Hepatobiliary Imaging Pictorial Essay Kim et al. Sonography of Hepatic Steatosis Hepatobiliary Imaging Pictorial Essay Kyoung Won Kim 1 Min Ju Kim 2 Seung Soo Lee 1 Hyoung Jung Kim 3 Yong Moon Shin 1 Pyo-Nyun Kim 1 Moon-Gyu Lee 1 Kim KW, Kim MJ, Lee SS, et al. Keywords: Doppler study, fatty liver, liver neoplasms, sonography DOI:10.2214/JR.07.2863 Received July 12, 2007; accepted after revision October 10, 2007. 1 Department of Radiology, san Medical enter, University of Ulsan ollege of Medicine, 388-1, Pungnap 2-dong, Songpa-ku, Seoul 138-736, Korea. ddress correspondence to K. W. Kim (kimkw@amc.seoul.kr). 2 Department of Radiology, National ancer enter, Gyeonggi-do, Korea. 3 Department of Diagnostic Radiology, Kyung Hee University Hospital, Seoul, South Korea. JR 2008; 190:1018 1027 0361 803X/08/1904 1018 merican Roentgen Ray Society Sparing of Fatty Infiltration round Focal Hepatic Lesions in Patients with Hepatic Steatosis: Sonographic ppearance with T and MRI orrelation OJETIVE. The purposes of this study were to illustrate the sonographic features of focal hepatic lesions with peritumoral sparing of fatty infiltration in patients with hepatic steatosis, to correlate the sonographic findings with T and MRI findings, and to discuss the possible mechanisms. ONLUSION. Various focal hepatic lesions can accompany peritumoral sparing of fatty infiltration in patients with hepatic steatosis, and they can manifest with an atypical sonographic appearance. F ocal sparing of fatty infiltration frequently occurs around various hepatic space-occupying lesions in patients with hepatic steatosis [1]. Opposed-phase gradient-echo MRI is the best method for depicting peritumoral sparing of fatty infiltration under these circumstances [2 5]. t sonography, the sparing of infiltration can obscure the presence of focal hepatic lesions or at least modify the sonographic appearance, leading to diagnostic confusion. Sonography is the first-line radiologic investigation for patients with suspected liver lesions. It therefore is important for radiologists both to recognize peritumoral sparing of fatty infiltration so that it can be identified as a sign of adjacent focal lesions and to be familiar with the sonographic appearance of various focal hepatic lesions with peritumoral sparing of fatty infiltration. The purposes of this article are to illustrate the sonographic features of various focal hepatic lesions with peritumoral sparing of fatty infiltration in patients with hepatic steatosis, to correlate the features with the T and MRI findings, and to discuss the possible mechanisms of peritumoral sparing of fatty infiltration. Hepatic Hemangioma Peritumoral sparing of fatty infiltration frequently occurs around hepatic hemangiomas, appearing as a hyperattenuating rim on unenhanced T [6] and as a hyperintense peritumoral rim on chemical shift MRI [2, 3]. hen et al. [2] found that areas of peritumoral sparing of fatty infiltration around hemangiomas on chemical shift MRI were well correlated with those of temporal peritumoral enhancement during the arterial phase of dynamic contrast-enhanced studies. Dilution of portal blood flow by non-lipid-rich arterial blood through the arterioportal shunt is considered the cause of peritumoral sparing of fatty infiltration around hemangiomas [2, 7]. In patients with hepatic steatosis, peritumoral sparing of fatty infiltration can modify the sonographic appearance of hemangiomas. Given that hepatic steatosis causes an echopoor appearance of hemangiomas and that high-flow hemangiomas with arterioportal shunt are commonly seen as hypoechoic lesions, it is not surprising that hemangiomas with peritumoral sparing of fatty infiltration tend to have a hypoechoic appearance with or without a hyperechoic rim [8] (Fig. 1). In addition, these tumors are surrounded by geographic hypoechoic areas representing peritumoral sparing of fatty infiltration that are similar to the hyperattenuating areas on unenhanced T and to the hyperintense areas on opposed-phase gradient-echo MR images. In a previous study [9], we compared sonography and chemical shift MRI of patients with hepatic hemangioma. We found that among 40 hemangiomas with a hyper intense peritumoral rim on opposed-phase gradientecho MR that represented peritumoral sparing of fatty infiltration, a geographic peritumoral hypoechoic area was correspondingly 1018 JR:190, pril 2008
