Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Current Landscape and Future Perspectives of Abbreviated MRI for Hepatocellular Carcinoma Surveillance

  • Hyo Jung, Park (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Nieun Seo (Department of Radiology, Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • So Yeon Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • Received : 2021.11.28
  • Accepted : 2022.02.10
  • Published : 2022.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

While ultrasound (US) is considered an important tool for hepatocellular carcinoma (HCC) surveillance, it has limited sensitivity for detecting early-stage HCC. Abbreviated MRI (AMRI) has recently gained popularity owing to better sensitivity in its detection of early-stage HCC than US, while also minimizing the time and cost in comparison to complete contrast-enhanced MRI, as AMRI includes only a few essential sequences tailored for detecting HCC. Currently, three AMRI protocols exist, namely gadoxetic acid-enhanced hepatobiliary-phase AMRI, dynamic contrast-enhanced AMRI, and non-enhanced AMRI. In this study, we discussed the rationale and technical details of AMRI techniques for achieving optimal surveillance performance. The strengths, weaknesses, and current issues of each AMRI protocol were also elucidated. Moreover, we scrutinized previously performed AMRI studies regarding clinical and technical factors. Reporting and recall strategies were discussed while considering the differences in AMRI protocols. A risk-stratified approach for the target population should be taken to maximize the benefits of AMRI and the cost-effectiveness should be considered. In the era of multiple HCC surveillance tools, patients need to be fully informed about their choices for better adherence to a surveillance program.

Keywords

References

  1. Llovet JM, Kelley RK, Villanueva A, Singal AG, Pikarsky E, Roayaie S, et al. Hepatocellular carcinoma. Nat Rev Dis Primers 2021;7:6
  2. Global Burden of Disease Liver Cancer Collaboration. The burden of primary liver cancer and underlying etiologies from 1990 to 2015 at the global, regional, and national level: results from the global burden of disease study 2015. JAMA Oncol 2017;3:1683-1691
  3. Petrick JL, Kelly SP, Altekruse SF, McGlynn KA, Rosenberg PS. Future of hepatocellular carcinoma incidence in the United States forecast through 2030. J Clin Oncol 2016;34:1787-1794
  4. Zhang BH, Yang BH, Tang ZY. Randomized controlled trial of screening for hepatocellular carcinoma. J Cancer Res Clin Oncol 2004;130:417-422
  5. Kim DH, Choi SH, Shim JH, Kim SY, Lee SS, Byun JH, et al. Meta-analysis of the accuracy of abbreviated magnetic resonance imaging for hepatocellular carcinoma surveillance: non-contrast versus hepatobiliary phase-abbreviated magnetic resonance imaging. Cancers (Basel) 2021;13:2975
  6. 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;68:723-750
  7. Korean Liver Cancer Association (KLCA), National Cancer Center (NCC). 2018 Korean Liver Cancer Association-National Cancer Center Korea practice guidelines for the management of hepatocellular carcinoma. Korean J Radiol 2019;20:1042-1113
  8. Bolondi L. Screening for hepatocellular carcinoma in cirrhosis. J Hepatol 2003;39:1076-1084
  9. Singal A, Volk ML, Waljee A, Salgia R, Higgins P, Rogers MA, et al. Meta-analysis: surveillance with ultrasound for early-stage hepatocellular carcinoma in patients with cirrhosis. Aliment Pharmacol Ther 2009;30:37-47
  10. Tzartzeva K, Obi J, Rich NE, Parikh ND, Marrero JA, Yopp A, et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology 2018;154:1706-1718.e1
  11. Kim SY, An J, Lim YS, Han S, Lee JY, Byun JH, et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncol 2017;3:456-463
