DOI:10.2214/AJR.07.2863
AJR 2008; 190:1018-1027
© American Roentgen Ray Society
Sparing of Fatty Infiltration Around Focal Hepatic Lesions in Patients with Hepatic Steatosis: Sonographic Appearance with CT and MRI Correlation
Kyoung Won Kim1,
Min Ju Kim2,
Seung Soo Lee1,
Hyoung Jung Kim3,
Yong Moon Shin1,
Pyo-Nyun Kim1 and
Moon-Gyu Lee1
1 Department of Radiology, Asan Medical Center, University of Ulsan College of
Medicine, 388-1, Pungnap 2-dong, Songpa-ku, Seoul 138-736, Korea.
2 Department of Radiology, National Cancer Center, Gyeonggi-do, Korea.
3 Department of Diagnostic Radiology, Kyung Hee University Hospital, Seoul,
South Korea.
Received July 12, 2007;
accepted after revision October 10, 2007.
Address correspondence to K. W. Kim
(kimkw{at}amc.seoul.kr).
Abstract
OBJECTIVE. 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 CT and MRI findings, and to discuss the possible
mechanisms.
CONCLUSION. 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.
Keywords: Doppler study fatty liver liver neoplasms sonography
Introduction
Focal 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].
At 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 CT 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 CT
[6] and as a hyperintense
peritumoral rim on chemical shift MRI
[2,
3]. Chen 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 echo-poor 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] (Figs.
1A,
1B,
1C,
1D, and
1E). 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 CT 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
gradient-echo MR that represented peritumoral sparing of fatty infiltration, a
geographic peritumoral hypoechoic area was correspondingly seen in 27 (68%) of
the tumors. Although 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.
Color 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] (Figs.
2A,
2B,
2C, and
2D).

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Fig. 1A —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).
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Fig. 1B —50-year-old woman with hepatic steatosis and hemangioma.
Peritumoral sparing of fatty infiltration is present around hemangioma.
Unenhanced CT 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 A, suggesting presence of peritumoral sparing of
fatty infiltration.
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Fig. 1C —50-year-old woman with hepatic steatosis and hemangioma.
Peritumoral sparing of fatty infiltration is present around hemangioma.
Contrast-enhanced hepatic arterial phase CT scan shows temporal peritumoral
enhancement (arrowheads) around hemangioma possibly caused by
arterioportal shunt.
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Fig. 1D —50-year-old woman with hepatic steatosis and hemangioma.
Peritumoral sparing of fatty infiltration is present around hemangioma.
In-phase gradient-echo T1-weighted MR image shows hypointense pericaval
mass.
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Fig. 1E —50-year-old woman with hepatic steatosis and hemangioma.
Peritumoral sparing of fatty infiltration is present around hemangioma.
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 A. Finding indicates presence of peritumoral sparing of fatty
infiltration.
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Fig. 2A —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).
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Fig. 2B —70-year-old woman with hepatic steatosis and high-flow
hemangioma with arterioportal shunt. Peritumoral sparing of fatty infiltration
is present around hemangioma. Color 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.
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Fig. 2C —70-year-old woman with hepatic steatosis and high-flow
hemangioma with arterioportal shunt. Peritumoral sparing of fatty infiltration
is present around hemangioma. Unenhanced CT 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.
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Fig. 2D —70-year-old woman with hepatic steatosis and high-flow
hemangioma with arterioportal shunt. Peritumoral sparing of fatty infiltration
is present around hemangioma. Contrast-enhanced hepatic arterial phase CT scan
shows strong homogeneous enhancement of tumor (arrow) and peritumoral
parenchymal enhancement (arrowheads) suggestive of high-flow
hemangioma with arterioportal shunt.
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Hepatocellular Carcinoma
In contrast to the high frequency of arterioportal shunt in hepatic
hemangioma [11], the shunt is
rare in small hepatocellular carcinomas (HCCs)
[12]. Nevertheless, HCC also
can accompany peritumoral sparing of fatty infiltration in hepatic steatosis.
Matsui et al. [13] found
corona-like enhancement of HCC on single-level dynamic CT 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 CT during arterial portography. Therefore, the
decrease in regional portal flow may cause peritumoral sparing of fatty
infiltration around an HCC [4].
In the case of larger tumors, the arterial perfusion in the hepatic parenchyma
around the hypervascular HCC 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 HCCs with peritumoral sparing of
fatty infiltration (Figs. 3A,
3B, and
3C). Because 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 HCC. A well-designed
prospective study is warranted to determine the frequency of peritumoral
sparing of fatty infiltration around HCCs on sonography and to better describe
the sonographic appearance of HCCs with peritumoral sparing of fatty
infiltration. Color Doppler sonography may show large feeding arteries and
intratumoral flow, but corona-like enhancement and hemodynamic alteration
around HCC are usually below the sensitivity limits of the examination.

