Abstract
Contrast-enhanced ultrasound (CEUS) using microbubble contrast agents has expanded the role of US in the diagnosis of liver nodules in high risk patients for hepatocellular carcinoma (HCC). HCC is typically characterized by arterial hypervascularity and later washout (negative enhancement). Washout in the portal phase is often not obvious until late (>90 s). Benign nodules such as regenerative nodules or dysplastic nodules are usually isoechoic or slightly hypoechoic in the arterial and portal venous phases. However, there are occasional cases with overlap of imaging features between benign and malignant nodules, including hypovascular HCC and hypervascular HCC without washout. CEUS is helpful to characterize potential mimickers of HCC on imaging such as nontumorous arterioportal shunt or hemangioma. CEUS is also useful for a guidance of percutaneous local therapy of HCC and post-procedure monitoring of therapeutic response. CEUS can be effectively used in the diagnostic algorithm of small (1–2 cm) newly detected nodules during HCC surveillance.
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Kim TK, Jang HJ, Wilson SR (2005) Imaging diagnosis of hepatocellular carcinoma with differentiation from other pathology. Clin Liver Dis 9:253–279
Colombo M (2009) Screening and diagnosis of hepatocellular carcinoma. Liver Int 29 Suppl 1:143–147
Ren FY, Piao XX, Jin AL (2006) Efficacy of ultrasonography and alpha-fetoprotein on early detection of hepatocellular carcinoma. World J Gastroenterol 12:4656–4659
Sherman M (2001) Surveillance for hepatocellular carcinoma. Semin Oncol 28:450–459
Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236
Matsui O (2005) Detection and characterization of hepatocellular carcinoma by imaging. Clin Gastroenterol Hepatol 3:S136–S140
Choi BI, Kim TK, Han JK, et al. (2000) Vascularity of hepatocellular carcinoma: assessment with contrast-enhanced second-harmonic versus conventional power Doppler US. Radiology 214:381–386
Dill-Macky MJ, Burns PN, Khalili K, Wilson SR (2002) Focal hepatic masses: enhancement patterns with SH U 508A and pulse-inversion US. Radiology 222:95–102
Jang HJ, Kim TK, Wilson SR (2006) Imaging of malignant liver masses: characterization and detection. Ultrasound Q 22:19–29
Kim TK, Choi BI, Han JK, et al. (2000) Hepatic tumors: contrast agent-enhancement patterns with pulse-inversion harmonic US. Radiology 216:411–417
Kim AY, Choi BI, Kim TK, et al. (1998) Hepatocellular carcinoma: power Doppler US with a contrast agent—preliminary results. Radiology 209:135–140
Nicolau C, Catala V, Vilana R, et al. (2004) Evaluation of hepatocellular carcinoma using SonoVue, a second generation ultrasound contrast agent: correlation with cellular differentiation. Eur Radiol 14:1092–1099
Quaia E, Calliada F, Bertolotto M, et al. (2004) Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: diagnostic performance and confidence. Radiology 232:420–430
Wilson SR, Burns PN (2006) An algorithm for the diagnosis of focal liver masses using microbubble contrast-enhanced pulse-inversion sonography. AJR 186:1401–1412
Kim TK, Kim AY, Choi BI (2002) Hepatocellular carcinoma: harmonic ultrasound and contrast agent. Abdom Imaging 27:129–138
Jang HJ, Kim TK, Wilson SR (2008) Small nodules (1–2 cm) in liver cirrhosis: characterization with contrast-enhanced ultrasound. Eur J Radiol 190: 691–695
Jang HJ, Kim TK, Burns PN, Wilson SR (2007) Enhancement patterns of hepatocellular carcinoma at contrast-enhanced US: comparison with histologic differentiation. Radiology 244:898–906
Jang HJ, Yu H, Kim TK (2009) Contrast-enhanced ultrasound in the detection and characterization of liver tumors. Cancer Imaging 9:96–103
Jang HJ, Yu H, Kim TK (2009) Imaging of focal liver lesions. Semin Roentgenol 44:266–282
Wilson SR, Jang HJ, Kim TK, Burns PN (2007) Diagnosis of focal liver masses on ultrasonography: comparison of unenhanced and contrast-enhanced scans. J Ultrasound Med 26:775–787 (quiz 788-790)
Forner A, Vilana R, Ayuso C, et al. (2008) Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 47:97–104
Burns PN, Wilson SR (2006) Microbubble contrast for radiological imaging: 1. Principles. Ultrasound Q 22:5–13
Brannigan M, Burns PN, Wilson SR (2004) Blood flow patterns in focal liver lesions at microbubble-enhanced US. Radiographics 24:921–935
Wilson SR, Kim TK, Jang HJ, Burns PN (2007) Enhancement patterns of focal liver masses: discordance between contrast-enhanced sonography and contrast-enhanced CT and MRI. AJR 189:W7–W12
