DOI QR코드

DOI QR Code

Noninvasive Diagnosis of Hepatocellular Carcinoma: Elaboration on Korean Liver Cancer Study Group-National Cancer Center Korea Practice Guidelines Compared with Other Guidelines and Remaining Issues

  • Yoon, Jeong Hee (Department of Radiology, Seoul National University Hospital) ;
  • Park, Joong-Won (Center for Liver Cancer, National Cancer Center) ;
  • Lee, Jeong Min (Department of Radiology, Seoul National University Hospital)
  • 투고 : 2015.05.07
  • 심사 : 2015.09.30
  • 발행 : 2016.02.01

초록

Hepatocellular carcinoma (HCC) can be diagnosed based on characteristic findings of arterial-phase enhancement and portal/delayed "washout" in cirrhotic patients. Several countries and major academic societies have proposed varying specific diagnostic criteria for HCC, largely reflecting the variable HCC prevalence in different regions and ethnic groups, as well as different practice patterns. In 2014, a new version of Korean practice guidelines for management of HCC was released by the Korean Liver Cancer Study Group (KLCSG) and the National Cancer Center (NCC). According to the KLCSG-NCC Korea practice guidelines, if the typical hallmark of HCC (i.e., hypervascularity in the arterial phase with washout in the portal or 3 min-delayed phases) is identified in a nodule ${\geq}1cm$ in diameter on either dynamic CT, dynamic MRI, or MRI using hepatocyte-specific contrast agent in high-risk groups, a diagnosis of HCC is established. In addition, the KLCSG-NCC Korea practice guidelines provide criteria to diagnose HCC for subcentimeter hepatic nodules according to imaging findings and tumor marker, which has not been addressed in other guidelines such as Association for the Study of Liver Diseases and European Association for the Study of the Liver. In this review, we briefly review the new HCC diagnostic criteria endorsed by the 2014 KLCSG-NCC Korea practice guidelines, in comparison with other recent guidelines; we furthermore address several remaining issues in noninvasive diagnosis of HCC, including prerequisite of sonographic demonstration of nodules, discrepancy between transitional phase and delayed phase, and implementation of ancillary features for HCC diagnosis.

키워드

참고문헌

  1. El-Serag HB. Hepatocellular carcinoma. N Engl J Med 2011;365:1118-1127 https://doi.org/10.1056/NEJMra1001683
  2. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001;94:153-156 https://doi.org/10.1002/ijc.1440
  3. Trevisani F, Cantarini MC, Wands JR, Bernardi M. Recent advances in the natural history of hepatocellular carcinoma. Carcinogenesis 2008;29:1299-1305 https://doi.org/10.1093/carcin/bgn113
  4. Bruix J, Llovet JM. Major achievements in hepatocellular carcinoma. Lancet 2009;373:614-616 https://doi.org/10.1016/S0140-6736(09)60381-0
  5. Coleman WB. Mechanisms of human hepatocarcinogenesis. Curr Mol Med 2003;3:573-588 https://doi.org/10.2174/1566524033479546
  6. Ueda K, Matsui O, Kawamori Y, Nakanuma Y, Kadoya M, Yoshikawa J, et al. Hypervascular hepatocellular carcinoma: evaluation of hemodynamics with dynamic CT during hepatic arteriography. Radiology 1998;206:161-166 https://doi.org/10.1148/radiology.206.1.9423667
  7. Levy I, Greig PD, Gallinger S, Langer B, Sherman M. Resection of hepatocellular carcinoma without preoperative tumor biopsy. Ann Surg 2001;234:206-209 https://doi.org/10.1097/00000658-200108000-00010
  8. Torzilli G, Minagawa M, Takayama T, Inoue K, Hui AM, Kubota K, et al. Accurate preoperative evaluation of liver mass lesions without fine-needle biopsy. Hepatology 1999;30:889-893 https://doi.org/10.1002/hep.510300411
  9. Bruix J, Sherman M; American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology 2011;53:1020-1022 https://doi.org/10.1002/hep.24199
  10. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421-430 https://doi.org/10.1016/S0168-8278(01)00130-1
