Contrast-enhanced ultrasound features of hepatic angiomyolipoma:
                    comparison with AFP-negative and non-viral hepatocellular
                    carcinoma

Yafang Zhang; Zhi-xing Guo; Ying Liao; Yiwen Yu; Ruohan Guo; Xu Han; Lilong Lan; Jianhua Zhou

doi:10.1055/a-2318-6654

Ultrasound International Open, Table of Contents

CC BY-NC-ND 4.0 · Ultrasound Int Open 2025; 11: a23186654
DOI: 10.1055/a-2318-6654

Original Article

Contrast-enhanced ultrasound features of hepatic angiomyolipoma: comparison with AFP-negative and non-viral hepatocellular carcinoma

Authors

Yafang Zhang‡

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Zhi-xing Guo‡

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Ying Liao‡

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Yiwen Yu

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Ruohan Guo

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Xu Han

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Lilong Lan

²Department of Pathology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China
Jianhua Zhou

¹Department of Ultrasound, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China

Abstract

Purpose This study aimed to compare contrast-enhanced ultrasound (CEUS) features of hepatic angiomyolipoma (HAML) and challenging cases of HCC, mainly those with no hepatitis infection but also with a low level of AFP (non-viral AFP- HCC).

Materials and Methods The study included pathologically confirmed HAMLs and non-viral AFP- HCCs undergoing CEUS from 2012 to 2023. Sonovue (SV) CEUS and Sonazoid (SZ) CEUS characteristics of the two groups were compared.

Results The study included 50 HAMLs (24% on SZ-CEUS) and 88 non-viral AFP- HCCs (21.6% on SZ-CEUS). The CEUS characteristics on SZ-CEUS were similar to those on SV-CEUS to a certain extent. HAMLs more frequently displayed no washout and partial washout with partial no washout, so-called PWNW, in the late phase and post-vascular phase, whereas HCCs more commonly exhibited mild washout. In the post-vascular phase, all non-viral AFP- HCCs exhibited washout, thereby facilitating differentiation from no-washoutHAMLs, superior to SV-CEUS, where some non-viral AFP- HCCs still exhibited no washout in late phase that could not be distinguished from HAMLs. It is noteworthy that PWNW was exclusively found in nodules exhibiting hyper- and hypoechoic separation of the nodules, and hyper- and hypoechoic separation of HAMLs in the post-vascular phase on SZ-CEUS demonstrated PWNW more frequently compared to the late phase, which can potentially help distinguish nodules with hyper- and hypoechoic separation as either HAML or non-viral AFP- HCC. Conclusion: This study highlighted the usefulness of SV- and SZ-CEUS for distinguishing HAML and non-viral AFP- HCC and filled in existing gaps regarding the SZ-CEUS features of HAML.

Keywords

hepatic angiomyolipoma - hepatocellular carcinoma - contrast-enhanced ultrasound - Sonazoid

Bibliographical Record
Yafang Zhang, Zhi-xing Guo, Ying Liao, Yiwen Yu, Ruohan Guo, Xu Han, Lilong Lan, Jianhua Zhou. Contrast-enhanced ultrasound features of hepatic angiomyolipoma: comparison with AFP-negative and non-viral hepatocellular carcinoma. Ultrasound Int Open 2025; 11: a23186654.
DOI: 10.1055/a-2318-6654