Piscaglia F, Bolondi L (2006) The safety of Sonovue in abdominal applications: retrospective analysis of 23188 investigations. Ultrasou Med Biol 32:1369–1375
Wilson SR, Jang HJ, Kim TK, et al. (2008) Real-time temporal maximum-intensity-projection imaging of hepatic lesions with contrast-enhanced sonography. AJR 190:691–695
Hudson JM, Karshafian R, Burns PN (2009) Quantification of flow using ultrasound and microbubbles: a disruption replenishment model based on physical principles. Ultrasou Med Biol 35:2007–2020
Matsui O, Kadoya M, Kameyama T, et al. (1991) Benign and malignant nodules in cirrhotic livers: distinction based on blood supply. Radiology 178:493–497
Hayashi M, Matsui O, Ueda K, et al. (1999) Correlation between the blood supply and grade of malignancy of hepatocellular nodules associated with liver cirrhosis: evaluation by CT during intraarterial injection of contrast medium. AJR 172:969–976
Murphy-Lavallee J, Jang HJ, Kim TK, Burns PN, Wilson SR (2007) Are metastases really hypovascular in the arterial phase? The perspective based on contrast-enhanced ultrasonography. J Ultrasound Med 26:1545–1556
Bhayana D, Kim TK, Jang HJ, Burns PN, Wilson SR (2010) Hypervascular liver masses on contrast-enhanced ultrasound: the importance of washout. AJR 194:977–983
Lee KH, Choi BI, Han JK, et al. (2000) Nodular hepatocellular carcinoma: variation of tumor conspicuity on single-level dynamic scan and optimization of fixed delay times for two-phase helical CT. J Comput Assist Tomogr 24:212–218
Rossi S, Ghittoni G, Ravetta V, et al. (2008) Contrast-enhanced ultrasonography and spiral computed tomography in the detection and characterization of portal vein thrombosis complicating hepatocellular carcinoma. Eur Radiol 18:1749–1756
Lim JH, Cho JM, Kim EY, Park CK (2000) Dysplastic nodules in liver cirrhosis: evaluation of hemodynamics with CT during arterial portography and CT hepatic arteriography. Radiology 214:869–874
Kim TK, Choi BI, Han JK, et al. (1998) Nontumorous arterioportal shunt mimicking hypervascular tumor in cirrhotic liver: two-phase spiral CT findings. Radiology 208:597–603
Yu JS, Kim KW, Jeong MG, Lee JT, Yoo HS (2000) Nontumorous hepatic arterial-portal venous shunts: MR imaging findings. Radiology 217:750–756
Byun JH, Kim TK, Lee CW, et al. (2004) Arterioportal shunt: prevalence in small hemangiomas versus that in hepatocellular carcinomas 3 cm or smaller at two-phase helical CT. Radiology 232:354–360
Kim KW, Kim TK, Han JK, et al. (2001) Hepatic hemangiomas with arterioportal shunt: findings at two-phase CT. Radiology 219:707–711
Kim JH, Kim TK, Kim BS, et al. (2002) Enhancement of hepatic hemangiomas with levovist on coded harmonic angiographic ultrasonography. J Ultrasound Med 21:141–148
Jang HJ, Kim TK, Lim HK, et al. (2003) Hepatic hemangioma: atypical appearances on CT, MR imaging, and sonography. AJR 180:135–141
Kim TK, Jang HJ, Wilson SR (2006) Benign liver masses: imaging with microbubble contrast agents. Ultrasound Q 22:31–39
Meloni MF, Livraghi T, Filice C, et al. (2006) Radiofrequency ablation of liver tumors: the role of microbubble ultrasound contrast agents. Ultrasound Q 22:41–47
Leen E, Kumar S, Khan SA, et al. (2009) Contrast-enhanced 3D ultrasound in the radiofrequency ablation of liver tumors. World J Gastroenterol 15:289–299
Claudon M, Cosgrove D, Albrecht T, et al. (2008) Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS)—update 2008. Ultraschall Med 29:28–44
Solbiati L, Tonolini M, Cova L (2004) Monitoring RF ablation. Eur Radiol 14 Suppl 8:P34–P42
Dill-Macky MJ, Asch M, Burns P, Wilson S (2006) Radiofrequency ablation of hepatocellular carcinoma: predicting success using contrast-enhanced sonography. AJR 186:S287–S295
Yu H, Jang HJ, Kim TK, et al. (2010) Pseudoenhancement within the local ablation zone of hepatic tumors due to a nonlinear artifact on contrast-enhanced ultrasound. AJR 194:653–659
Kim HJ, Kim TK, Kim PN, et al. (2006) Assessment of the therapeutic response of hepatocellular carcinoma treated with transcatheter arterial chemoembolization: comparison of contrast-enhanced sonography and 3-phase computed tomography. J Ultrasound Med 25:477–486
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Kim, T.K., Lee, K.H., Khalili, K. et al. Hepatocellular nodules in liver cirrhosis: contrast-enhanced ultrasound. Abdom Imaging 36, 244–263 (2011). https://doi.org/10.1007/s00261-011-9686-0
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DOI: https://doi.org/10.1007/s00261-011-9686-0