MRI for screening and surveillance for hepatocellular cancer in NAFLD and NASH

Christine Pocha , Sabina Choudhry

Hepatoma Research ›› 2023, Vol. 9 : 22

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Hepatoma Research ›› 2023, Vol. 9:22 DOI: 10.20517/2394-5079.2023.08
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MRI for screening and surveillance for hepatocellular cancer in NAFLD and NASH

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Abstract

Chronic liver disease is an important risk factor for the development of hepatocellular carcinoma (HCC), with 80%-90% developing in the background of cirrhosis, primarily due to alcohol abuse and chronic viral infection with hepatitis B and C. Non-alcoholic fatty liver disease (NAFLD) and non-alcoholic steatohepatitis (NASH) related HCC is rising due to the global epidemic of obesity and diabetes. NAFLD also potentiates other risk factors of HCC, such as chronic hepatitis C and alcoholic liver injury. Furthermore, HCC may complicate non-cirrhotic NAFLD, greatly expanding the population potentially at risk. Screening and surveillance for HCC with ultrasonography (US) in this patient population pose challenges related to body habitus, liver morphology, and co-morbidities. Magnetic resonance imaging (MRI) applying various image sequence protocols and contrast agents could aid in early detection and improved prognosis of HCC. It is of utmost importance to define the most cost-effective dynamic imaging protocol for use in patients where high-quality ultrasonography images cannot be obtained and for patients undergoing surveillance for lesions identified with US. Furthermore, standardization of MRI protocols will help to define potential unique HCC features in this population. A scoring system including patient-derived factors may help to identify high-risk patients. Standardized protocols as part of prospective cohort studies and randomized clinical trials will help to stratify high-risk patients and to aid the development of professional guidelines for screening and surveillance of HCC in patients with NAFLD and NASH using dynamic imagining techniques.

Keywords

Hepatocellular carcinoma / non-alcoholic fatty liver disease / non-alcoholic steatohepatitis / magnetic resonance imaging

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Christine Pocha, Sabina Choudhry. MRI for screening and surveillance for hepatocellular cancer in NAFLD and NASH. Hepatoma Research, 2023, 9: 22 DOI:10.20517/2394-5079.2023.08

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References

[1]

Charlton MR,Pedersen RA,Heimbach JK.Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States.Gastroenterology2011;141:1249-53

[2]

Loomba R,Patton H.AGA clinical practice update on screening and surveillance for hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: expert review.Gastroenterology2020;158:1822-30 PMCID:PMC8012107

[3]

Huang DQ,Loomba R.Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention.Nat Rev Gastroenterol Hepatol2021;18:223-38 PMCID:PMC8016738

[4]

Leung C,Patrick D.Characteristics of hepatocellular carcinoma in cirrhotic and non-cirrhotic non-alcoholic fatty liver disease.World J Gastroenterol2015;21:1189-96 PMCID:PMC4306163

[5]

Al-Sharhan F,Barat M.MRI presentation of hepatocellular carcinoma in non-alcoholic steatohepatitis (NASH).Eur J Radiol2019;119:108648

[6]

Mikuriya Y,Kobayashi T.Clinicopathological features of hepatocellular carcinoma in patients with nonalcoholic fatty liver disease.Langenbecks Arch Surg2015;400:471-6

[7]

Asfari MM,Alomari M,Dasarathy S.The association of nonalcoholic steatohepatitis and hepatocellular carcinoma.Eur J Gastroenterol Hepatol2020;32:1566-70 PMCID:PMC7431369

[8]

Llovet JM,Heikenwalder M.Immunotherapies for hepatocellular carcinoma.Nat Rev Clin Oncol2022;19:151-72

[9]

Rizzo A,Di Federico A.Predictive biomarkers for checkpoint inhibitor-based immunotherapy in hepatocellular carcinoma: where do we stand?.Front Oncol2021;11:803133 PMCID:PMC8718608

[10]

Finn RS,Ikeda M.IMbrave150 InvestigatorsAtezolizumab plus bevacizumab in unresectable hepatocellular carcinoma.N Engl J Med2020;382:1894-905