  11. Wald C, Russo MW, Heimbach JK, Hussain HK, Pomfret EA, Bruix J. New OPTN/UNOS policy for liver transplant allocation: standardization of liver imaging, diagnosis, classification, and reporting of hepatocellular carcinoma. Radiology 2013;266:376-382 https://doi.org/10.1148/radiol.12121698
  12. American College of Radiology. Liver imaging reporting and data system (LI-RADS). American College of Radiology. Web site. http://www.acr.org/Quality-Safety/Resources/LIRADS. Published May 25, 2014. Accessed August 1, 2015
  13. Kudo M, Matsui O, Izumi N, Iijima H, Kadoya M, Imai Y, et al. JSH consensus-based clinical practice guidelines for the management of hepatocellular carcinoma: 2014 update by the Liver Cancer Study Group of Japan. Liver Cancer 2014;3:458-468 https://doi.org/10.1159/000343875
  14. Omata M, Kanda T, Yu ML, Yokosuka O, Lim SG, Jafri W, et al. APASL consensus statements and management algorithms for hepatitis C virus infection. Hepatol Int 2012;6:409-435 https://doi.org/10.1007/s12072-012-9342-y
  15. European Association For The Study Of The Liver; European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012;56:908-943 https://doi.org/10.1016/j.jhep.2011.12.001
  16. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology 2014;272:635-654 https://doi.org/10.1148/radiol.14132361
  17. Lee JM, Yoon JH, Kim KW. Diagnosis of hepatocellular carcinoma: newer radiological tools. Semin Oncol 2012;39:399-409 https://doi.org/10.1053/j.seminoncol.2012.05.010
  18. Park MJ, Kim YK, Lee MW, Lee WJ, Kim YS, Kim SH, et al. Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology 2012;264:761-770 https://doi.org/10.1148/radiol.12112517
  19. Xu PJ, Yan FH, Wang JH, Lin J, Ji Y. Added value of breathhold diffusion-weighted MRI in detection of small hepatocellular carcinoma lesions compared with dynamic contrast-enhanced MRI alone using receiver operating characteristic curve analysis. J Magn Reson Imaging 2009;29:341-349 https://doi.org/10.1002/jmri.21650
  20. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology 2014;273:30-50 https://doi.org/10.1148/radiol.14132362
  21. Kitao A, Matsui O, Yoneda N, Kozaka K, Shinmura R, Koda W, et al. The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: correlation with gadoxetic acid enhanced MR imaging. Eur Radiol 2011;21:2056-2066 https://doi.org/10.1007/s00330-011-2165-8
  22. Kogita S, Imai Y, Okada M, Kim T, Onishi H, Takamura M, et al. Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol 2010;20:2405-2413 https://doi.org/10.1007/s00330-010-1812-9
  23. Kudo M, Matsui O, Izumi N, Iijima H, Kadoya M, Imai Y; Liver Cancer Study Group of Japan. Surveillance and diagnostic algorithm for hepatocellular carcinoma proposed by the Liver Cancer Study Group of Japan: 2014 update. Oncology 2014;87 Suppl 1:7-21
  24. Lee JM, Park JW, Choi BI. 2014 KLCSG-NCC Korea Practice Guidelines for the management of hepatocellular carcinoma: HCC diagnostic algorithm. Dig Dis 2014;32:764-777 https://doi.org/10.1159/000368020
  25. Korean Liver Cancer Study Group (KLCSG); National Cancer Center, Korea (NCC). 2014 Korean Liver Cancer Study Group-National Cancer Center Korea practice guideline for the management of hepatocellular carcinoma. Korean J Radiol 2015;16:465-522 https://doi.org/10.3348/kjr.2015.16.3.465
  26. Yamamoto A, Ito K, Tamada T, Higaki A, Kanki A, Sato T, et al. Newly developed hypervascular hepatocellular carcinoma during follow-up periods in patients with chronic liver disease: observation in serial gadoxetic acid-enhanced MRI. AJR Am J Roentgenol 2013;200:1254-1260 https://doi.org/10.2214/AJR.12.9136
  27. Yoon JH, Lee JM, Yang HK, Lee KB, Jang JJ, Han JK, et al. Non-hypervascular hypointense nodules ${\geq}$ 1 cm on the hepatobiliary phase of gadoxetic acid-enhanced magnetic resonance imaging in cirrhotic livers. Dig Dis 2014;32:678-689 https://doi.org/10.1159/000368000