Sonography of Hepatic Steatosis seen in 27 (68%) of the tumors. lthough the results may indicate that sonography is less sensitive than chemical shift MRI in depicting this finding, it seems that the value of sonography may have been underestimated because it is operator-dependent. In other words, the peritumoral hypoechoic area might have been neglected if sonographers were unaware of the importance of this finding. olor Doppler sonography can depict intratumoral blood flow, large feeding arteries, and sometimes reversed blood flow in the portal branch parallel to the feeding arteries [8, 10] (Fig. 2). Hepatocellular arcinoma In contrast to the high frequency of arterioportal shunt in hepatic hemangioma [11], the shunt is rare in small hepatocellular carcinomas (Hs) [12]. Nevertheless, H also can accompany peritumoral sparing of fatty infiltration in hepatic steatosis. Matsui et al. [13] found corona-like enhancement of H on single-level dynamic T during hepatic arteriography, describing it as projecting into the surrounding liver while gradually spreading with a wedge-shaped configuration. Those authors proposed that this finding may represent direct venous drainage from tumor sinusoids into adjacent hepatic sinusoids. The area of corona-like enhancement is seen as a perfusion defect on T during arterial portography. Therefore, the decrease in regional portal flow may cause peritumoral sparing of fatty infiltration around an H [4]. In the case of larger tumors, the arterial perfusion in the hepatic parenchyma around the hypervascular H can increase owing to a siphoning effect while portal flow reciprocally decreases [14], causing peritumoral sparing of fatty infiltration. On sonography, a hypoechoic halo, a possible indicator of hepatic malignancy, may not be discernible around Hs with peritumoral sparing of fatty infiltration (Fig. 3). ecause the tumor may be believed to be larger than it actually is, targeting the periphery of the lesion during sonographically guided percutaneous biopsy may result in erroneous tissue sampling. In contrast to the descriptions of hemangioma, the sonographic literature in English has little information about the prevalence of peritumoral sparing of fatty infiltration around H. well-designed prospective study is warranted to determine the frequency of peritumoral sparing of fatty infiltration around Hs on sonography and to better describe the sonographic appearance of Hs with peritumoral sparing of fatty infiltration. olor Doppler sonography may show large feeding arteries and intratumoral flow, but corona-like enhancement and hemodynamic alteration around H are usually below the sensitivity limits of the examination. holangiocarcinoma holangiocarcinoma can accompany peritumoral sparing of fatty infiltration in patients with hepatic steatosis [1]. Obstruction of or a marked decrease in portal blood flow caused by tumor invasion with a reciprocal increase in arterial flow is considered the cause of peritumoral sparing of fatty infiltration. Obstruction of a large portal branch also can lead to hepatic parenchymal atrophy. On sonography, the area of peritumoral sparing of fatty infiltration is seen as a wedge-shaped peritumoral hypoechoic lesion in which the vertex points to the portal branch invaded by the tumor (Fig. 4). The extent of peritumoral sparing of fatty infiltration varies with the degree of portal compromise and arterial compensation. Metastatic Lesions Several factors can account for the decrease in portal flow to the hepatic parenchyma adjacent to metastatic lesions [5, 14] that causes peritumoral sparing of fatty infiltration in patients with hepatic steatosis (Figs. 5 and 6). First, portal branches proximal to the metastatic lesions can be narrowed or occluded by tumor emboli, invasion, or