  12. Yoon JH, Lee JM, Lee DH, Joo I, Jeon JH, Ahn SJ, et al. A comparison of biannual two-phase low-dose liver CT and US for HCC surveillance in a group at high risk of HCC development. Liver Cancer 2020;9:503-517
  13. Gupta P, Soundararajan R, Patel A, Kumar-M P, Sharma V, Kalra N. Abbreviated MRI for hepatocellular carcinoma screening: a systematic review and meta-analysis. J Hepatol 2021;75:108-119
  14. Chan MV, Huo YR, Trieu N, Mitchelle A, George J, He E, et al. Noncontrast MRI for hepatocellular carcinoma detection: a systematic review and meta-analysis-a potential surveillance tool? Clin Gastroenterol Hepatol 2022;20:44-56.e2
  15. Kim DH, Choi SH, Shim JH, Kim SY, Lee SS, Byun JH, et al. Magnetic resonance imaging for surveillance of hepatocellular carcinoma: a systematic review and metaanalysis. Diagnostics (Basel) 2021;11:1665
  16. Brunsing RL, Chen DH, Schlein A, Wolfson T, Gamst A, Mamidipalli A, et al. Gadoxetate-enhanced abbreviated MRI for hepatocellular carcinoma surveillance: preliminary experience. Radiol Imaging Cancer 2019;1:e190010
  17. Vietti Violi N, Lewis S, Liao J, Hulkower M, Hernandez-Meza G, Smith K, et al. Gadoxetate-enhanced abbreviated MRI is highly accurate for hepatocellular carcinoma screening. Eur Radiol 2020;30:6003-6013
  18. An JY, Pena MA, Cunha GM, Booker MT, Taouli B, Yokoo T, et al. Abbreviated MRI for hepatocellular carcinoma screening and surveillance. Radiographics 2020;40:1916-1931
  19. Ahn SS, Kim MJ, Lim JS, Hong HS, Chung YE, Choi JY. Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 2010;255:459-466
  20. Ueno A, Masugi Y, Yamazaki K, Komuta M, Effendi K, Tanami Y, et al. OATP1B3 expression is strongly associated with Wnt/β-catenin signalling and represents the transporter of gadoxetic acid in hepatocellular carcinoma. J Hepatol 2014;61:1080-1087
  21. Joo I, Kim SY, Kang TW, Kim YK, Park BJ, Lee YJ, et al. Radiologic-pathologic correlation of hepatobiliary phase hypointense nodules without arterial phase hyperenhancement at gadoxetic acid-enhanced MRI: a multicenter study. Radiology 2020;296:335-345
  22. Joo I, Lee JM, Lee DH, Jeon JH, Han JK, Choi BI. Noninvasive diagnosis of hepatocellular carcinoma on gadoxetic acid-enhanced MRI: can hypointensity on the hepatobiliary phase be used as an alternative to washout? Eur Radiol 2015;25:2859-2868
  23. Kim TK, Lee E, Jang HJ. Imaging findings of mimickers of hepatocellular carcinoma. Clin Mol Hepatol 2015;21:326-343
  24. Kim YK, Lee WJ, Park MJ, Kim SH, Rhim H, Choi D. Hypovascular hypointense nodules on hepatobiliary phase gadoxetic acid-enhanced MR images in patients with cirrhosis: potential of DW imaging in predicting progression to hypervascular HCC. Radiology 2012;265:104-114
  25. Piana G, Trinquart L, Meskine N, Barrau V, Beers BV, Vilgrain V. New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Hepatol 2011;55:126-132
  26. Vandecaveye V, De Keyzer F, Verslype C, Op de Beeck K, Komuta M, Topal B, et al. Diffusion-weighted MRI provides additional value to conventional dynamic contrast-enhanced MRI for detection of hepatocellular carcinoma. Eur Radiol 2009;19:2456-2466
  27. Park HJ, Jang HY, Kim SY, Lee SJ, Won HJ, Byun JH, et al. Non-enhanced magnetic resonance imaging as a surveillance tool for hepatocellular carcinoma: comparison with ultrasound. J Hepatol 2020;72:718-724
  28. Kim HJ, Lee SS, Byun JH, Kim JC, Yu CS, Park SH, et al. Incremental value of liver MR imaging in patients with potentially curable colorectal hepatic metastasis detected at CT: a prospective comparison of diffusion-weighted imaging, gadoxetic acid-enhanced MR imaging, and a combination of both MR techniques. Radiology 2015;274:712-722
  29. Taouli B, Koh DM. Diffusion-weighted MR imaging of the liver. Radiology 2010;254:47-66