  28. Takayama Y, Nishie A, Nakayama T, Asayama Y, Ishigami K, Kakihara D, et al. Hypovascular hepatic nodule showing hypointensity in the hepatobiliary phase of gadoxetic acid-enhanced MRI in patients with chronic liver disease: prediction of malignant transformation. Eur J Radiol 2012;81:3072-3078 https://doi.org/10.1016/j.ejrad.2012.05.008
  29. Joo I, Lee JM, Lee DH, Jeon JH, Han JK, Choi BI. Noninvasive diagnosis of hepatocellular carcinoma on gadoxetic acidenhanced MRI: can hypointensity on the hepatobiliary phase be used as an alternative to washout? Eur Radiol 2015;25:2859-2868 https://doi.org/10.1007/s00330-015-3686-3
  30. Takechi M, Tsuda T, Yoshioka S, Murata S, Tanaka H, Hirooka M, et al. Risk of hypervascularization in small hypovascular hepatic nodules showing hypointense in the hepatobiliary phase of gadoxetic acid-enhanced MRI in patients with chronic liver disease. Jpn J Radiol 2012;30:743-751 https://doi.org/10.1007/s11604-012-0120-5
  31. Lee DH, Lee JM, Baek JH, Shin CI, Han JK, Choi BI. Diagnostic performance of gadoxetic acid-enhanced liver MR imaging in the detection of HCCs and allocation of transplant recipients on the basis of the Milan criteria and UNOS guidelines: correlation with histopathologic findings. Radiology 2015;274:149-160 https://doi.org/10.1148/radiol.14140141
  32. Lee JM, Trevisani F, Vilgrain V, Wald C. Imaging diagnosis and staging of hepatocellular carcinoma. Liver Transpl 2011;17 Suppl 2:S34-S43
  33. Rimola J, Forner A, Reig M, Vilana R, de Lope CR, Ayuso C, et al. Cholangiocarcinoma in cirrhosis: absence of contrast washout in delayed phases by magnetic resonance imaging avoids misdiagnosis of hepatocellular carcinoma. Hepatology 2009;50:791-798 https://doi.org/10.1002/hep.23071
  34. Kim AY, Lee MW, Rhim H, Cha DI, Choi D, Kim YS, et al. Pretreatment evaluation with contrast-enhanced ultrasonography for percutaneous radiofrequency ablation of hepatocellular carcinomas with poor conspicuity on conventional ultrasonography. Korean J Radiol 2013;14:754-763 https://doi.org/10.3348/kjr.2013.14.5.754
  35. Kim SH, Kim SH, Lee J, Kim MJ, Jeon YH, Park Y, et al. Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. AJR Am J Roentgenol 2009;192:1675-1681 https://doi.org/10.2214/AJR.08.1262
  36. Sun HY, Lee JM, Shin CI, Lee DH, Moon SK, Kim KW, et al. Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (< or =2 cm in diameter) from arterial enhancing pseudolesions: special emphasis on hepatobiliary phase imaging. Invest Radiol 2010;45:96-103 https://doi.org/10.1097/RLI.0b013e3181c5faf7
  37. Park G, Kim YK, Kim CS, Yu HC, Hwang SB. Diagnostic efficacy of gadoxetic acid-enhanced MRI in the detection of hepatocellular carcinomas: comparison with gadopentetate dimeglumine. Br J Radiol 2010;83:1010-1016 https://doi.org/10.1259/bjr/66686028
  38. Hope TA, Fowler KJ, Sirlin CB, Costa EA, Yee J, Yeh BM, et al. Hepatobiliary agents and their role in LI-RADS. Abdom Imaging 2015;40:613-625 https://doi.org/10.1007/s00261-014-0227-5
  39. Shoreibah MG, Bloomer JR, McGuire BM, Massoud OI. Surveillance for hepatocellular carcinoma: evidence, guidelines and utilization. Am J Med Sci 2014;347:415-419 https://doi.org/10.1097/MAJ.0000000000000200
  40. Beasley RP, Hwang LY, Lin CC, Chien CS. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet 1981;2:1129-1133
  41. Bagnardi V, Blangiardo M, La Vecchia C, Corrao G. A metaanalysis of alcohol drinking and cancer risk. Br J Cancer 2001;85:1700-1705 https://doi.org/10.1054/bjoc.2001.2140
  42. Bellentani S, Saccoccio G, Costa G, Tiribelli C, Manenti F, Sodde M, et al. Drinking habits as cofactors of risk for alcohol induced liver damage. The Dionysos Study Group. Gut 1997;41:845-850 https://doi.org/10.1136/gut.41.6.845