compression, there by blocking portal inflow. Second, expansively growing metastatic lesions can compress and flatten parenchymal structures, cause sinusoidal congestion, and decrease the portal flow around the tumors. Third, arterial perfusion of the hepatic parenchyma around hypervascular metastatic lesions increases because of a siphoning effect similar to that in Hs, and portal flow decreases reciprocally. It should be kept in mind that focal sparing in hepatic steatosis found on sonography can be a sign of the presence of an adjacent spaceoccupying lesion, although further studies are necessary to determine the prevalence of this finding around metastatic lesions. Therefore, focal sparing of hepatic steatosis should not be overlooked during sonographic examinations of patients with underlying malignant tumors. In other words, whether focal fat sparing is associated with a metastatic tumor should be carefully determined whenever fat sparing is encountered, because the tumor itself can be small and obscured by peritumoral sparing of fatty infiltration. Equivocal cases should be referred for MRI that includes chemical shift imaging, which is considered the technique of choice in these circumstances [5]. t sonographically guided percutaneous biopsy, the site of tissue sampling should be carefully determined so as to increase the yield of the biopsy. Nonneoplastic Lesions It seems obvious that peritumoral sparing of fatty infiltration can occur around hepatic abscesses in patients with hepatic steatosis, considering that abscesses commonly accompany transient hepatic attenuation differences on T owing to a decrease in portal flow with pylephlebitis and reciprocal arterial hyperperfusion [15]. On sonography, however, although the straight border between the parenchyma and the lesion may suggest the presence of associated peritumoral sparing of fatty infiltration, it is difficult to discriminate the peritumoral sparing of fatty infiltration and the peripheral part of the abscess composed of inflammatory and edematous parenchyma (Figs. 7 and 8). In rare instances hepatic cysts can accompany peritumoral sparing of fatty infiltration. We believe that compression of the hepatic parenchyma surrounding a cyst is the most likely cause of peritumoral sparing of fatty infiltration. Peritumoral sparing of fatty infiltration can modify the sonographic appearance of an uncomplicated hepatic cyst, which can be misinterpreted as a complicated cyst or a cystic tumor (Fig. 9). onclusion Various focal hepatic lesions can accompany peritumoral sparing of fatty infiltration in patients with hepatic steatosis, and they can manifest with an atypical sonographic appearance. It is important to recognize the possibility of peritumoral sparing of fatty infiltration on sonography, not only to decrease diagnostic confusion but also to increase the yield of sonographically guided percutaneous biopsy. References 1. Grossholz M, Terrier F, Rubbia L, et al. Focal sparing in the fatty liver as a sign of an adjacent space-occupying lesion. JR 1998; 171:1391 1395 2. hen R, Li S, Lii JM, hen WT, Tu HY. Peritumoral fat-spared area is well correlated with the presence of temporal peritumoral enhancement in hepatic hemangioma in fatty liver. J Magn Reson Imaging 2005; 22:86 91 JR:190, pril 2008 1019
Kim et al. 3. Xu H, Jiang D, Yang L, Xiong Y, Yang F, Kong X. The value of in-phase and opposed-phase T1- weighted breath-hold FLSH sequences for hepatic imaging. J Tongji Med Univ 2000; 20: 290 293 4. Gabata T, Kadoya M, Matsui O, et al. Peritumoral spared area in fatty liver: correlation between opposed-phase gradient-echo MR imaging and T arteriography. bdom Imaging 2001; 26:384 389 5. hung JJ, Kim MJ, Kim JH, Lee JT, Yoo HS. Fat sparing of surrounding liver from metastasis in patients with fatty liver: MR imaging with histopathologic correlation. JR 2003; 180:1347 1350 6. Itai Y, Maeda M, Echigo J, et al. Hyperattenuating rim on noncontrast T of the liver: probable peritumoral sparing of fatty infiltration. lin Radiol 1996; 51:406 410 7. rita T, Matsunaga N, Honma Y, Nishikawa