[11]

Lin ZF,Chen JH.Biomarkers for response to immunotherapy in hepatobiliary malignancies.Hepatobiliary Pancreat Dis Int2022;21:413-9

[12]

Gong XQ,Wu YK.Progress of MRI radiomics in hepatocellular carcinoma.Front Oncol2021;11:698373 PMCID:PMC8488263

[13]

Yoon JK,Rhee H.MRI features of histologic subtypes of hepatocellular carcinoma: correlation with histologic, genetic, and molecular biologic classification.Eur Radiol2022;32:5119-33

[14]

Marrero JA,Sirlin CB.Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the study of liver diseases.Hepatology2018;68:723-50

[15]

Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu, European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma.J Hepatol2018;69:182-236

[16]

Patel K.Limitations of non-invasive tests for assessment of liver fibrosis.JHEP Rep2020;2:100067 PMCID:PMC7047178

[17]

Trépo E.Update on NAFLD genetics: from new variants to the clinic.J Hepatol2020;72:1196-209

[18]

Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu, Clinical Practice Guideline Panel, Chair:, EASL Governing Board representative:, Panel members:. EASL clinical practice guidelines on non-invasive tests for evaluation of liver disease severity and prognosis - 2021 update.J Hepatol2021;75:659-89

[19]

Riley TR 3rd,Bruno MA.Bedside ultrasound can predict nonalcoholic fatty liver disease in the hands of clinicians using a prototype image.Dig Dis Sci2006;51:982-5

[20]

Starekova J,Pickhardt PJ.Quantification of liver fat content with CT and MRI: state of the art.Radiology2021;301:250-62 PMCID:PMC8574059

[21]

Pickhardt PJ.Abdominal imaging in the coming decades: better, faster, safer, and cheaper?.Radiology2023;307:e222551

[22]

Huang DQ,Liau J.Comparative efficacy of an optimal exam between ultrasound versus abbreviated MRI for HCC screening in NAFLD cirrhosis: a prospective study.Aliment Pharmacol Ther2022;55:820-7 PMCID:PMC9762322

[23]

Zhang J,Li Y.Diagnostic value of contrast-enhanced ultrasound in hepatocellular carcinoma: a meta-analysis with evidence from 1998 to 2016.Oncotarget2017;8:75418-26 PMCID:PMC5650432

[24]

Available from: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/LI-RADS-CEUS-v2017 [Last accessed on 24 May 2023]

[25]

Kono Y,Cosgrove D.Contrast enhanced ultrasound (CEUS) Liver imaging reporting and data system (LI-RADS®): the official version by the American college of radiology (ACR).Ultraschall Med2017;38:85-6

[26]

Hu YX,Han J.Diagnosis of non-hepatocellular carcinoma malignancies in patients with risks for hepatocellular carcinoma: CEUS LI-RADS versus CT/MRI LI-RADS.Front Oncol2021;11:641195 PMCID:PMC8074676

[27]

Schellhaas B,Strobel D.DEGUM CEUS HCC Study GroupContrast-enhanced ultrasound pattern of hepatocellular carcinoma in noncirrhotic liver - results from the prospective multicentre DEGUM CEUS HCC study.Eur J Gastroenterol Hepatol2023;35:313-9

[28]

Bartolotta TV,Bruno E.Focal liver lesions in cirrhosis: role of contrast-enhanced ultrasonography.World J Radiol2022;14:70-81 PMCID:PMC9124982

[29]

Eisenbrey JR,Savsani E.Contrast-enhanced ultrasound (CEUS) in HCC diagnosis and assessment of tumor response to locoregional therapies.Abdom Radiol2021;46:3579-95 PMCID:PMC8569604

[30]

Westwood M,Grutters J.Contrast-enhanced ultrasound using SonoVue® (sulphur hexafluoride microbubbles) compared with contrast-enhanced computed tomography and contrast-enhanced magnetic resonance imaging for the characterisation of focal liver lesions and detection of liver metastases: a systematic review and cost-effectiveness analysis.Health Technol Assess2013;17:1-243 PMCID:PMC4781376