  30. Barth M, Breuer F, Koopmans PJ, Norris DG, Poser BA. Simultaneous multislice (SMS) imaging techniques. Magn Reson Med 2016;75:63-81
  31. Taron J, Martirosian P, Erb M, Kuestner T, Schwenzer NF, Schmidt H, et al. Simultaneous multislice diffusion-weighted MRI of the liver: analysis of different breathing schemes in comparison to standard sequences. J Magn Reson Imaging 2016;44:865-879
  32. Obele CC, Glielmi C, Ream J, Doshi A, Campbell N, Zhang HC, et al. Simultaneous multislice accelerated free-breathing diffusion-weighted imaging of the liver at 3T. Abdom Imaging 2015;40:2323-2330
  33. Choi JY, Kim MJ, Chung YE, Kim JY, Jones AC, de Becker J, et al. Abdominal applications of 3.0-T MR imaging: comparative review versus a 1.5-T system. Radiographics 2008;28:e30
  34. Semelka RC, Kelekis NL, Thomasson D, Brown MA, Laub GA. HASTE MR imaging: description of technique and preliminary results in the abdomen. J Magn Reson Imaging 1996;6:698-699
  35. Yu JS, Kim KW, Kim YH, Jeong EK, Chien D. Comparison of multishot turbo spin echo and HASTE sequences for T2-weighted MRI of liver lesions. J Magn Reson Imaging 1998;8:1079-1084
  36. Lee MJ, Kim MJ, Yoon CS, Song SY, Park K, Kim WS. The T2-shortening effect of gadolinium and the optimal conditions for maximizing the CNR for evaluating the biliary system: a phantom study. Korean J Radiol 2011;12:358-364
  37. Nakamura Y, Ohmoto T, Saito T, Kajima T, Nishimaru E, Ito K. Effects of gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid on T2-weighted MRCP. Magn Reson Med Sci 2009;8:143-148
  38. Chung TK, Lee CH, Lee J, Choi JW, Kim KA, Park CM. Usefulness of postcontrast T2-weighted images in shortening the total scan time of a gadoxectic acid enhanced MRI of the liver: a comparison between precontrast and postcontrast T2-weighted images. J Korean Soc Radiol 2010;62:249-256
  39. Ahn SJ, Kim MJ, Hong HS, Kim KA, Song HT. Distinguishing hemangiomas from malignant solid hepatic lesions: a comparison of heavily T2-weighted images obtained before and after administration of gadoxetic acid. J Magn Reson Imaging 2011;34:310-317
  40. Lee D, Lee J, Ko J, Yoon J, Ryu K, Nam Y. Deep learning in MR image processing. Investig Magn Reson Imaging 2019;23:81-99
  41. Shanbhogue K, Tong A, Smereka P, Nickel D, Arberet S, Anthopolos R, et al. Accelerated single-shot T2-weighted fat-suppressed (FS) MRI of the liver with deep learning-based image reconstruction: qualitative and quantitative comparison of image quality with conventional T2-weighted FS sequence. Eur Radiol 2021;31:8447-8457
  42. Herrmann J, Gassenmaier S, Nickel D, Arberet S, Afat S, Lingg A, et al. Diagnostic confidence and feasibility of a deep learning accelerated HASTE sequence of the abdomen in a single breath-hold. Invest Radiol 2021;56:313-319
  43. Herrmann J, Nickel D, Mugler JP 3rd, Arberet S, Gassenmaier S, Afat S, et al. Development and evaluation of deep learning-accelerated single-breath-hold abdominal HASTE at 3 T using variable refocusing flip angles. Invest Radiol 2021;56:645-652
  44. Hu Z, Wang Y, Zhang Z, Zhang J, Zhang H, Guo C, et al. Distortion correction of single-shot EPI enabled by deep-learning. Neuroimage 2020;221:117170
  45. American College of Radiology. CT/MRI LI-RADS® v2018 CORE. Web site. https://www.acr.org/-/media/ACR/Files/RADS/LI-RADS/LI-RADS-2018-Core.pdf?la=en. Published 2018. Accessed November 7, 2021
  46. Besa C, Lewis S, Pandharipande PV, Chhatwal J, Kamath A, Cooper N, et al. Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdom Radiol (NY) 2017;42:179-190
  47. Park SH, Kim B, Kim SY, Shim YS, Kim JH, Huh J, et al. Abbreviated MRI with optional multiphasic CT as an alternative to full-sequence MRI: LI-RADS validation in a HCC-screening cohort. Eur Radiol 2020;30:2302-2311
