AJR 2003; 180:135-141
© American Roentgen Ray Society
Hepatic Hemangioma: Atypical Appearances on CT, MR Imaging, and Sonography
Hyun-Jung Jang1,2,
Tae Kyoung Kim3,
Hyo Keun Lim4,
Sang Jae Park2,
Jung Suk Sim1,
Hyae Young Kim1 and
Joo-Hyuk Lee1
1 Radiation Medicine Branch, Research Institute, National Cancer Center, 809
Madu 1-dong, Ilsan-gu, Goyang-si, Gyeonggi-do, 411-764, Korea.
2 Center for Liver Cancer, National Cancer Center Hospital, National Cancer
Center, Gyeonggi-do, 411-764, Korea.
3 Department of Diagnostic Radiology, Asan Medical Center, University of Ulsan
College of Medicine, 388-1, Poongnap-dong, Songpa-gu, Seoul, 138-736,
Korea.
4 Department of Radiology and Gastrointestinal Center, Sungkyunkwan University
School of Medicine, Samsung Medical Center, 50 Ilwon-dong, Kangnam-gu, Seoul,
135-710, Korea.
Received April 25, 2002;
accepted after revision July 2, 2002.
Address correspondence to H.-J. Jang.
Introduction
Hemangioma is the most common benign tumor of the liver. The classic
diagnostic findings for hemangioma are as follows
[1]: on unenhanced CT,
hypoattenuation similar to that of vessels; on dynamic contrast-enhanced CT or
MR imaging, peripheral globular enhancement and a centripetal fill-in pattern
with the attenuation of enhancing areas identical to that of the aorta and
blood pool; on T2- and heavily T2-weighted MR imaging, hyperintensity similar
to that of cerebrospinal fluid; on sonography, homogeneous hyperechogenicity
or hypo- or isoechogenicity with a hyperechoic rim; and on delayed phases of
99mTc RBC scanning, a defect in the early phases that shows
prolonged and persistent filling-in. Because of advances in imaging
technology, hemangiomas are being detected more frequently. We have
encountered various atypical forms that may be difficult to recognize as
hemangiomas on cross-sectional imaging. In this pictorial essay, we illustrate
the varied appearances of hemangiomas that do not meet conventional criteria
on various current imaging techniques and provide possible explanations for
their atypical appearances.
Small Hypoattenuating Hemangioma
Small hemangiomas are detected more frequently with helical CT, whereas
they are easily overlooked on conventional CT because they tend to be
isoattenuating on late-phase images
[2]. Due to earlier scanning,
slowly enhancing hemangiomas have more chance to show persistent
hypoattenuation, the incidence being up to 8-16%
[2,
3]. In daily practice, the
incidence of this form of hemangioma is even greater than previously reported,
especially for small hemangiomas that may not show the classic rapid-fill-in
pattern [2]. The reason for
this reported lower incidence is likely that the atypical appearance of this
type of hemangioma may have misled researchers into precluding the possibility
of hemangioma in the first place.
Small hypoattenuating hemangiomas are particularly problematic in patients
with underlying malignancy. If present, the "bright-dot"
signtiny enhancing dots in the hemangioma that do not progress to the
classic globular enhancement because of the small size of the lesion and the
propensity for very slow fill-inis helpful in diagnosing this type of
hemangioma [2] (Fig.
1A,1B,1C,1D).
However, a number of hemangiomas have no discernible enhancement
(Fig. 2A). One pathologic
correlative study suggested that hemangiomas with a slow fill-in pattern have
relatively large vascular spaces and that those with rapid enhancement have
small vascular spaces and a large interstitium
[4]. Such a tendency has no
relationship to the size of the tumor
[4]. Therefore, hemangioma
should be included in the differential diagnoses of small hypoattenuating
lesions as well as hypervascular lesions. Contrast-enhanced gray-scale
harmonic sonography, which has the capability of real-time dynamic assessment,
could be of help in characterizing such a small hypoattenuating hemangioma
seen on routine single-phase helical CT (Figs.
2B and
2C).