[31]

Snowberger N,Lepe RM.Alpha fetoprotein, ultrasound, computerized tomography and magnetic resonance imaging for detection of hepatocellular carcinoma in patients with advanced cirrhosis.Aliment Pharmacol Ther2007;26:1187-94

[32]

Rode A,Douek P.Small nodule detection in cirrhotic livers: evaluation with US, spiral CT, and MRI and correlation with pathologic examination of explanted liver.J Comput Assist Tomogr2001;25:327-36

[33]

Power SP,Twomey M,O'Connor OJ.Computed tomography and patient risk: facts, perceptions and uncertainties.World J Radiol2016;8:902-15 PMCID:PMC5183924

[34]

Renzulli M.Bologna Liver Oncology Group (BLOG)Proposal of a new diagnostic algorithm for hepatocellular carcinoma based on the Japanese guidelines but adapted to the Western world for patients under surveillance for chronic liver disease.J Gastroenterol Hepatol2016;31:69-80

[35]

Golfieri R,Ascanio S.Focal lesions in the cirrhotic liver: their pivotal role in gadoxetic acid-enhanced MRI and recognition by the Western guidelines.Dig Dis2014;32:696-704

[36]

Inoue T,Komuta M.Assessment of Gd-EOB-DTPA-enhanced MRI for HCC and dysplastic nodules and comparison of detection sensitivity versus MDCT.J Gastroenterol2012;47:1036-47

[37]

Lee YJ,Lee JS.Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis.Radiology2015;275:97-109

[38]

Choi JY,Sirlin CB.CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features.Radiology2014;273:30-50 PMCID:PMC4263770

[39]

Kim SJ.Safety issues and updates under MR environments.Eur J Radiol2017;89:7-13

[40]

Pasquini L,Visconti E.Gadolinium-based contrast agent-related toxicities.CNS Drugs2018;32:229-40

[41]

Nahon P,Layese R.ANRS CO12 CirVirANRS CO22 HepatherScientific Committee – Voting membersCIRRAL groupsEarly hepatocellular carcinoma detection using magnetic resonance imaging is cost-effective in high-risk patients with cirrhosis.JHEP Rep2022;4:100390 PMCID:PMC8683591

[42]

Kim SY,Lim YS.MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma.JAMA Oncol2017;3:456-63 PMCID:PMC5470420

[43]

Kim HA,Choi JI.Comparison of biannual ultrasonography and annual non-contrast liver magnetic resonance imaging as surveillance tools for hepatocellular carcinoma in patients with liver cirrhosis (MAGNUS-HCC): a study protocol.BMC Cancer2017;17:877 PMCID:PMC5740703

[44]

Cunha G, Chernyak V, Fowler KJ, Sirlin CB. Up-to-date role of CT/MRI LI-RADS in hepatocellular carcinoma.J Hepatocell Carcinoma2021;8:513-27 PMCID:PMC8180267

[45]

Liu JKJ,Tan CH.Evaluation of non-contrast magnetic resonance imaging as an imaging surveillance tool for hepatocellular carcinoma in at-risk patients.Singapore Med J2022;63:203-8 PMCID:PMC9251266

[46]

LIRADS R. Available from: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/LI-RADS-CT-MRI-v2018 [Last accessed on 6 May 2023]

[47]

Davenport MS,Al-Hawary MM.Comparison of acute transient dyspnea after intravenous administration of gadoxetate disodium and gadobenate dimeglumine: effect on arterial phase image quality.Radiology2013;266:452-61

[48]

Horowitz JM,Arif-Tiwari H.Expert panel on gastrointestinal imaging:ACR appropriateness criteria(®) chronic liver disease.J Am Coll Radiol2017;14:S103-17

[49]

Chang SD,Chernyak V.MR imaging contrast agents: role in imaging of chronic liver diseases.Magn Reson Imaging Clin N Am2021;29:329-45

[50]