E, Nagaoka S. Focally spared area of fatty livers caused by arteriportal shunt. J omput ssist Tomogr 1996; 20:360 362 8. Kim KW, Kim Y, Kim TK, et al. Hepatic hemangiomas with arterioportal shunt: sonographic appearances with T and MRI correlation. JR 2006; 187:1010;[web]W406 W414 9. Kim MJ, Kim KW, Won HJ, et al. Hepatic hemangiomas with peritumoral sparing of fatty infiltration in hepatic steatosis: findings on contrast-enhanced MR imaging and on sonography. J Korean Radiol Soc 2006; 55:571 577 10. Naganuma H, Ishida H, Konno K, et al. Hepatic hemangioma with arterioportal shunts. bdom Imaging 1999; 24:42 46 11. Kim KW, Kim TK, Han JK, Kim Y, Lee HJ, hoi I. Hepatic hemangiomas with arterioportal shunt: findings at two-phase T. Radiology 2001; 219:707 711 12. yun JH, Kim TK, Lee W, et al. rterioportal shunt: prevalence in small hemangiomas versus that in hepatocellular carcinomas 3 cm or smaller at two-phase helical T. Radiology 2004; 232:354 360 13. Matsui O, Ueda K, Kobayashi S, et al. Intra- and perinodular hemodynamics of hepatocellular carcinoma: T observation during intra-arterial contrast injection. bdom Imaging 2002; 27: 147 156 14. Kanematsu M, Hoshi H, Yamada T, et al. Overestimating the size of hepatic malignancy on helical T during arterial portography: equilibrium phase T and pathology. J omput ssist Tomogr 1997; 21:713 719 15. Gabata T, Kadoya M, Matsui O, et al. Dynamic T of hepatic abscesses: significance of transient segmental enhancement. JR 2001; 176:675 679 Fig. 1 50-year-old woman with hepatic steatosis and hemangioma. Peritumoral sparing of fatty infiltration is present around hemangioma., Transverse sonogram shows increased liver echogenicity suggestive of hepatic steatosis. Well-defined hypoechoic mass with thick hyperechoic rim is surrounded by geographic hypoechoic area (arrowheads)., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and pericaval mass with profoundly low attenuation. Geographic hyperdense area (arrowheads) around tumor corresponds to peritumoral hypoechoic area in, suggesting presence of peritumoral sparing of fatty infiltration., ontrast-enhanced hepatic arterial phase T scan shows temporal peritumoral enhancement (arrowheads) around hemangioma possibly caused by arterioportal shunt. (Fig. 1 continues on next page) 1020 JR:190, pril 2008
Sonography of Hepatic Steatosis D Fig. 1 (continued) 50-year-old woman with hepatic steatosis and hemangioma. Peritumoral sparing of fatty infiltration is present around hemangioma. D, In-phase gradient-echo T1-weighted MR image shows hypointense pericaval mass. E, Opposed-phase gradient-echo T1-weighted MR image shows low signal intensity of hepatic parenchyma, suggesting hepatic steatosis. Geographic peritumoral hyperintense area (arrowheads) corresponds to peritumoral hypoechoic area in. Finding indicates presence of peritumoral sparing of fatty infiltration. Fig. 2 70-year-old woman with hepatic steatosis and high-flow hemangioma with arterioportal shunt. Peritumoral sparing of fatty infiltration is present around hemangioma., Oblique sagittal sonogram shows increased liver echogenicity suggestive of hepatic steatosis. Small hypoechoic mass with thick hyperechoic rim (arrows) is surrounded by wedge-shaped hypoechoic area (arrowheads)., olor Doppler sonogram shows vigorous intratumoral blood flow (long arrows). Reversed blood flow in portal branch (short arrows) parallel to feeding artery suggests presence of high-flow hemangioma with arterioportal shunt. (Fig. 2 continues on next page) E JR:190, pril 2008 1021