  43. Seitz HK, Stickel F. Molecular mechanisms of alcohol-mediated carcinogenesis. Nat Rev Cancer 2007;7:599-612 https://doi.org/10.1038/nrc2191
  44. Vilgrain V, Rautou PE, Paradis V, Ronot M. Benign and malignant hepatocellular lesions in patients with vascular liver disease. Clin Liver Dis (Hoboken) 2014;3:122-125 https://doi.org/10.1002/cld.338
  45. Brancatelli G, Federle MP, Grazioli L, Golfieri R, Lencioni R. Benign regenerative nodules in Budd-Chiari syndrome and other vascular disorders of the liver: radiologic-pathologic and clinical correlation. Radiographics 2002;22:847-862 https://doi.org/10.1148/radiographics.22.4.g02jl17847
  46. Choi JY, Lee HC, Yim JH, Shim JH, Lim YS, Shin YM, et al. Focal nodular hyperplasia or focal nodular hyperplasialike lesions of the liver: a special emphasis on diagnosis. J Gastroenterol Hepatol 2011;26:1004-1009 https://doi.org/10.1111/j.1440-1746.2011.06659.x
  47. Nakashima O, Kurogi M, Yamaguchi R, Miyaaki H, Fujimoto M, Yano H, et al. Unique hypervascular nodules in alcoholic liver cirrhosis: identical to focal nodular hyperplasia-like nodules? J Hepatol 2004;41:992-998 https://doi.org/10.1016/j.jhep.2004.08.014
  48. Mitchell DG, Bruix J, Sherman M, Sirlin CB. LI-RADS (Liver Imaging Reporting and Data System): summary, discussion, and consensus of the LI-RADS Management Working Group and future directions. Hepatology 2015;61:1056-1065 https://doi.org/10.1002/hep.27304
  49. Serste T, Barrau V, Ozenne V, Vullierme MP, Bedossa P, Farges O, et al. Accuracy and disagreement of computed tomography and magnetic resonance imaging for the diagnosis of small hepatocellular carcinoma and dysplastic nodules: role of biopsy. Hepatology 2012;55:800-806 https://doi.org/10.1002/hep.24746
  50. Forner A, Vilana R, Ayuso C, Bianchi L, Sole M, Ayuso JR, et al. Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 2008;47:97-104
  51. Jang HJ, Kim TK, Khalili K, Yazdi L, Menezes R, Park SH, et al. Characterization of 1-to 2-cm liver nodules detected on hcc surveillance ultrasound according to the criteria of the American Association for the Study of Liver Disease: is quadriphasic CT necessary? AJR Am J Roentgenol 2013;201:314-321 https://doi.org/10.2214/AJR.12.9341
  52. Andersson KL, Salomon JA, Goldie SJ, Chung RT. Cost effectiveness of alternative surveillance strategies for hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol 2008;6:1418-1424 https://doi.org/10.1016/j.cgh.2008.08.005
  53. Singal A, Volk ML, Waljee A, Salgia R, Higgins P, Rogers MA, et al. Meta-analysis: surveillance with ultrasound for earlystage hepatocellular carcinoma in patients with cirrhosis. Aliment Pharmacol Ther 2009;30:37-47 https://doi.org/10.1111/j.1365-2036.2009.04014.x
  54. Kim S, Lim YS, Byun J, Won H, Lee S, Han S, et al. A prospective study to compare the diagnostic performance of gadoxetic acid-enhanced MRI and US for surveillance of HCC in high risk patients with liver cirrhosis. 21st Annual conference of European Congress of Radiology; 2015 March 4-8; Vienna
  55. 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 https://doi.org/10.1016/j.cgh.2010.09.017
  56. Kim PN, Choi D, Rhim H, Rha SE, Hong HP, Lee J, et al. Planning ultrasound for percutaneous radiofrequency ablation to treat small (${\leq}$ 3 cm) hepatocellular carcinomas detected on computed tomography or magnetic resonance imaging: a multicenter prospective study to assess factors affecting ultrasound visibility. J Vasc Interv Radiol 2012;23:627-634 https://doi.org/10.1016/j.jvir.2011.12.026
  57. Rhim H, Lee MH, Kim YS, Choi D, Lee WJ, Lim HK. Planning sonography to assess the feasibility of percutaneous radiofrequency ablation of hepatocellular carcinomas. AJR Am J Roentgenol 2008;190:1324-1330 https://doi.org/10.2214/AJR.07.2970