  48. Hernando D, Wells SA, Vigen KK, Reeder SB. Effect of hepatocyte-specific gadolinium-based contrast agents on hepatic fat-fraction and R2*. Magn Reson Imaging 2015;33:43-50
  49. Koo NH, Choi KW, Yoo BG. Effect of Gd-EOB-DTPA on hepatic fat quantification using two-point Dixon technique. Journal of Korea Contents Association 2017;17:215-221
  50. Park CC, Hamilton G, Desai A, Zand KA, Wolfson T, Hooker JC, et al. Effect of intravenous gadoxetate disodium and flip angle on hepatic proton density fat fraction estimation with six-echo, gradient-recalled-echo, magnitude-based MR imaging at 3T. Abdom Radiol (NY) 2017;42:1189-1198
  51. Marks RM, Ryan A, Heba ER, Tang A, Wolfson TJ, Gamst AC, et al. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. AJR Am J Roentgenol 2015;204:527-535
  52. Tillman BG, Gorman JD, Hru JM, Lee MH, King MC, Sirlin CB, et al. Diagnostic per-lesion performance of a simulated gadoxetate disodium-enhanced abbreviated MRI protocol for hepatocellular carcinoma screening. Clin Radiol 2018;73:485-493
  53. Park HJ, Kim SY, Singal AG, Lee SJ, Won HJ, Byun JH, et al. Abbreviated magnetic resonance imaging vs ultrasound for surveillance of hepatocellular carcinoma in highrisk patients. Liver Int 2021 Nov [Epub]. https://doi.org/10.1111/liv.15110
  54. Whang S, Choi MH, Choi JI, Youn SY, Kim DH, Rha SE. Comparison of diagnostic performance of non-contrast MRI and abbreviated MRI using gadoxetic acid in initially diagnosed hepatocellular carcinoma patients: a simulation study of surveillance for hepatocellular carcinomas. Eur Radiol 2020;30:4150-4163
  55. American College of Radiology. Ultrasound LI-RADS® v2017. Web site. https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/Ultrasound-LI-RADS-v2017. Accessed November 11, 2021
  56. Kim JY, Lee SS, Byun JH, Kim SY, Park SH, Shin YM, et al. Biologic factors affecting HCC conspicuity in hepatobiliary phase imaging with liver-specific contrast agents. AJR Am J Roentgenol 2013;201:322-331
  57. Kim SY, Wu EH, Park SH, Wang ZJ, Hope TA, Yee J, et al. Comparison of hepatocellular carcinoma conspicuity on hepatobiliary phase images with gadoxetate disodium vs. delayed phase images with extracellular cellular contrast agent. Abdom Radiol (NY) 2016;41:1522-1531
  58. Brismar TB, Dahlstrom N, Edsborg N, Persson A, Smedby O, Albiin N. Liver vessel enhancement by Gd-BOPTA and Gd- EOB-DTPA: a comparison in healthy volunteers. Acta Radiol 2009;50:709-715
  59. Tamada T, Ito K, Sone T, Yamamoto A, Yoshida K, Kakuba K, et al. Dynamic contrast-enhanced magnetic resonance imaging of abdominal solid organ and major vessel: comparison of enhancement effect between Gd-EOB-DTPA and Gd-DTPA. J Magn Reson Imaging 2009;29:636-640
  60. Davenport MS, Viglianti BL, Al-Hawary MM, Caoili EM, Kaza RK, Liu PS, et al. Comparison of acute transient dyspnea after intravenous administration of gadoxetate disodium and gadobenate dimeglumine: effect on arterial phase image quality. Radiology 2013;266:452-461
  61. Kim DW, Choi SH, Park T, Kim SY, Lee SS, Byun JH. Transient severe motion artifact on arterial phase in gadoxetic acid-enhanced liver magnetic resonance imaging: a systematic review and meta-analysis. Invest Radiol 2022;57:62-70
  62. Huh J, Kim SY, Yeh BM, Lee SS, Kim KW, Wu EH, et al. Troubleshooting arterial-phase MR images of gadoxetate disodium-enhanced liver. Korean J Radiol 2015;16:1207-1215
  63. Petrasek J, Singal AG, Rich NE. Harms of hepatocellular carcinoma surveillance. Curr Hepatol Rep 2019;18:383-389
  64. Takizawa D, Kakizaki S, Sohara N, Sato K, Takagi H, Arai H, et al. Hepatocellular carcinoma with portal vein tumor thrombosis: clinical characteristics, prognosis, and patient survival analysis. Dig Dis Sci 2007;52:3290-3295
