 2022;55:292–301. [DOI] [PubMed] [PMC]

59.

Kasai Y, Moriyasu F, Saito K, Hara T, Kobayashi Y, Nakamura I, et al. Value of shear wave elastography for predicting hepatocellular carcinoma and esophagogastric varices in patients with chronic liver disease. J Med Ultrason (2001). 2015;42:349–55. [DOI] [PubMed]

60.

Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64:73–84. [DOI] [PubMed]

61.

McPherson S, Hardy T, Henderson E, Burt AD, Day CP, Anstee QM. Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis and clinical management. J Hepatol. 2015;62:1148–55. [DOI] [PubMed]

62.

Shili-Masmoudi S, Wong GL, Hiriart J, Liu K, Chermak F, Shu SS, et al. Liver stiffness measurement predicts long-term survival and complications in non-alcoholic fatty liver disease. Liver Int. 2020;40:581–9. [DOI] [PubMed]

63.

Lee JS, Sinn DH, Park SY, Shin HJ, Lee HW, Kim BK, et al. Liver Stiffness-Based Risk Prediction Model for Hepatocellular Carcinoma in Patients with Nonalcoholic Fatty Liver Disease. Cancers (Basel). 2021;13:4567. [DOI] [PubMed] [PMC]

64.

Ajmera V, Kim BK, Yang K, Majzoub AM, Nayfeh T, Tamaki N, et al. Liver Stiffness on Magnetic Resonance Elastography and the MEFIB Index and Liver-Related Outcomes in Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-Analysis of Individual Participants. Gastroenterology. 2022;163:1079–89.e5. [DOI] [PubMed] [PMC]

65.

Abdelhamed W, El-Kassas M. Hepatocellular carcinoma recurrence: Predictors and management. Liver Res. 2023;7:321–32. [DOI]

66.

Marasco G, Colecchia A, Colli A, Ravaioli F, Casazza G, Reggiani MLB, et al. Role of liver and spleen stiffness in predicting the recurrence of hepatocellular carcinoma after resection. J Hepatol. 2019;70:440–8. [DOI] [PubMed]

67.

Cho HJ, Kim B, Kim HJ, Huh J, Kim JK, Lee JH, et al. Liver stiffness measured by MR elastography is a predictor of early HCC recurrence after treatment. Eur Radiol. 2020;30:4182–92. [DOI] [PubMed]

68.

Friedrich-Rust M, Poynard T, Castera L. Critical comparison of elastography methods to assess chronic liver disease. Nat Rev Gastroenterol Hepatol. 2016;13:402–11. [DOI] [PubMed]

69.

Enomoto M, Vutien P, Kawada N. Hepatocelluar Carcinoma Risk in Advanced Fibrosis After Sustained Virologic Response: When Can We Safely Stop Hepatocellular Carcinoma Surveillance? Hepatol Commun. 2022;6:445–7. [DOI] [PubMed] [PMC]

70.

Onori P, Morini S, Franchitto A, Sferra R, Alvaro D, Gaudio E. Hepatic microvascular features in experimental cirrhosis: a structural and morphometrical study in CCl4-treated rats. J Hepatol. 2000;33:555–63. [DOI] [PubMed]

71.

Wu D, Chen E, Liang T, Wang M, Chen B, Lang B, et al. Predicting the risk of postoperative liver failure and overall survival using liver and spleen stiffness measurements in patients with hepatocellular carcinoma. Medicine (Baltimore). 2017;96:e7864. [DOI] [PubMed] [PMC]

72.

Peng W, Zhang X, Li C, Wen T, Yan L, Yang J. Spleen stiffness and volume help to predict posthepatectomy liver failure in patients with hepatocellular carcinoma. Medicine (Baltimore). 2019;98:e15458. [DOI] [PubMed] [PMC]

73.

Lee PC, Chiou YY, Chiu NC, Chen PH, Liu CA, Kao WY, et L. Liver stiffness measured by acoustic radiation force impulse elastography predicted prognoses of hepatocellular carcinoma after radiofrequency ablation. Sci Rep. 2020;10:2006. [DOI] [PubMed] [PMC]

74.

Semmler G, Lens S, Meyer EL, Baiges A, Alvardo-Tapias E, Llop E, et al. Non-invasive tests for clinically significant portal hypertension after HCV cure. J Hepatol. 2022;77:1573–85. [DOI] [PubMed]

75.

López SA, Manzano ML, Gea F, Gutiérrez ML, Ahumada AM, Devesa MJ, et al. A Model Based on Noninvasive Markers Predicts Very Low Hepatocellular Carcinoma Risk After Viral Response in Hepatitis C Virus-Advanced Fibrosis. Hepatology. 2020;72:1924–34. [DOI] [PubMed]

76.

Liang LY, Wong VW, Tse Y, Yip TC, Lui GC, Chan HL, et al. Improvement in enhanced liver fibrosis score and liver stiffness measurement reflects lower risk of hepatocellular carcinoma. Aliment Pharmacol Ther. 2019;49:1509–17. [DOI] [PubMed]

77.

Lin H, Li G, Delamarre A, Ahn SH, Zhang X, Kim BK, et al. A Liver Stiffness-Based Etiology-Independent Machine Learning Algorithm to Predict Hepatocellular Carcinoma. Clin Gastroenterol Hepatol. 2024;22:602–10.e7. [DOI] [PubMed]