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Fig. 1A. Hypoattenuating hemangioma with "bright-dot" sign
in 62-year-old woman with rectal carcinoma. Contrast-enhanced CT scan obtained
during portal venous phase shows small hypoattenuating mass with tiny
enhancing dots (arrows).
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Fig. 1B. Hypoattenuating hemangioma with "bright-dot" sign
in 62-year-old woman with rectal carcinoma. T2-weighted MR image (TR/TE,
3800/138) shows mass (arrows) with typical bright signal
intensity.
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Fig. 1C. Hypoattenuating hemangioma with "bright-dot" sign
in 62-year-old woman with rectal carcinoma. Dynamic gadolinium-enhanced
T1-weighted MR images obtained 1 min (C) and 5 min (D) after
initiation of contrast agent administration show very slow enhancement
(arrows), a finding that is known to be rare in small
hemangiomas.
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Fig. 1D. Hypoattenuating hemangioma with "bright-dot" sign
in 62-year-old woman with rectal carcinoma. Dynamic gadolinium-enhanced
T1-weighted MR images obtained 1 min (C) and 5 min (D) after
initiation of contrast agent administration show very slow enhancement
(arrows), a finding that is known to be rare in small
hemangiomas.
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Fig. 2A. Hemangioma in 56-year-old man with gastric carcinoma.
Preoperative CT scan obtained during portal venous phase shows small
hypoattenuating hepatic lesion (arrow) with no discernible area of
enhancement.
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Fig. 2B. Hemangioma in 56-year-old man with gastric carcinoma.
Longitudinal scans of left hepatic lobe on contrast-enhanced gray-scale
harmonic sonograms obtained 1 min (B) and 3 min (C) after
initiation of contrast agent administration show typical nodular enhancement
with progressive fill-in pattern in mass (arrows), diagnostic of
hemangioma. CR = cranial aspect, CAUD = caudal aspect.
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Fig. 2C. Hemangioma in 56-year-old man with gastric carcinoma.
Longitudinal scans of left hepatic lobe on contrast-enhanced gray-scale
harmonic sonograms obtained 1 min (B) and 3 min (C) after
initiation of contrast agent administration show typical nodular enhancement
with progressive fill-in pattern in mass (arrows), diagnostic of
hemangioma. CR = cranial aspect, CAUD = caudal aspect.
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Atypical Signal on T2-Weighted MR Imaging
A long T2 relaxation time has been attributed to the presence of slowly
flowing blood in the vascular spaces of the tumor, and this bright T2 signal
on MR imaging is one of the most reliable findings in diagnosing hemangioma
[5]. It has been reported that
a threshold of 112 msec of T2 relaxation time results in 92% accuracy, 96%
sensitivity, and 87% specificity for differentiating hemangiomas from
metastases [5]. In small
hemangiomas, marked hyperintensity on T2-weighted images is a particularly
important finding because the pathognomonic nodular enhancement is frequently
not present [3]. Rarely,
hemangiomas with rapid enhancement (Fig.
3A,3B)
or with unusual abnormalities (Fig.
4A) may show T2 signal intensity that is not as bright as
cerebrospinal fluid on MR imaging and may cause confusion. The signal
intensity characteristics are known to be related to the relative composition
of vascular spaces and connective tissue in the lesion and to the presence of
thrombosis, calcification, hemorrhage, or fibrosis
[5].

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Fig. 3A. Hemangioma in 59-year-old man with gastric carcinoma.
T2-weighted MR image (TR/TE, 3800/138) shows small nodule (long
arrow) with unusually lower signal intensity than that of cerebrospinal
fluid (short arrows).
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Fig. 3B. Hemangioma in 59-year-old man with gastric carcinoma. Dynamic
gadolinium-enhanced T1-weighted MR image obtained 30 sec after initiation of
contrast agent administration shows rapid, uniform enhancement
(arrow). Intraoperative biopsy of hepatic lesion during gastric
surgery revealed cavernous hemangioma.
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Fig. 4A. Sclerosing hemangioma proven by sonography-guided core biopsy
in 47-year-old woman. T2-weighted MR image (TR/TE, infinite/134) shows mass
(long arrow) with hypointensity relative to cerebrospinal fluid
(short arrows).
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Attenuation Relative to Vascular Pool
Because enhancing areas in hemangioma consist of vascular spaces directly
supplied by arteries, the attenuation of such areas is theoretically identical
to that of the aorta on hepatic arterial phase and that of blood pool during
later phase imaging. Such a characteristic is helpful in differentiating
hemangiomas from other tumors, but occasionally this finding makes it
difficult to distinguish hemangiomas from vessels on CT
(Fig. 5). On the other hand,
not rarely for hemangiomas in general, and more commonly in small hemangiomas,
the enhancing areas show lower attenuation than that of the aorta or portal or
hepatic veins on multiphase helical CT
[3] (Figs.
4B and
6).