  58. Sarkar M, Stewart S, Yu A, Chen MS, Nguyen TT, Khalili M. Hepatocellular carcinoma screening practices and impact on survival among hepatitis B-infected Asian Americans. J Viral Hepat 2012;19:594-600 https://doi.org/10.1111/j.1365-2893.2011.01577.x
  59. Lee YJ, Lee JM, Lee JS, Lee HY, Park BH, Kim YH, et al. Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology 2015;275:97-109 https://doi.org/10.1148/radiol.14140690
  60. Hamm B, Staks T, Muhler A, Bollow M, Taupitz M, Frenzel T, et al. Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: safety, pharmacokinetics, and MR imaging. Radiology 1995;195:785-792 https://doi.org/10.1148/radiology.195.3.7754011
  61. Filippone A, Blakeborough A, Breuer J, Grazioli L, Gschwend S, Hammerstingl R, et al. Enhancement of liver parenchyma after injection of hepatocyte-specific MRI contrast media: a comparison of gadoxetic acid and gadobenate dimeglumine. J Magn Reson Imaging 2010;31:356-364 https://doi.org/10.1002/jmri.22054
  62. Kim HD, Lim YS, Han S, An J, Kim GA, Kim SY, et al. Evaluation of early-stage hepatocellular carcinoma by magnetic resonance imaging with gadoxetic acid detects additional lesions and increases overall survival. Gastroenterology 2015;148:1371-1382 https://doi.org/10.1053/j.gastro.2015.02.051
  63. Reimer P, Rummeny EJ, Shamsi K, Balzer T, Daldrup HE, Tombach B, et al. Phase II clinical evaluation of Gd-EOBDTPA: dose, safety aspects, and pulse sequence. Radiology 1996;199:177-183 https://doi.org/10.1148/radiology.199.1.8633143
  64. 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 https://doi.org/10.1148/radiol.12120826
  65. Pietryga JA, Burke LM, Marin D, Jaffe TA, Bashir MR. Respiratory motion artifact affecting hepatic arterial phase imaging with gadoxetate disodium: examination recovery with a multiple arterial phase acquisition. Radiology 2014;271:426-434 https://doi.org/10.1148/radiol.13131988
  66. Golfieri R, Grazioli L, Orlando E, Dormi A, Lucidi V, Corcioni B, et al. Which is the best MRI marker of malignancy for atypical cirrhotic nodules: hypointensity in hepatobiliary phase alone or combined with other features? Classification after Gd-EOBDTPA administration. J Magn Reson Imaging 2012;36:648-657 https://doi.org/10.1002/jmri.23685
  67. Akai H, Matsuda I, Kiryu S, Tajima T, Takao H, Watanabe Y, et al. Fate of hypointense lesions on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Eur J Radiol 2012;81:2973-2977 https://doi.org/10.1016/j.ejrad.2012.01.007
  68. Motosugi U. Hypovascular hypointense nodules on hepatocyte phase gadoxetic acid-enhanced MR images: too early or too progressed to determine hypervascularity. Radiology 2013;267:317-318
  69. Ichikawa S, Ichikawa T, Motosugi U, Sano K, Morisaka H, Enomoto N, et al. Presence of a hypovascular hepatic nodule showing hypointensity on hepatocyte-phase image is a risk factor for hypervascular hepatocellular carcinoma. J Magn Reson Imaging 2014;39:293-297 https://doi.org/10.1002/jmri.24164
  70. 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 https://doi.org/10.1148/radiol.12112649
  71. Lee DH, Lee JM, Lee JY, Kim SH, Kim JH, Yoon JH, et al. Nonhypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol 2015;62:1122-1130
  72. Toyoda H, Kumada T, Tada T, Sone Y, Maeda A, Kaneoka Y. Non-hypervascular hypointense nodules on Gd-EOB-DTPA-enhanced MRI as a predictor of outcomes for early-stage HCC. Hepatol Int 2015;9:84-92 https://doi.org/10.1007/s12072-014-9553-5
  73. Hwang J, Kim YK, Jeong WK, Choi D, Rhim H, Lee WJ. Nonhypervascular Hypointense Nodules at Gadoxetic Acidenhanced MR Imaging in Chronic Liver Disease: Diffusionweighted Imaging for Characterization. Radiology 2015;276:137-146 https://doi.org/10.1148/radiol.15141350
