J Liver Cancer.  2020 Sep;20(2):99-105. 10.17998/jlc.20.2.99.

Imaging Modalities for Hepatocellular Carcinoma Surveillance: Expanding Horizons beyond Ultrasound

Affiliations
  • 1Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

Abstract

In Asian countries favoring loco-regional treatment such as surgical resection or ablation, very early-stage hepatocellular carcinoma (HCC) should be the main target for surveillance. Even though ultrasound (US) has been accepted as a primary imaging modality for HCC surveillance, its performance in detecting very early-stage HCCs is insufficient. Moreover, in more than 20% of patients at high risk for HCC, visualization of the liver on US may be limited owing to the advanced distortion and heterogeneity of the liver parenchyma. Recently revised HCC clinical guidelines allow the use of alternative surveillance tools including computed tomography or magnetic resonance imaging in patients with inadequate US exams. This paper summarizes the findings of recent studies using imaging modalities other than US as surveillance tools for HCC as well as strengths and limitations of these modalities.

Keyword

Hepatocellular carcinoma; Surveillance; Imaging

Reference

1. Kim NM, Doh YS, Jang JW, Kim SH, Eun HS, Jun JH, et al. Discrepancy between the actual clinical status of patients with hepatocellular carcinoma and expectations from hepatocellular carcinoma surveillance: a single-center study. J Liver Cancer. 2019; 19:30–37.
2. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatocellular carcinoma. J Hepatol. 2018; 69:182–236.
3. 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.
4. Korean Liver Cancer Association, National Cancer Center. 2018 Korean Liver Cancer Association-National Cancer Center Korea practice guidelines for the management of hepatocellular carcinoma. Gut Liver. 2019; 13:227–299.
5. Park JW, Chen M, Colombo M, Roberts LR, Schwartz M, Chen PJ, et al. Global patterns of hepatocellular carcinoma management from diagnosis to death: the BRIDGE Study. Liver Int. 2015; 35:2155–2166.
6. Yang JD. Detect or not to detect very early stage hepatocellular carcinoma? The western perspective. Clin Mol Hepatol. 2019; 25:335–343.
7. Hwang S, Lee YJ, Kim KH, Ahn CS, Moon DB, Ha TY, et al. The impact of tumor size on long-term survival outcomes after resection of solitary hepatocellular carcinoma: single-institution experience with 2558 patients. J Gastrointest Surg. 2015; 19:1281–1290.
8. Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg. 2015; 261:947–955.
9. Groeschl RT, Gamblin TC, Turaga KK. Ablation for hepatocellular carcinoma: validating the 3-cm breakpoint. Ann Surg Oncol. 2013; 20:3591–3595.
10. Brunt E, Aishima S, Clavien PA, Fowler K, Goodman Z, Gores G, et al. cHCC-CCA: Consensus terminology for primary liver carcinomas with both hepatocytic and cholangiocytic differentation. Hepatology. 2018; 68:113–126.
11. Livraghi T, Meloni F, Di Stasi M, Rolle E, Solbiati L, Tinelli C, et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: is resection still the treatment of choice? Hepatology. 2008; 47:82–89.
12. Takayama T, Makuuchi M, Hirohashi S, Sakamoto M, Yamamoto J, Shimada K, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology. 1998; 28:1241–1246.
13. Shindoh J, Andreou A, Aloia TA, Zimmitti G, Lauwers GY, Laurent A, et al. Microvascular invasion does not predict long-term survival in hepatocellular carcinoma up to 2 cm: reappraisal of the staging system for solitary tumors. Ann Surg Oncol. 2013; 20:1223–1229.
14. Goldberg SN, Grassi CJ, Cardella JF, Charboneau JW, Dodd GD 3rd, Dupuy DE, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria. J Vasc Interv Radiol. 2009; 20(7 Suppl):S377–S390.
15. 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.
16. 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.