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Fig. 5. Hemangioma in 41-year-old woman. Contrast-enhanced CT scan
obtained during portal venous phase shows ovoid mass (arrow)
isoattenuating relative to hepatic vessels, which is apt to be overlooked
without scrutiny. Diagnosis was verified by typical homogeneous
hyperechogenicity and absence of new growth on follow-up sonography (not
shown) after 17 months.
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Fig. 4B. Sclerosing hemangioma proven by sonography-guided core biopsy
in 47-year-old woman. Contrast-enhanced CT scan obtained during portal venous
phase shows fuzzy area of enhancement within mass hypoattenuating relative to
hepatic vessels (arrow), which is unusual for hemangioma.
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Fig. 6. Hemangioma in 59-year-old man with gastric carcinoma.
Preoperative CT scan obtained during single portal venous phase shows small
nodule with area of enhancement (thick arrow) hypoattenuating to
aorta (a) and to portal vein (thin arrow). Diagnosis was verified by
typical findings on MR imaging and absence of new growth on 1-year follow-up
CT scan (not shown).
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Hemangioma Versus Hypervascular Malignancy
Differentiation of hemangiomas from other hypervascular tumors can be a
challenge because some hypervascular tumors can mimic peripheral globular
enhancement (Fig.
7A,7B,7C),
and not all hemangiomas show such a characteristic pattern
[3,
5]. Neuroendocrine tumors or
metastases from breast or colon cancer may show strong T2 hyperintensity
[5], and prolonged
contrast-enhancement may be seen in certain hypervascular malignancies
[3]. It is helpful to know that
hemangiomas can remain unenhanced, but once the areas enhance they do not
diminish. Interpretation based on the combination of two or more imaging
characteristics is required.

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Fig. 7A. Multiple angiosarcomas in 48-year-old man with no
predisposing factor. Dynamic gadolinium-enhanced T1-weighted MR images
obtained 45 sec (A) and 3 min (B) after initiation of contrast
agent administration show multiple masses (arrows, B) with
progressive fill-in pattern. Also visible is globular enhancement
(arrows, A), as seen in typical hemangioma.
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Fig. 7B. Multiple angiosarcomas in 48-year-old man with no
predisposing factor. Dynamic gadolinium-enhanced T1-weighted MR images
obtained 45 sec (A) and 3 min (B) after initiation of contrast
agent administration show multiple masses (arrows, B) with
progressive fill-in pattern. Also visible is globular enhancement
(arrows, A), as seen in typical hemangioma.
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Fig. 7C. Multiple angiosarcomas in 48-year-old man with no
predisposing factor. T2-weighted MR image (TR/TE, infinite/134) shows masses
(arrows) with bright but slightly heterogeneous signal intensity,
which is unusual for hemangioma. Ascites (asterisks) is visible in
perihepatic and perisplenic spaces.
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Hemangioma with Arterioportal Shunt
An arterioportal shunt associated with a hepatic tumor is generally
recognized to be most characteristic of malignant tumors. However, an
arterioportal shunt sometimes is seen in hepatic hemangiomas on multiphase
helical CT [6] (Fig.
8A,8B).
Similar temporal peritumoral enhancement can be seen on dynamic MR images
[7] (Fig.
9A,9B).
These tumors tend to show rapid enhancement
[6,
7]. One possible explanation
for this finding is that a rapidly enhancing small hemangioma has hyperdynamic
status with large arterial inflow, rapid tumoral enhancement, and
consequently, large and rapid outflow, which seems to result in early
opacification of the draining portal vein via shunt and peritumoral
enhancement [7]. The finding to
note is a wedge-shaped or irregularly shaped enhancement adjacent to the
hemangiomawith or without early visualized portal branchesduring
the hepatic arterial phase (Fig.
8A,8B)
that becomes isoattenuating or slightly hyperattenuating relative to the
normal liver during the portal venous phase
[6]. An association with
arterioportal shunt does not necessarily imply that the underlying tumor is
malignant.