  74. Xu PJ, Yan FH, Wang JH, Shan Y, Ji Y, Chen CZ. Contribution of diffusion-weighted magnetic resonance imaging in the characterization of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver. J Comput Assist Tomogr 2010;34:506-512 https://doi.org/10.1097/RCT.0b013e3181da3671
  75. Hyodo T, Murakami T, Imai Y, Okada M, Hori M, Kagawa Y, et al. Hypovascular nodules in patients with chronic liver disease: risk factors for development of hypervascular hepatocellular carcinoma. Radiology 2013;266:480-490 https://doi.org/10.1148/radiol.12112677
  76. Di Pietropaolo M, Briani C, Federici GF, Marignani M, Begini P, Delle Fave G, et al. Comparison of diffusion-weighted imaging and gadoxetic acid-enhanced MR images in the evaluation of hepatocellular carcinoma and hypovascular hepatocellular nodules. Clin Imaging 2015;39:468-475 https://doi.org/10.1016/j.clinimag.2014.12.020
  77. Krinsky GA, Lee VS, Theise ND, Weinreb JC, Morgan GR, Diflo T, et al. Transplantation for hepatocellular carcinoma and cirrhosis: sensitivity of magnetic resonance imaging. Liver Transpl 2002;8:1156-1164 https://doi.org/10.1053/jlts.2002.35670
  78. Sangiovanni A, Manini MA, Iavarone M, Romeo R, Forzenigo LV, Fraquelli M, et al. The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut 2010;59:638-644 https://doi.org/10.1136/gut.2009.187286
  79. Taouli B, Koh DM. Diffusion-weighted MR imaging of the liver. Radiology 2010;254:47-66 https://doi.org/10.1148/radiol.09090021
  80. Kadoya M, Matsui O, Takashima T, Nonomura A. Hepatocellular carcinoma: correlation of MR imaging and histopathologic findings. Radiology 1992;183:819-825 https://doi.org/10.1148/radiology.183.3.1316622
  81. Matsui O, Kadoya M, Kameyama T, Yoshikawa J, Arai K, Gabata T, et al. Adenomatous hyperplastic nodules in the cirrhotic liver: differentiation from hepatocellular carcinoma with MR imaging. Radiology 1989;173:123-126 https://doi.org/10.1148/radiology.173.1.2550995
  82. Bashir MR, Gupta RT, Davenport MS, Allen BC, Jaffe TA, Ho LM, et al. Hepatocellular carcinoma in a North American population: does hepatobiliary MR imaging with Gd-EOB-DTPA improve sensitivity and confidence for diagnosis? J Magn Reson Imaging 2013;37:398-406 https://doi.org/10.1002/jmri.23818
  83. Le Moigne F, Durieux M, Bancel B, Boublay N, Boussel L, Ducerf C, et al. Impact of diffusion-weighted MR imaging on the characterization of small hepatocellular carcinoma in the cirrhotic liver. Magn Reson Imaging 2012;30:656-665 https://doi.org/10.1016/j.mri.2012.01.002
  84. Sandrasegaran K, Tahir B, Patel A, Ramaswamy R, Bertrand K, Akisik FM, et al. The usefulness of diffusion-weighted imaging in the characterization of liver lesions in patients with cirrhosis. Clin Radiol 2013;68:708-715 https://doi.org/10.1016/j.crad.2012.10.023
  85. Rimola J, Forner A, Tremosini S, Reig M, Vilana R, Bianchi L, et al. Non-invasive diagnosis of hepatocellular carcinoma ${\leq}$2 cm in cirrhosis. Diagnostic accuracy assessing fat, capsule and signal intensity at dynamic MRI. J Hepatol 2012;56:1317-1323 https://doi.org/10.1016/j.jhep.2012.01.004
  86. Darnell A, Forner A, Rimola J, Reig M, Garcia-Criado A, Ayuso C, et al. Liver Imaging Reporting and Data System with MR Imaging: Evaluation in Nodules 20 mm or Smaller Detected in Cirrhosis at Screening US. Radiology 2015;275:698-707 https://doi.org/10.1148/radiol.15141132
  87. Davenport MS, Khalatbari S, Liu PS, Maturen KE, Kaza RK, Wasnik AP, et al. Repeatability of diagnostic features and scoring systems for hepatocellular carcinoma by using MR imaging. Radiology 2014;272:132-142 https://doi.org/10.1148/radiol.14131963
  88. Song do S, Bae SH. Changes of guidelines diagnosing hepatocellular carcinoma during the last ten-year period. Clin Mol Hepatol 2012;18:258-267 https://doi.org/10.3350/cmh.2012.18.3.258