  65. Bae JS, Lee JM, Yoon JH, Jang S, Chung JW, Lee KB, et al. How to best detect portal vein tumor thrombosis in patients with hepatocellular carcinoma meeting the Milan criteria: gadoxetic acid-enhanced MRI versus contrast-enhanced CT. Liver Cancer 2020;9:293-307
  66. Ahn JH, Yu JS, Cho ES, Chung JJ, Kim JH, Kim KW. Diffusion-weighted MRI of malignant versus benign portal vein thrombosis. Korean J Radiol 2016;17:533-540
  67. Sandrasegaran K, Tahir B, Nutakki K, Akisik FM, Bodanapally U, Tann M, et al. Usefulness of conventional MRI sequences and diffusion-weighted imaging in differentiating malignant from benign portal vein thrombus in cirrhotic patients. AJR Am J Roentgenol 2013;201:1211-1219
  68. Rogosnitzky M, Branch S. Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms. Biometals 2016;29:365-376
  69. Levine D, McDonald RJ, Kressel HY. Gadolinium retention after contrast-enhanced MRI. JAMA 2018;320:1853-1854
  70. Lee JY, Huo EJ, Weinstein S, Santos C, Monto A, Corvera CU, et al. Evaluation of an abbreviated screening MRI protocol for patients at risk for hepatocellular carcinoma. Abdom Radiol (NY) 2018;43:1627-1633
  71. Khatri G, Pedrosa I, Ananthakrishnan L, de Leon AD, Fetzer DT, Leyendecker J, et al. Abbreviated-protocol screening MRI vs. complete-protocol diagnostic MRI for detection of hepatocellular carcinoma in patients with cirrhosis: an equivalence study using LI-RADS v2018. J Magn Reson Imaging 2020;51:415-425
  72. Chernyak V, Fowler KJ, Kamaya A, Kielar AZ, Elsayes KM, Bashir MR, et al. Liver imaging reporting and data system (LI-RADS) version 2018: imaging of hepatocellular carcinoma in at-risk patients. Radiology 2018;289:816-830
  73. Yang JD. Detect or not to detect very early stage hepatocellular carcinoma? The western perspective. Clin Mol Hepatol 2019;25:335-343
  74. Park SH, Kim B, Kim SY, Choi SJ, Huh J, Kim HJ, et al. Characterizing computed tomography-detected arterial hyperenhancing-only lesions in patients at risk of hepatocellular carcinoma: can non-contrast magnetic resonance imaging be used for sequential imaging? Korean J Radiol 2020;21:280-289
  75. Paisant A, Vilgrain V, Riou J, Oberti F, Sutter O, Laurent V, et al. Comparison of extracellular and hepatobiliary MR contrast agents for the diagnosis of small HCCs. J Hepatol 2020;72:937-945
  76. Min JH, Kim JM, Kim YK, Kang TW, Lee SJ, Choi GS, et al. 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. Hepatology 2018;68:2254-2266
  77. Sutherland T, Watts J, Ryan M, Galvin A, Temple F, Vuong J, et al. Diffusion-weighted MRI for hepatocellular carcinoma screening in chronic liver disease: direct comparison with ultrasound screening. J Med Imaging Radiat Oncol 2017;61:34-39
  78. Coates GG, Borrello JA, McFarland EG, Mirowitz SA, Brown JJ. Hepatic T2-weighted MRI: a prospective comparison of sequences, including breath-hold, half-Fourier turbo spin echo (HASTE). J Magn Reson Imaging 1998;8:642-649
  79. Schwartz LH, Seltzer SE, Tempany CM, Silverman SG, Piwnica-Worms DR, Adams DF, et al. Prospective comparison of T2- weighted fast spin-echo, with and without fat suppression, and conventional spin-echo pulse sequences in the upper abdomen. Radiology 1993;189:411-416
  80. Hanna RF, Aguirre DA, Kased N, Emery SC, Peterson MR, Sirlin CB. Cirrhosis-associated hepatocellular nodules: correlation of histopathologic and MR imaging features. Radiographics 2008;28:747-769
  81. Choi MH, Choi JI, Yoon JH, Lee CH, Kang TW, Kim HA, et al. Annual non-contrast liver MRI versus biannual liver ultrasonography for surveillance of HCC in patients with trial. Proceedings of the 76th Annual Meeting of the Korean Congress of Radiology; 2020 Sep 19; Seoul, Korea: Korean Society of Radiology; p. 204