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Fig. 8A. Rapidly enhancing hemangioma with arterioportal shunt in
43-year-old woman. Contrast-enhanced CT scan obtained during hepatic arterial
phase shows mass (large arrow) with strong homogeneous enhancement.
Also seen are hypoattenuating lesions (small arrows), proven to be
other hemangiomas.
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Fig. 8B. Rapidly enhancing hemangioma with arterioportal shunt in
43-year-old woman. Contrast-enhanced CT scan obtained during hepatic arterial
phase at level next caudal to A shows wedge-shaped faint enhancement
(arrows) with early draining portal branch (arrowheads)
accompanying mass seen in A.
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Fig. 9A. Rapidly enhancing hemangioma with arterioportal shunt in
58-year-old man. Dynamic gadolinium-enhanced T1-weighted MR image obtained 30
sec after initiation of contrast agent administration shows two masses
(black arrows) with nearly complete fill-in pattern of enhancement.
Also visible is wedge-shaped faint peritumoral enhancement (white
arrows) that became isoattenuating relative to normal parenchyma on later
phases (not shown).
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Fig. 9B. Rapidly enhancing hemangioma with arterioportal shunt in
58-year-old man. T2-weighted MR image (TR/TE, infinite/134) shows bright
signal intensity of masses (arrows), typical for hemangioma.
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Hemangioma in Fatty Liver
Severe fatty liver may alter the apparent enhancement pattern of focal
hepatic lesions. Even hypovascular tumors such as metastases can show
relatively high attenuation on CT and may mimic hemangiomas with a persistent
enhancement pattern (Fig.
10A,10B).
In severe fatty liver, the attenuation of hemangioma may reverse to even
hyperattenuation, although not greater than that of vessels, on unenhanced CT.
Hemangiomas may also be accompanied by a focal spared zone as seen in
malignant tumors in fatty liver. On sonography, this finding could create
confusion with the hypoechoic halo seen in malignant tumors (Fig.
11A,11B,11C),
contrary to hemangiomas' usual hyperechogenicity or hyperechoic rim. This
unusual finding often makes subsequent CT or MR imaging necessary. Hemangiomas
in fatty liver could produce a peculiar halo on CT or MR imaging as well, but
in most cases, accurate diagnosis can be made without difficulty because of
the characteristic dynamic enhancement pattern of hemangiomas.

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Fig. 10A. Metastasis from breast carcinoma in 37-year-old woman with
severe fatty liver. Contrast-enhanced CT scan obtained 3 min after initiation
of contrast agent administration shows mass (arrow) mimicking
prolonged homogeneous enhancement of hemangioma. Hepatic arterial and portal
venous phase images (not shown) also revealed homogeneous
hyperattenuation.
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Fig. 11B. Hemangioma with hypoechoic halo in 37-year-old man with
background fatty liver. Opposed-phase T1-weighted MR image shows hyperintense
rim representing focal spared zone (arrows) around mass.
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Fig. 11C. Hemangioma with hypoechoic halo in 37-year-old man with
background fatty liver. Dynamic gadolinium-enhanced T1-weighted MR image
obtained 90 sec after initiation of contrast agent administration shows
typical peripheral globular enhancement (arrows) that can lead to
confident diagnosis of hemangioma.
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Hemangioma in Liver Cirrhosis
With progressive cirrhosis, hemangiomas are likely to decrease in size and
become more fibrotic (Fig.
12A,12B,12C)
and difficult to diagnose radiologically and pathologically
[8]. Conversely, hepatocellular
carcinoma and dysplastic nodules often mimic hemangioma on sonography (Fig.
13A,13B)
because of hyperechogenicity resulting from factors such as necrosis,
fibrosis, fatty change, or sinusoid dilatation. In cirrhosis, any hyperechoic
nodule should be considered a probable hepatocellular carcinoma until proven
otherwise.

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Fig. 12A. Hemangioma in 59-year-old man with cirrhosis and known
hepatocellular carcinoma in right lobe (not shown). Contrast-enhanced CT scan
obtained during portal venous phase shows nodule (arrows) with subtle
hypoattenuation.
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Fig. 12B. Hemangioma in 59-year-old man with cirrhosis and known
hepatocellular carcinoma in right lobe (not shown). Intraoperative sonogram
shows hyperechoic nodule (arrows), which cannot exclude possibility
of hepatocellular carcinoma. Surgical resection revealed cavernous
hemangioma.
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Fig. 12C. Hemangioma in 59-year-old man with cirrhosis and known
hepatocellular carcinoma in right lobe (not shown). Photomicrograph of
surgical specimen shows large noncommunicating vascular spaces (v) and
abundant fibrosis (f), which may be responsible for lack of enhancement. (H
and E, x 200)
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Fig. 13A. Early hepatocellular carcinoma in 51-year-old man. Patient
had another known hepatocellular carcinoma (not shown) in lower part of right
lobe and underlying cirrhosis. Sonogram shows homogeneous hyperechoic nodule
(arrows), indistinguishable from typical hemangioma.
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Fig. 13B. Early hepatocellular carcinoma in 51-year-old man. Patient
had another known hepatocellular carcinoma (not shown) in lower part of right
lobe and underlying cirrhosis. Photomicrograph of surgical specimen reveals
early hepatocellular carcinoma with extensive fatty infiltration (clear
spaces). (H and E, x 40)
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Conclusion
A subset of hepatic hemangiomas does not show the classic findings on CT,
MR imaging, and sonography that are well known to radiologists. Radiologists
should be aware that some hepatic hemangiomas may have atypical features on
cross-sectional imaging that correlate with their varied hemodynamic and
pathologic findings.
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