  89. Song KD, Kim SH, Lim HK, Jung SH, Sohn I, Kim HS. Subcentimeter hypervascular nodule with typical imaging findings of hepatocellular carcinoma in patients with history of hepatocellular carcinoma: natural course on serial gadoxetic acid-enhanced MRI and diffusion-weighted imaging. Eur Radiol 2015;25:2789-2796 https://doi.org/10.1007/s00330-015-3680-9
  90. Jang KM, Kim SH, Kim YK, Choi D. Imaging features of subcentimeter hypointense nodules on gadoxetic acidenhanced hepatobiliary phase MR imaging that progress to hypervascular hepatocellular carcinoma in patients with chronic liver disease. Acta Radiol 2015;56:526-535 https://doi.org/10.1177/0284185114534652
  91. Wang JH, Changchien CS, Hu TH, Lee CM, Kee KM, Lin CY, et al. The efficacy of treatment schedules according to Barcelona Clinic Liver Cancer staging for hepatocellular carcinoma - Survival analysis of 3892 patients. Eur J Cancer 2008;44:1000-1006 https://doi.org/10.1016/j.ejca.2008.02.018
  92. Tseng PL, Wang JH, Tung HD, Hung CH, Kee KM, Chen CH, et al. Optimal treatment increased survival of hepatocellular carcinoma patients detected with community-based screening. J Gastroenterol Hepatol 2010;25:1426-1434 https://doi.org/10.1111/j.1440-1746.2010.06285.x
  93. Farinati F, Sergio A, Baldan A, Giacomin A, Di Nolfo MA, Del Poggio P, et al. Early and very early hepatocellular carcinoma: when and how much do staging and choice of treatment really matter? A multi-center study. BMC Cancer 2009;9:33 https://doi.org/10.1186/1471-2407-9-33
  94. Silva MA, Hegab B, Hyde C, Guo B, Buckels JA, Mirza DF. Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut 2008;57:1592-1596 https://doi.org/10.1136/gut.2008.149062
  95. Khalili K, Kim TK, Jang HJ, Yazdi LK, Guindi M, Sherman M. Indeterminate 1-2-cm nodules found on hepatocellular carcinoma surveillance: biopsy for all, some, or none? Hepatology 2011;54:2048-2054 https://doi.org/10.1002/hep.24638
  96. Joo I, Kim H, Lee JM. Cancer stem cells in primary liver cancers: pathological concepts and imaging findings. Korean J Radiol 2015;16:50-68 https://doi.org/10.3348/kjr.2015.16.1.50
  97. Lu Q, Xue LY, Wang WP, Huang BJ, Li CX. Dynamic enhancement pattern of intrahepatic cholangiocarcinoma on contrast-enhanced ultrasound: the correlation with cirrhosis and tumor size. Abdom Imaging 2015;40:1558-1566 https://doi.org/10.1007/s00261-015-0379-y
  98. Fowler KJ, Sheybani A, Parker RA 3rd, Doherty S, M Brunt E, Chapman WC, et al. Combined hepatocellular and cholangiocarcinoma (biphenotypic) tumors: imaging features and diagnostic accuracy of contrast-enhanced CT and MRI. AJR Am J Roentgenol 2013;201:332-339 https://doi.org/10.2214/AJR.12.9488
  99. Ji J, Wang XW. Clinical implications of cancer stem cell biology in hepatocellular carcinoma. Semin Oncol 2012;39:461-472 https://doi.org/10.1053/j.seminoncol.2012.05.011

피인용 문헌

  1. Angled Cool-Tip Electrode for Radiofrequency Ablation of Small Superficial Subcapsular Tumors in the Liver: A Feasibility Study vol.17, pp.5, 2016, https://doi.org/10.3348/kjr.2016.17.5.742
  2. Gadoxetic acid-enhanced magnetic resonance imaging characteristics of hepatocellular carcinoma occurring in liver transplants vol.27, pp.8, 2016, https://doi.org/10.1007/s00330-016-4662-2
  3. Asia–Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update vol.11, pp.4, 2017, https://doi.org/10.1007/s12072-017-9799-9
  4. Diagnosis of Hepatocellular Carcinoma with Gadoxetic Acid-Enhanced MRI: 2016 Consensus Recommendations of the Korean Society of Abdominal Radiology vol.18, pp.3, 2016, https://doi.org/10.3348/kjr.2017.18.3.427
  5. Quantitative Measurement of Hepatic Fibrosis with Gadoxetic Acid-Enhanced Magnetic Resonance Imaging in Patients with Chronic Hepatitis B Infection: A Comparative Study on Aspartate Aminotransferase t vol.18, pp.3, 2017, https://doi.org/10.3348/kjr.2017.18.3.444