Kim et al. Fig. 2 (continued) 70-year-old woman with hepatic steatosis and high-flow hemangioma with arterioportal shunt. Peritumoral sparing of fatty infiltration is present around hemangioma., Unenhanced T scan shows inhomogeneously low hepatic attenuation suggestive of mild hepatic steatosis. Subtle hyperdense area (arrowheads) around tumor (arrow) suggests presence of peritumoral sparing of fatty infiltration. D, ontrast-enhanced hepatic arterial phase T scan shows strong homogeneous enhancement of tumor (arrow) and peritumoral parenchymal enhancement (arrowheads) suggestive of high-flow hemangioma with arterioportal shunt. Fig. 3 79-year-old man with hepatic steatosis and hepatocellular carcinoma. Peritumoral sparing of fatty infiltration is present around hepatocellular carcinoma., Transverse sonogram shows increased liver echogenicity suggestive of hepatic steatosis. Hypoechoic mass (arrow) and wedge-shaped hypoechoic area (arrowheads) are present in right hepatic lobe., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and well-defined hypoattenuating mass. Ill-defined hyperdense rim (arrowheads) surrounds tumor, which corresponds to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration., ontrast-enhanced hepatic arterial phase T scan shows enhancing tumor surrounded by wedge-shaped parenchymal enhancement (arrowheads) in right hepatic lobe. It is not definite whether this type of temporal enhancement indicates arterioportal shunt or corona-like enhancement. Diagnosis of hepatocellular carcinoma was made after percutaneous biopsy of tumor. D 1022 JR:190, pril 2008
Sonography of Hepatic Steatosis Fig. 4 65-year-old woman with hepatic steatosis and cholangiocarcinoma. Peritumoral sparing of fatty infiltration surrounds cholangiocarcinoma., Transverse sonogram shows increased liver echogenicity suggestive of hepatic steatosis and slightly hypoechoic mass in right hepatic lobe. Mass is surrounded by wedge-shaped hypoechoic areas (arrowheads). apsular retraction adjacent to mass (arrows) is evident., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and low-attenuation mass in right hepatic lobe. Wedge-shaped peritumoral hyperdense area (arrowheads) corresponds to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration., ontrast-enhanced hepatic arterial phase T scan shows tumor encasing right anterior segmental portal vein (arrow). Rimlike and wedge-shaped parenchymal enhancement (arrowheads) surrounds tumor. Right hepatectomy was performed; pathologic diagnosis of mass was cholangiocarcinoma. Fig. 5 57-year-old man with hepatic steatosis and metastasis from gallbladder carcinoma. Peritumoral sparing of fatty infiltration surrounds metastatic lesion., Oblique sagittal sonogram shows increased liver echogenicity suggestive of hepatic steatosis and slightly hypoechoic mass with subtle hyperechoic rim (long arrow) in right hepatic lobe. Mass is surrounded by large hypoechoic areas (arrowheads). Tram track like hypoechoic lesion (short arrows) surrounding small tubular structure, presumed to be thrombosed portal branch, is adjacent to mass. (Fig. 5 continues on next page) JR:190, pril 2008 1023
Kim et al. Fig. 5 (continued) 57-year-old man with hepatic steatosis and metastasis from gallbladder carcinoma. Peritumoral sparing of fatty infiltration surrounds metastatic lesion., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and low-attenuation mass (long arrow) with ill-defined geographic peritumoral hyperdense area (arrowheads) corresponding to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration. Small dotlike lowattenuation lesion (short arrow) is adjacent to mass., ontrast-enhanced hepatic arterial phase T scan shows ill-defined tumor with poor contrast enhancement (long arrow), geographic peritumoral parenchymal enhancement (arrowheads), and lack of opacification of portal branch (short arrow). Diagnosis of metastasis from gallbladder carcinoma was made after percutaneous biopsy of tumor. Fig. 6 55-year-old man with hepatic steatosis and metastasis from renal cell carcinoma. Peritumoral sparing of fatty infiltration is present around metastatic lesions., Oblique sagittal sonogram shows increased liver echogenicity suggestive of hepatic steatosis and hypoechoic mass (asterisk) surrounded by slightly hypoechoic area (arrowheads) in right hepatic lobe., In-phase gradient-echo T1-weighted MR image shows multiple hypointense metastatic masses. (Fig. 6 continues on next page) 1024 JR:190, pril 2008