Min JH,Kim YK.Prospective intraindividual comparison of magnetic resonance imaging with gadoxetic acid and extracellular contrast for diagnosis of hepatocellular carcinomas using the liver imaging reporting and data system.Hepatology2018;68:2254-66

[51]

Liu X,Chen J,Huang Z.Gadoxetic acid disodium-enhanced magnetic resonance imaging outperformed multidetector computed tomography in diagnosing small hepatocellular carcinoma: a meta-analysis.Liver Transpl2017;23:1505-18

[52]

Ueno A,Yamazaki K.OATP1B3 expression is strongly associated with Wnt/β-catenin signalling and represents the transporter of gadoxetic acid in hepatocellular carcinoma.J Hepatol2014;61:1080-7

[53]

Taouli B.Diffusion-weighted MR imaging of the liver.Radiology2010;254:47-66

[54]

Semelka RC,Ascher SM.Hepatic hemangiomas: a multi-institutional study of appearance on T2-weighted and serial gadolinium-enhanced gradient-echo MR images.Radiology1994;192:401-6

[55]

Kang HJ,Lee DH.Gadoxetate-enhanced MRI features of proliferative hepatocellular carcinoma are prognostic after surgery.Radiology2021;300:572-82

[56]

Moon JY,Kim YK.Prognosis after curative resection of single hepatocellular carcinoma with a focus on LI-RADS targetoid appearance on preoperative gadoxetic acid-enhanced MRI.Korean J Radiol2021;22:1786-96 PMCID:PMC8546127

[57]

Kim SS,Kim MJ.Prognostic factors of gadoxetic acid-enhanced MRI for postsurgical outcomes in multicentric hepatocellular carcinoma.Eur Radiol2021;31:3405-16

[58]

Motosugi U,Sou H.Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging.Radiology2010;256:151-8

[59]

Davenport MS,Pang Y,Chenevert TL.Effect of gadoxetate disodium on arterial phase respiratory waveforms using a quantitative fast fourier transformation-based analysis.AJR Am J Roentgenol2017;208:328-36

[60]

Lanier H,Khanna G.Rate of gadoxetate disodium (Eovist®) induced transient respiratory motion in children and young adults.Abdom Radiol2020;45:101-6

[61]

Marks RM,Chernyak V.LI-RADS: past, present, and future, from the AJR special series on radiology reporting and data systems.AJR Am J Roentgenol2021;216:295-304

[62]

Elsayes KM,Chernyak V.LI-RADS: a conceptual and historical review from its beginning to its recent integration into AASLD clinical practice guidance.J Hepatocell Carcinoma2019;6:49-69

[63]

Cunha GM,Fowler KJ.Imaging diagnosis of hepatocellular carcinoma: LI-RADS.Chin Clin Oncol2021;10:3

[64]

An C,Choi JY,Roh YH.Noncontrast magnetic resonance imaging versus ultrasonography for hepatocellular carcinoma surveillance (MIRACLE-HCC): study protocol for a prospective randomized trial.BMC Cancer2018;18:915 PMCID:PMC6154402

[65]

Available from: https://clinicaltrials.gov/ct2/show/NCT04539717[Last accessed on 24 May 2023]

[66]

Vietti Violi N,Liao J.Gadoxetate-enhanced abbreviated MRI is highly accurate for hepatocellular carcinoma screening.Eur Radiol2020;30:6003-13

[67]

Chan MV,Ong YY.HCC screening: assessment of an abbreviated non-contrast MRI protocol.Eur Radiol Exp2019;3:49 PMCID:PMC6920271

[68]

Kim DW,Kim SY.Diagnostic performance of MRI for HCC according to contrast agent type: a systematic review and meta-analysis.Hepatol Int2020;14:1009-22

[69]

Roberts LR,Zaiem F.Imaging for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis.Hepatology2018;67:401-21

[70]

Liu YI,Jeffrey RB.Quantitatively defining washout in hepatocellular carcinoma.AJR Am J Roentgenol2013;200:84-9

[71]

Barat M,Hollande C.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 Radiol2021;138:109651

[72]