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Fig. 3A —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.
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Fig. 3B —79-year-old man with hepatic steatosis and hepatocellular
carcinoma. Peritumoral sparing of fatty infiltration is present around
hepatocellular carcinoma. Unenhanced CT 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 A. Finding represents
peritumoral sparing of fatty infiltration.
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Fig. 3C —79-year-old man with hepatic steatosis and hepatocellular
carcinoma. Peritumoral sparing of fatty infiltration is present around
hepatocellular carcinoma. Contrast-enhanced hepatic arterial phase CT 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.
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Cholangiocarcinoma
Cholangiocarcinoma 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 (Figs.
4A,
4B, and
4C). The extent of peritumoral
sparing of fatty infiltration varies with the degree of portal compromise and
arterial compensation.

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Fig. 4A —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). Capsular retraction adjacent to mass (arrows)
is evident.
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Fig. 4B —65-year-old woman with hepatic steatosis and
cholangiocarcinoma. Peritumoral sparing of fatty infiltration surrounds
cholangiocarcinoma. Unenhanced CT 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 A. Finding represents
peritumoral sparing of fatty infiltration.
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Fig. 4C —65-year-old woman with hepatic steatosis and
cholangiocarcinoma. Peritumoral sparing of fatty infiltration surrounds
cholangiocarcinoma. Contrast-enhanced hepatic arterial phase CT 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.
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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.
5A,
5B,
5C,
6A,
6B,
6C, and
6D). 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 HCCs, and portal flow decreases reciprocally.

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Fig. 5A —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.
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Fig. 5B —57-year-old man with hepatic steatosis and metastasis from
gallbladder carcinoma. Peritumoral sparing of fatty infiltration surrounds
metastatic lesion. Unenhanced CT 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 A. Finding represents
peritumoral sparing of fatty infiltration. Small dotlike low-attenuation
lesion (short arrow) is adjacent to mass.
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Fig. 5C —57-year-old man with hepatic steatosis and metastasis from
gallbladder carcinoma. Peritumoral sparing of fatty infiltration surrounds
metastatic lesion. Contrast-enhanced hepatic arterial phase CT 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.
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Fig. 6A —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.
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Fig. 6B —55-year-old man with hepatic steatosis and metastasis from
renal cell carcinoma. Peritumoral sparing of fatty infiltration is present
around metastatic lesions. In-phase gradient-echo T1-weighted MR image shows
multiple hypointense metastatic masses.
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Fig. 6C —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 A. Finding represents peritumoral sparing of fatty
infiltration.
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Fig. 6D —55-year-old man with hepatic steatosis and metastasis from
renal cell carcinoma. Peritumoral sparing of fatty infiltration is present
around metastatic lesions. Contrast-enhanced CT 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.
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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 space-occupying
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]. At 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 CT
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.
7A,
7B,
7C,
8A,
8B, and
8C).

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Fig. 7A —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.
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Fig. 7B —56-year-old man with hepatic steatosis and pyogenic abscess.
Peritumoral sparing of fatty infiltration is present around abscess.
Unenhanced CT 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 A. Finding represents peritumoral
sparing of fatty infiltration.
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Fig. 7C —56-year-old man with hepatic steatosis and pyogenic abscess.
Peritumoral sparing of fatty infiltration is present around abscess.
Contrast-enhanced hepatic arterial phase CT scan shows segmental hepatic
arterial hyperperfusion (arrowheads) around large abscess
(asterisk) in right hepatic lobe. Diagnosis of pyogenic abscess was
made with percutaneous fine-needle aspiration of lesion.
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Fig. 8A —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.
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Fig. 8B —63-year-old man with hepatic steatosis and parasitic abscess.
Peritumoral sparing of fatty infiltration is present around abscess.
Unenhanced CT 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 A. Finding represents peritumoral sparing of fatty
infiltration.
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Fig. 8C —63-year-old man with hepatic steatosis and parasitic abscess.
Peritumoral sparing of fatty infiltration is present around abscess.
Contrast-enhanced CT 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.
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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 (Figs.
9A,
9B,
9C,
9D,
9E, and
9F).

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Fig. 9A —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.
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Fig. 9B —65-year-old woman with hepatic steatosis and simple cyst.
Peritumoral sparing of fatty infiltration is present around cyst. Unenhanced
CT 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.
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Fig. 9C —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.
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Fig. 9D —65-year-old woman with hepatic steatosis and simple cyst.
Peritumoral sparing of fatty infiltration is present around cyst.
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. Because 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)
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Fig. 9E —65-year-old woman with hepatic steatosis and simple cyst.
Peritumoral sparing of fatty infiltration is present around cyst. Low-power
photomicrograph shows mild fatty infiltration in hepatic parenchyma.
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Fig. 9F —65-year-old woman with hepatic steatosis and simple cyst.
Peritumoral sparing of fatty infiltration is present around cyst. Low-power
photomicrograph shows peritumoral sparing of fatty infiltration in hepatic
parenchyma surrounding cyst. (H and E)
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Conclusion
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.
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