Sonography of Hepatic Steatosis Fig. 6 (continued) 55-year-old man with hepatic steatosis and metastasis from renal cell carcinoma. Peritumoral sparing of fatty infiltration is present around metastatic lesions., Opposed-phase gradient-echo T1-weighted MR image shows low parenchymal signal intensity in right hepatic lobe, suggesting hepatic steatosis. Subsegmental hyperintense area (arrowheads) surrounds metastatic lesions (arrows) corresponding to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration. D, ontrast-enhanced T scan shows diffuse tumoral enhancement (arrows) and arterial hyperperfusion around tumors (arrowheads) probably caused by siphoning effect of hypervascular metastatic lesions. Right hepatectomy was performed; pathologic diagnosis was metastasis from renal cell carcinoma. Fig. 7 56-year-old man with hepatic steatosis and pyogenic abscess. Peritumoral sparing of fatty infiltration is present around abscess., Oblique sagittal sonogram shows increased liver echogenicity suggestive of hepatic steatosis and hypoechoic lesion (asterisk) surrounded by slightly hypoechoic area (arrowheads) in right hepatic lobe., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and low-attenuation mass (asterisk) in right hepatic lobe. Ill-defined peritumoral hyperdense area (arrowheads) corresponds to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration., ontrast-enhanced hepatic arterial phase T scan shows segmental hepatic arterial hyperperfusion (arrowheads) around large abscess (asterisk) in right hepatic lobe. Diagnosis of pyogenic abscess was made with percutaneous fineneedle aspiration of lesion. D JR:190, pril 2008 1025
Kim et al. Fig. 8 63-year-old man with hepatic steatosis and parasitic abscess. Peritumoral sparing of fatty infiltration is present around abscess., Oblique coronal sonogram shows increased liver echogenicity suggestive of hepatic steatosis and slightly hypoechoic lesion with hyperechoic rim (arrows) surrounded by ill-defined hypoechoic area (arrowheads) in right hepatic lobe., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and small low-attenuation lesion (arrow) with peritumoral hyperdense area (arrowheads) corresponding to peritumoral hypoechoic area in. Finding represents peritumoral sparing of fatty infiltration., ontrast-enhanced T scan shows ill-defined parenchymal enhancement (arrowheads) surrounding small necrotic lesion (arrow) in right hepatic lobe. Diagnosis of parasitic abscess was made after percutaneous needle biopsy of lesion. Enzyme-linked immunosorbent assay result was positive for Fasciola hepatica. Fig. 9 65-year-old woman with hepatic steatosis and simple cyst. Peritumoral sparing of fatty infiltration is present around cyst., Transverse sonogram shows increased liver echogenicity suggestive of hepatic steatosis and anechoic cystic lesion in left hepatic lobe. Ill-defined boundary (arrowheads) between hepatic parenchyma and lesion and focal dilatation of segmental intrahepatic duct (arrows) suggest complicated cyst or cystic tumor., Unenhanced T scan shows low hepatic attenuation suggestive of hepatic steatosis and well-defined cystic lesion in left hepatic lobe surrounded by thin hyperdense rim (arrowheads). Focal dilatation of segmental intrahepatic duct (arrows) also is present. (Fig. 9 continues on next page) 1026 JR:190, pril 2008
Sonography of Hepatic Steatosis E Fig. 9 (continued) 65-year-old woman with hepatic steatosis and simple cyst. Peritumoral sparing of fatty infiltration is present around cyst., In-phase gradient-echo T1-weighted MR image shows cystic lesion with low signal intensity. D, Opposed-phase gradient-echo T1-weighted MR image shows low signal intensity of hepatic parenchyma suggestive of hepatic steatosis. Thin rim (arrowheads) of high signal intensity around cyst suggests peritumoral sparing of fatty infiltration. ecause of mass effect of lesion, left hepatic lobectomy was performed for diagnosis of cystic tumor. Diagnosis of simple biliary cyst was made at pathologic examination. (H and E) E, Low-power photomicrograph shows mild fatty infiltration in hepatic parenchyma. F, Low-power photomicrograph shows peritumoral sparing of fatty infiltration in hepatic parenchyma surrounding cyst. (H and E) D F JR:190, pril 2008 1027