Thompson SM,Ehman EC.Non-alcoholic fatty liver disease-associated hepatocellular carcinoma: effect of hepatic steatosis on major hepatocellular carcinoma features at MRI.Br J Radiol2018;91:20180345 PMCID:PMC6319849

[73]

Valenti L,Colombo M.Distinctive features of hepatocellular carcinoma in non-alcoholic fatty liver disease.Dig Liver Dis2022;54:154-63

[74]

Kim HL,Park JA.Magnetic resonance imaging is cost-effective for hepatocellular carcinoma surveillance in high-risk patients with cirrhosis.Hepatology2019;69:1599-613

[75]

Pocha C.Hepatocellular carcinoma in alcoholic and non-alcoholic fatty liver disease-one of a kind or two different enemies? Transl Gastroenterol Hepatol 2019;4:p. 72.

[76]

Ioannou GN,Lowy E,Berry K.Differences in hepatocellular carcinoma risk, predictors and trends over time according to etiology of cirrhosis.PLoS One2018;13:e0204412 PMCID:PMC6160079

[77]

Yang JD,Mara KC.GALAD score for hepatocellular carcinoma detection in comparison with liver ultrasound and proposal of GALADUS score.Cancer Epidemiol Biomarkers Prev2019;28:531-8 PMCID:PMC6401221

[78]

Best J,Sowa JP.GALAD Score detects early hepatocellular carcinoma in an international cohort of patients with nonalcoholic steatohepatitis.Clin Gastroenterol Hepatol2020;18:728-735.e4

[79]

Ohki T,Shiina S.Visceral fat accumulation is an independent risk factor for hepatocellular carcinoma recurrence after curative treatment in patients with suspected NASH.Gut2009;58:839-44

[80]

Fujiwara N,Kudo Y.Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma.J Hepatol2015;63:131-40

[81]

Welzel TM,Zeuzem S.Metabolic syndrome increases the risk of primary liver cancer in the United States: a study in the SEER-Medicare database.Hepatology2011;54:463-71 PMCID:PMC4141525

[82]

Chen CL,Yang WS.Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan.Gastroenterology2008;135:111-21

[83]

Wideroff L,Mellemkjaer L.Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark.J Natl Cancer Inst1997;89:1360-5

[84]

Adami HO,Nyrén O.Excess risk of primary liver cancer in patients with diabetes mellitus.J Natl Cancer Inst1996;88:1472-7

[85]

El-Serag HB,Javadi F.The association between diabetes and hepatocellular carcinoma: a systematic review of epidemiologic evidence.Clin Gastroenterol Hepatol2006;4:369-80

[86]

Rosmorduc O.HCC and NASH: how strong is the clinical demonstration?.Clin Res Hepatol Gastroenterol2012;36:202-8

[87]

Pais R., Temporal trends, clinical patterns and outcomes of NAFLD-related HCC in patients undergoing liver resection over a 20-year period.Aliment Pharmacol Ther2017;46:p.856-63.

[88]

Sorrentino P.Liver iron excess in patients with hepatocellular carcinoma developed on non-alcoholic steato-hepatitis. J Hepatol 2009;50:p.351-7.

[89]

Zhang H,Fang L,Yao SK.Metformin and reduced risk of hepatocellular carcinoma in diabetic patients: a meta-analysis.Scand J Gastroenterol2013;48:78-87

[90]

Tan JL,Woodman R.Regular Aspirin Use Is Associated with a Reduced Risk of Hepatocellular Carcinoma (HCC) in Chronic Liver Disease: a Systematic Review and Meta-analysis.J Gastrointest Cancer2022;

[91]

Goh MJ.Statin and aspirin for chemoprevention of hepatocellular carcinoma: Time to use or wait further?.Clin Mol Hepatol2022;28:p.380-395.

[92]

Yamaoka K,Kinowaki K.Clinicopathological assessment of steatohepatitic hepatocellular carcinoma.Clin Res Hepatol Gastroenterol2022;46:101799

[93]

Park EJ,Choi SH.Imaging features of hepatocellular carcinoma in nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: a systematic review and meta-analysis.Abdom Radiol2022;47:2089-98

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