Full Text

References

References
1 Tan Y, Xie XY, Li XJ. et al. Comparison of hepatic epithelioid angiomyolipoma and non-hepatitis B, non-hepatitis C hepatocellular carcinoma on contrast-enhanced ultrasound. Diagn Interv Imaging 2020; 101: 733-738
2 Yang X, Li A, Wu M. Hepatic angiomyolipoma: clinical, imaging and pathological features in 178 cases. Med Oncol 2013; 30: 416
3 Jung DH, Hwang S, Hong SM. et al. Clinico-pathological correlation of hepatic angiomyolipoma: a series of 23 resection cases. ANZ J Surg 2018; 88: E60-e65
4 Marrero JA, Kulik LM, Sirlin CB. 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
5 Liu Z, Jiang Y, Yuan H. et al. The trends in incidence of primary liver cancer caused by specific etiologies: Results from the Global Burden of Disease Study 2016 and implications for liver cancer prevention. J Hepatol 2019; 70: 674-683
6 Takeishi K, Maeda T, Shirabe K. et al. Clinicopathologic Features and Outcomes of Non-B, Non-C Hepatocellular Carcinoma After Hepatectomy. Ann Surg Oncol 2015; 22: S1116-S1124
7 Tateishi R, Uchino K, Fujiwara N. et al. A nationwide survey on non-B, non-C hepatocellular carcinoma in Japan: 2011-2015 update. J Gastroenterol 2019; 54: 367-376
8 Zhang Y, Li Q, Li L. et al. Diagnostic Performance of Modified Contrast-Enhanced Ultrasound Liver Imaging Reporting and Data System in Patients Without Risk Factors for Hepatocellular Carcinoma: Comparison With World Federation for Ultrasound in Medicine and Biology Guideline. Ultrasound Med Biol 2024; 50: 243-250
9 Dietrich CF, Nolsøe CP, Barr RG. et al. Guidelines and Good Clinical Practice Recommendations for Contrast-Enhanced Ultrasound (CEUS) in the Liver-Update 2020 WFUMB in Cooperation with EFSUMB, AFSUMB, AIUM, and FLAUS. Ultrasound Med Biol 2020; 46: 2579-2604
10 Barr RG, Huang P, Luo Y. et al. Contrast-enhanced ultrasound imaging of the liver: a review of the clinical evidence for SonoVue and Sonazoid. Abdom Radiol (NY) 2020; 45: 3779-3788
11 Wang Z, Xu HX, Xie XY. et al. Imaging features of hepatic angiomyolipomas on real-time contrast-enhanced ultrasound. Br J Radiol 2010; 83: 411-418
12 Li R, Tang CL, Zhang Y. et al. Diagnosis of Hepatic Angiomyolipoma by Combination of Baseline and Contrast-Enhanced Ultrasound--A Prospective Study in Non-Cirrhotic Patients. PLoS One 2015; 10: e0132290
13 Seow J, McGill M, Wang W. et al. Imaging hepatic angiomyolipomas: key features and avoiding errors. Clin Radiol 2020; 75: 88-99
14 Zou MH, Huang Q, Zou Q. et al. Clinical and Contrast-enhanced Ultrasound Characteristics of Epithelioid and Classic Hepatic Angiomyolipoma: Comparison With Alpha-fetoprotein-negative Hepatocellular Carcinoma. Ultrasound Med Biol 2021; 47: 446-453
15 Huang Z, Wu X, Li S. et al. Contrast-Enhanced Ultrasound Findings and Differential Diagnosis of Hepatic Epithelioid Angiomyolipoma Compared with Hepatocellular Carcinoma. Ultrasound Med Biol 2020; 46: 1403-1411
16 Endo K, Kuroda H, Kakisaka K. et al. Hepatic Angiomyolipoma Staining in the Post-vascular Phase of Contrast-enhanced Ultrasound Due to the Presence of Macrophages. Intern Med 2018; 57: 1247-1251
17 Huang Z, Xin JY, Li KY. Ultrasound contrast agent Sonazoid for the diagnosis of hepatic epithelioid angiomyolipoma: a case report. BMC Gastroenterol 2021; 21: 487
18 Li R, Tang CL, Cai P. et al. Comparison of CT and contrast-enhanced ultrasound findings in hepatic angiomyolipoma with pathological correlations. Abdom Radiol (NY) 2016; 41: 248-256
19 Tan Y, Xie X, Lin Y. et al. Hepatic epithelioid angiomyolipoma: clinical features and imaging findings of contrast-enhanced ultrasound and CT. Clin Radiol 2017; 72: 339.e331-339.e336
20 Xu PJ, Shan Y, Yan FH. et al. Epithelioid angiomyolipoma of the liver: cross-sectional imaging findings of 10 immunohistochemically-verified cases. World J Gastroenterol 2009; 15: 4576-4581
21 Meitner-Schellhaas B, Jesper D, Goertz RS. et al. Washout appearance of hepatocellular carcinomas using standardized contrast-enhanced ultrasound (CEUS) including an extended late phase observation - Real-world data from the prospective multicentre DEGUM study. Clin Hemorheol Microcirc 2023; 84: 413-424
22 Chen S, Qiu YJ, Zhang Q. et al. Impact of Hepatocellular Carcinoma Tumor Size on Sonazoid Contrast-Enhanced Ultrasound Enhancement Features. Ultrasound Med Biol 2024; 50: 39-46
23 Kong WT, Tang M, Qiu YD. et al. The differential enhancement pattern of contrast enhanced ultrasound and magnetic resonance imaging characteristics in hepatic angiomyolipoma: 7 case reports. Clin Hemorheol Microcirc 2019; 71: 17-26
24 Tsui WM, Colombari R, Portmann BC. et al. Hepatic angiomyolipoma: a clinicopathologic study of 30 cases and delineation of unusual morphologic variants. Am J Surg Pathol 1999; 23: 34-48
25 Tochio H, Tamaki E, Imai Y. et al. CD68-Positive Cells in Hepatic Angiomyolipoma. Oncology 2017; 92: 35-39
26 Jia J, Bai Y, Fu K. et al. Expression of allograft inflammatory factor-1 and CD68 in haemangioma: implication in the progression of haemangioma. Br J Dermatol 2008; 159: 811-819
27 Rimola J. Heterogeneity of Hepatocellular Carcinoma on Imaging. Semin Liver Dis 2020; 40: 61-69
28 Komiyama S, Okazaki H, Nakao S. et al. Diffuse fatty metamorphosis of a large, well-differentiated hepatocellular carcinoma originating in the normal liver: a case report and literature review. Clin J Gastroenterol 2015; 8: 345-350
29 Liu W, Wang J, Huang Q. et al. Comparison of MRI Features of Epithelioid Hepatic Angiomyolipoma and Hepatocellular Carcinoma: Imaging Data From Two Centers. Front Oncol 2018; 8: 600
30 Chang Z, Zhang JM, Ying JQ. et al. Characteristics and treatment strategy of hepatic angiomyolipoma: a series of 94 patients collected from four institutions. J Gastrointestin Liver Dis 2011; 20: 65-69