  82. Ahmed NNA, El Gaafary SM, Elia RZ, Abdulhafiz EM. Role of abbreviated MRI protocol for screening of HCC in HCV related cirrhotic patients prior to direct-acting antiviral treatmen. Egypt J Radiol Nucl Med 2020;51:102
  83. Son JH, Choi SH, Kim SY, Jang HY, Byun JH, Won HJ, et al. Validation of US liver imaging reporting and data system version 2017 in patients at high risk for hepatocellular carcinoma. Radiology 2019;292:390-397
  84. Simmons O, Fetzer DT, Yokoo T, Marrero JA, Yopp A, Kono Y, et al. Predictors of adequate ultrasound quality for hepatocellular carcinoma surveillance in patients with cirrhosis. Aliment Pharmacol Ther 2017;45:169-177
  85. Wong LL, Reyes RJ, Kwee SA, Hernandez BY, Kalathil SC, Tsai NC. Pitfalls in surveillance for hepatocellular carcinoma: how successful is it in the real world? Clin Mol Hepatol 2017;23:239-248
  86. Esfeh JM, Hajifathalian K, Ansari-Gilani K. Sensitivity of ultrasound in detecting hepatocellular carcinoma in obese patients compared to explant pathology as the gold standard. Clin Mol Hepatol 2020;26:54-59
  87. Fattovich G. Natural history and prognosis of hepatitis B. Semin Liver Dis 2003;23:47-58
  88. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007;132:2557-2576
  89. Velazquez RF, Rodriguez M, Navascues CA, Linares A, Perez R, Sotorrios NG, et al. Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Hepatology 2003;37:520-527
  90. Goossens N, Singal AG, King LY, Andersson KL, Fuchs BC, Besa C, et al. Cost-effectiveness of risk score-stratified hepatocellular carcinoma screening in patients with cirrhosis. Clin Transl Gastroenterol 2017;8:e101
  91. Kim HL, An J, Park JA, Park SH, Lim YS, Lee EK. Magnetic resonance imaging is cost-effective for hepatocellular carcinoma surveillance in high-risk patients with cirrhosis. Hepatology 2019;69:1599-1613
  92. Singal AG, Yopp AC, Gupta S, Skinner CS, Halm EA, Okolo E, et al. Failure rates in the hepatocellular carcinoma surveillance process. Cancer Prev Res (Phila) 2012;5:1124-1130
  93. Davila JA, Morgan RO, Richardson PA, Du XL, McGlynn KA, El-Serag HB. Use of surveillance for hepatocellular carcinoma among patients with cirrhosis in the United States. Hepatology 2010;52:132-141
  94. Edenvik P, Davidsdottir L, Oksanen A, Isaksson B, Hultcrantz R, Stal P. Application of hepatocellular carcinoma surveillance in a European setting. What can we learn from clinical practice? Liver Int 2015;35:1862-1871
  95. Zhao C, Jin M, Le RH, Le MH, Chen VL, Jin M, et al. Poor adherence to hepatocellular carcinoma surveillance: a systematic review and meta-analysis of a complex issue. Liver Int 2018;38:503-514
  96. Singal AG, Volk ML, Rakoski MO, Fu S, Su GL, McCurdy H, et al. Patient involvement in healthcare is associated with higher rates of surveillance for hepatocellular carcinoma. J Clin Gastroenterol 2011;45:727-732
  97. Woolen SA, Singal AG, Davenport MS, Troost JP, Khalatbari S, Mittal S, et al. Patient preferences for hepatocellular carcinoma surveillance parameters. Clin Gastroenterol Hepatol 2022;20:204-215.e6
  98. European Society of Radiology (ESR). ESR concept paper on value-based radiology. Insights Imaging 2017;8:447-454
  99. Arguedas MR, Chen VK, Eloubeidi MA, Fallon MB. Screening for hepatocellular carcinoma in patients with hepatitis C cirrhosis: a cost-utility analysis. Am J Gastroenterol 2003;98:679-690
  100. Cucchetti A, Trevisani F, Cescon M, Ercolani G, Farinati F, Poggio PD, et al. Cost-effectiveness of semi-annual surveillance for hepatocellular carcinoma in cirrhotic patients of the Italian liver cancer population. J Hepatol 2012;56:1089-1096
  101. Ruggeri M. Hepatocellular carcinoma: cost-effectiveness of screening. A systematic review. Risk Manag Healthc Policy 2012;5:49-54