  6. T2 * Mapping from Multi-Echo Dixon Sequence on Gadoxetic Acid-Enhanced Magnetic Resonance Imaging for the Hepatic Fat Quantification: Can It Be Used for Hepatic Function Assessment? vol.18, pp.4, 2016, https://doi.org/10.3348/kjr.2017.18.4.682
  7. Liver imaging reporting and data system v2014 categorization of hepatocellular carcinoma on gadoxetic acid‐enhanced MRI: Comparison with multiphasic multidetector computed tomography vol.45, pp.3, 2016, https://doi.org/10.1002/jmri.25406
  8. Diagnostic value of contrast-enhanced ultrasound in hepatocellular carcinoma: a meta-analysis with evidence from 1998 to 2016 vol.8, pp.43, 2016, https://doi.org/10.18632/oncotarget.20049
  9. Non-invasive quantitative imaging of hepatocellular carcinoma growth in mice by micro-CT using liver-targeted iodinated nano-emulsions vol.7, pp.None, 2016, https://doi.org/10.1038/s41598-017-14270-7
  10. The Diagnostic Performance of Liver MRI without Intravenous Contrast for Detecting Hepatocellular Carcinoma: A Case-Controlled Feasibility Study vol.19, pp.4, 2018, https://doi.org/10.3348/kjr.2018.19.4.568
  11. Intra-individual comparison of hepatocellular carcinoma imaging features on contrast-enhanced computed tomography, gadopentetate dimeglumine-enhanced MRI, and gadoxetic acid-enhanced MRI vol.59, pp.6, 2016, https://doi.org/10.1177/0284185117728534
  12. Noninvasive imaging of hepatocellular carcinoma: From diagnosis to prognosis vol.24, pp.22, 2016, https://doi.org/10.3748/wjg.v24.i22.2348
  13. Characteristics of contrast-enhanced ultrasound in distinguishing small (≤3 cm) hepatocellular carcinoma from intrahepatic cholangiocarcinoma vol.97, pp.41, 2018, https://doi.org/10.1097/md.0000000000012781
  14. A Glimpse on Trends and Characteristics of Recent Articles Published in the Korean Journal of Radiology vol.20, pp.12, 2019, https://doi.org/10.3348/kjr.2019.0928
  15. Identification of Arterial Hyperenhancement in CT and MRI in Patients with Hepatocellular Carcinoma: Value of Unenhanced Images vol.20, pp.2, 2016, https://doi.org/10.3348/kjr.2018.0339
  16. High Acceleration Three-Dimensional T1-Weighted Dual Echo Dixon Hepatobiliary Phase Imaging Using Compressed Sensing-Sensitivity Encoding: Comparison of Image Quality and Solid Lesion Detectability wi vol.20, pp.3, 2016, https://doi.org/10.3348/kjr.2018.0310
  17. Hepatocellular Carcinoma: Current Imaging Modalities for Diagnosis and Prognosis vol.64, pp.4, 2019, https://doi.org/10.1007/s10620-019-05547-0
  18. Assessment of Treatment Efficacy Immediately After Combined Therapy of Ultrasound-Guided Radiofrequency Ablation and Conventional Transcatheter Arterial Chemoembolization for Hepatocellular Carcinoma: vol.16, pp.2, 2016, https://doi.org/10.5812/iranjradiol.80926
  19. Emerging Role of Hepatobiliary Magnetic Resonance Contrast Media and Contrast-Enhanced Ultrasound for Noninvasive Diagnosis of Hepatocellular Carcinoma: Emphasis on Recent Updates in Major Guidelines vol.20, pp.6, 2016, https://doi.org/10.3348/kjr.2018.0450
  20. Atypical Appearance of Hepatocellular Carcinoma and Its Mimickers: How to Solve Challenging Cases Using Gadoxetic Acid-Enhanced Liver Magnetic Resonance Imaging vol.20, pp.7, 2016, https://doi.org/10.3348/kjr.2018.0636
  21. 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 hepat vol.30, pp.8, 2016, https://doi.org/10.1007/s00330-020-06754-4
  22. MRI Ancillary Features for LI-RADS Category 3 and 4 Observations: Improved Categorization to Indicate the Risk of Hepatic Malignancy vol.215, pp.6, 2020, https://doi.org/10.2214/ajr.20.22802
  23. Value of gadoxetic acid-enhanced MRI for microvascular invasion of small hepatocellular carcinoma: a retrospective study vol.21, pp.1, 2016, https://doi.org/10.1186/s12880-021-00572-w