17. 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.e1701.
18. 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.
19. 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.
20. 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.
21. Yu NC, Chaudhari V, Raman SS, Lassman C, Tong MJ, Busuttil RW, et al. CT and MRI improve detection of hepatocellular carcinoma, compared with ultrasound alone, in patients with cirrhosis. Clin Gastroenterol Hepatol. 2011; 9:161–167.
22. 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.
23. Pocha C, Dieperink E, McMaken KA, Knott A, Thuras P, Ho SB. Surveillance for hepatocellular cancer with ultrasonography vs. computed tomography -- a randomised study. Aliment Pharmacol Ther. 2013; 38:303–312.
24. Roberts LR, Sirlin CB, Zaiem F, Almasri J, Prokop LJ, Heimbach JK, et al. Imaging for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Hepatology. 2018; 67:401–421.
25. Kierans AS, Kang SK, Rosenkrantz AB. The diagnostic performance of dynamic contrast-enhanced MR imaging for detection of small hepatocellular carcinoma measuring up to 2 cm: a meta-analysis. Radiology. 2016; 278:82–94.
26. Chou R, Cuevas C, Fu R, Devine B, Wasson N, Ginsburg A, et al. Imaging techniques for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Ann Intern Med. 2015; 162:697–711.
27. Choi SH, Byun JH, Lim YS, Yu E, Lee SJ, Kim SY, et al. Diagnostic criteria for hepatocellular carcinoma ≤3 cm with hepatocyte-specific contrast-enhanced magnetic resonance imaging. J Hepatol. 2016; 64:1099–1107.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. Rogosnitzky M, Branch S. Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms. Biometals. 2016; 29:365–376.
35. Levine D, McDonald RJ, Kressel HY. Gadolinium retention after contrast-enhanced MRI. JAMA. 2018; 320:1853–1854.
36. Kim YK, Kim YK, Park HJ, Park MJ, Lee WJ, Choi D. Noncontrast MRI with diffusion-weighted imaging as the sole imaging modality for detecting liver malignancy in patients with high risk for hepatocellular carcinoma. Magn Reson Imaging. 2014; 32:610–618.
37. Han S, Choi JI, Park MY, Choi MH, Rha SE, Lee YJ. the diagnostic performance of liver MRI without intravenous contrast for detecting hepatocellular carcinoma: a case-controlled feasibility study. Korean J Radiol. 2018; 19:568–577.
38. 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.
39. Maruyama H, Shiina S. Contrast-enhanced ultrasonography: is it an ideal tool for hepatocellular carcinoma surveillance? Quant Imaging Med Surg. 2019; 9:1611–1614.
40. Park JH, Park MS, Lee SJ, Jeong WK, Lee JY, Park MJ, et al. Contrast-enhanced US with perfluorobutane for hepatocellular carcinoma surveillance: a multicenter diagnostic trial (SCAN). Radiology. 2019; 292:638–646.
41. Kudo M, Ueshima K, Osaki Y, Hirooka M, Imai Y, Aso K, et al. B-Mode ultrasonography versus contrast-enhanced ultrasonography for surveillance of hepatocellular carcinoma: a prospective multicenter randomized controlled trial. Liver Cancer. 2019; 8:271–280.
42. Su TH, Kao JH. Surveillance of hepatocellular carcinoma by magnetic resonance imaging with liver-specific contrast. JAMA Oncol. 2017; 3:446–447.
43. 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.
44. 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.
45. Ruggeri M. Hepatocellular carcinoma: cost-effectiveness of screening. A systematic review. Risk Manag Healthc Policy. 2012; 5:49–54.
46. 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.
47. 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.
48. Atiq O, Tiro J, Yopp AC, Muffler A, Marrero JA, Parikh ND, et al. An assessment of benefits and harms of hepatocellular carcinoma surveillance in patients with cirrhosis. Hepatology. 2017; 65:1196–1205.
Full Text Links
  • JLC
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr