AJR 2005; 184:S82-S85
© American Roentgen Ray Society
Fluid-Fluid Levels in Cavernous Hemangiomas of the Liver: Baffled?
Sangeet Ghai,
Marcus Dill-Macky,
Stephanie Wilson and
Masoom Haider
Division of Abdominal Imaging, University Health Network, Mount Sinai
Hospital, University of Toronto, Princess Margaret Hospital 3-923, 610
University Ave., Toronto, Ontario, Canada, M5G 2M9.
Received March 14, 2004;
accepted after revision June 1, 2004.
Address correspondence to M. Dill-Macky
(Marcus.Dill-Macky{at}uhn.on.ca).
Introduction
Cavernous hemangioma is the most common benign tumor of the liver.
The imaging appearances and characteristic enhancement patterns identifying
these lesions are well described on sonography, CT, and MRI. The presence of a
fluid-fluid level within a hemangioma is an unusual variant that has been
rarely described
[1-3].
Extremely slow flow has been postulated as the cause of this phenomenon. We
present a case of fluid-fluid levels in multiple liver hemangiomas and offer
an explanation for their appearance, with an analogy observed in the penis on
MRI.
Case Report
A 34-year-old woman with vague abdominal pain was discovered to have
multiple liver lesions on sonography and was referred to our institution for
further characterization. A multiphasic MDCT was performed. Unenhanced scans
revealed multiple (
50) well-defined, low-density lesions compared with
the surrounding liver, ranging in diameter from 0.6 to 3 cm. Sixteen of the
lesions contained a single fluid-fluid level. Arterial phase images depicted
subtle peripheral enhancement in a minority (< 5) of lesions, none of which
contained a fluid-fluid level. Portal phase imaging depicted progressive
peripheral nodular enhancement typical of hemangiomas in most of the lesions
(30 of 50). Enhancement in those with fluid levels was of a peripheral nodular
type; however, the progression of enhancement was relatively delayed (Figs.
1A,
1B and
1C). Perflutren liquid
microsphere-enhanced (Definity, Bristol-Myers Squibb) sonography with pulse
inversion (DE-PII) and a multiphasic gadolinium-enhanced MRI were also
performed to increase diagnostic confidence.

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Fig. 1A. 34-year-old woman with vague abdominal pain. Multiphase axial
MDCT images were obtained at level of right adrenal gland. Precontrast image
depicts multiple lesions with fluid-fluid levels (arrows).
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Fig. 1B. 34-year-old woman with vague abdominal pain. Multiphase axial
MDCT images were obtained at level of right adrenal gland. Arterial phase
image detects subtle peripheral nodular enhancement in some lesions
(arrows).
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Fig. 1C. 34-year-old woman with vague abdominal pain. Multiphase axial
MDCT images were obtained at level of right adrenal gland. Centripetal
progression is identified on portal phase image typical of hemangiomas
(arrows).
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Sonography showed multifocal liver lesions that could be grouped into three
distinct populations. Most had the typical homogeneous hyperechoic appearance
of a hemangioma. Others had an atypical pattern, consisting of an isoechoic or
hypoechoic lesion compared with the liver, with an echogenic border. The third
group revealed a distinct fluid-fluid level that correlated with some,
although not all, of the lesion with fluid-fluid levels on CT
(Fig. 2). Sonography did not
identify fluid-fluid levels in these lesions after decubitus positioning of
the patient for 5 min. DE-PII revealed progressive peripheral nodular
enhancement diagnostic of hemangiomas in all lesions on imaging delayed up to
7 min (Fig. 3).

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Fig. 2. 34-year-old woman with vague abdominal pain. Sagittal
sonogram centers on dominant segment VIII hemangioma (straight arrow)
that is also depicted in Figures.
1A,
1B,
1C,
3, and
4. Three distinct populations
of hemangiomas are identified: a typical echogenic lesion (straight
arrow), atypical hypoechoic lesion with echogenic border (curved
arrow), and lesion containing fluid-fluid level (gray arrow). CT
and MRI (Figs. 1A,
1B,
1C and
4) identified fluid-fluid level
in segment VIII hemangioma (straight arrow) that was occult on
sonography because of background echogenicity of lesion.
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Fig. 3. 34-year-old woman with vague abdominal pain. Sagittal
sonograms center on dominant segment VIII hemangioma (straight arrow)
after perflutren liquid microsphere (Definity, Bristol-Myers Squibb) is
injected using contrast-specific, (low mechanical index) pulse-inversion
imaging technique. Same lesion is also depicted in Figures
1A,
1B,
1C,
2, and
4. Progressive and persistent
centripetal nodular enhancement (arrows) typical of hemangiomas is
shown on 3 min (A) and 5 min (B) delayed images.
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Fig. 4. 34-year-old woman with vague abdominal pain. T2-weighted
fat-saturated MR images were obtained at level of right adrenal. Supine
(A) and right lateral decubitus (B) positions show
gravity-dependent shifts in fluid-fluid level orientation in hemangiomas
(arrows).
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MRI was performed in the supine and right lateral decubitus positions to
evaluate "mobility" of the fluid-fluid levels. All lesions were
cerebrospinal fluid-bright on T2-weighted sequences. Sixteen lesions showed
fluid-fluid levels. All fluid-fluid levels changed orientation to realign
horizontally when moving the patient to the right lateral decubitus position
from a supine position when imaged after a 15-min delay
(Fig. 4). Enhancement after
administration of gadolinium was typical for hemangiomas in all lesions,
showing progressive nodular centripetal enhancement that persisted on imaging
delayed up to 3 min from injection. Sixteen lesions showed incomplete
centripetal progression on delayed imaging up to 3 min. All of these lesions
had fluid-fluid levels on precontrast imaging.
Discussion
Fluid-fluid levels may be seen where fluid-like material of different
densities are contained within a compartmentalized space. This has been
described in the imaging literature in complicated cysts, abscesses, chronic
hematomas, biliary cystadenomas, tumors with liquefactive necrosis or
hemorrhage, and necrotic metastases
[3]. Fluid-fluid levels within
hemangiomas are very rare
[1-3].
CT and especially MRI easily show these fluid-fluid levels. To our
knowledge, we are the first to describe the same features on sonography.
Stagnant or the slow flow of blood likely results in sedimentation of RBCs
within the serum, producing the fluid-fluid levels. The superior fluid layer
consists of serum and the inferior layer, unclotted sedimentary RBCs
[1,
4]. On CT, the superior layer
is of fluid attenuation, while the inferior layer has a higher attenuation due
to the density of the packed cells. On MRI, T2-weighted sequences depict the
superior fluid layer as high (fluid) signal intensity while the inferior layer
is of relatively low signal intensity compared with the liver, because of the
high cellular content. On T1-weighted imaging, the serum has low signal
intensity and the sedimentary packed cells, intermediate signal intensity
compared with the liver.
Itai et al. [1] describe
more than 10 hemangiomas in three patients with fluid-fluid levels on CT,
which were occult on sonography in the two patients who were scanned. CT did
not reveal positional changes in the levels, and no evidence of enhancement
was seen on dynamic CT. The authors postulate hemolyzed blood as the possible
cause of this phenomenon. Obata et al.
[2] report multiple fluid-fluid
levels in a giant cavernous hemangioma. Typical peripheral nodular enhancement
was observed on CT, but only on delayed 15-min scanning. Autopsy revealed no
evidence of thrombosis or hemolysis within the hemangioma. Extremely slow flow
within the hemangioma, resulting in separation of the blood cells and serum,
was proposed as the mechanism for fluid-fluid level formation. We have shown
changes in fluid-fluid level orientation on MRI when altering the patient's
position. In addition, we have shown on DE-PII, CT, and MRI relatively delayed
progressive enhancement of the lesions with fluid-fluid levels typical of
hemangiomas. Thus, we concur with the theory that this subcategory of
hemangioma has a relatively slow inflow of blood. As a result, a sedimentation
effect is the likely cause of the fluid-fluid levels.
Sonography is considered more sensitive for the detection of fluid-fluid
levels in liver lesions than CT
[5]. In hemangiomas, multiple
internal interfaces within the lesion result in the typical hyperechoic
appearance. On sonography, fluid-fluid levels in this setting would be
relatively more difficult to detect because of the resulting reduction in
contrast resolution from the increased background echogenicity
(Fig. 2). CT and MRI, however,
are not affected by the number of interfaces within a lesion, relying on
different physical properties to achieve contrast. We believe this may explain
the observed discrepancy of fluid-fluid level detection between sonography and
CT or MRI.
To further explain the imaging appearances, we propose an instructive
analogy in the penis. Incidental fluid-fluid levels were noted in the corpora
cavernosa on T2-weighted MR images in some patients having pelvic imaging for
un-related reasons (Fig. 5). To
our knowledge, this has not been previously described in the literature. The
normal enhancement of the corpora cavenosa on gadolinium-enhanced MRI has been
documented and bears an intriguing similarity to that of a cavernous
hemangioma with gradual enhancement on sequential postcontrast MR images. In
the penis, however, enhancement progresses in a centrifugal direction from the
central cavernosal artery as opposed to the centripetal progression seen in
hemangiomas [6]. As with the
hemangiomas we describe containing fluid-fluid levels, enhancement is
relatively delayed, occurring over 10 to 15 min. The corpus cavernosa consists
of an intercommunicating volume (the sinusoidal intracorporeal network)
separated by innumerable incomplete septations or baffles rather than multiple
separate vessels or a single, large vascular space
[7]. Blood flow in such a
structure is slow, almost stagnant. As free communication occurs between the
cavities, the volume of blood will act as a whole, explaining the appearance
of a single sedimentation level across the corpus cavernosa after a period of
inactivity by the patient. We propose that hemangiomas with fluid-fluid levels
can be explained in an analogous way. We theorize that these lesions contain a
large intercommunicating macroscopic space, baffled by a microscopic network
of incomplete septations similar to the corpus cavernosa. Soyer et al.
[3] describe a case in their
series with imaging very similar to ours, in which the lesion underwent
surgical biopsy. This showed a single large vascular space containing blood.
Cavernous hemangiomas are described pathologically as having larger vascular
spaces than capillary hemangiomas, but this is at a microscopic level. Large
vascular lakes in these lesions are lined by a single layer of flat
endothelial cells and separated by fibrous septa
[8]. We can find no pathologic
description of a variation of hemangiomas with macroscopic spaces that would
correlate with the proposal of a single dilated cavity. The truth in our case
will be revealed only with histologic correlation. However, the diagnosis of
hemangioma in our patient did not require biopsy.
In summary, a fluid-fluid level in a hemangioma is an unusual and dramatic
variant in an otherwise common, benign, and well-described lesion. Our case
illustrates typical enhancement characteristics on DE-PII, CT, and MRI that
are preserved in these lesions, allowing a confident diagnosis of hemangioma
without resorting to biopsy. We propose that this subcategory of hemangiomas
consists of an intercommunicating volume "baffled" by incomplete
septations, similar to the sinusoidal intracorporeal network of the corpus
cavernosa. The relatively low sensitivity of sonography in detecting
fluid-fluid levels in these lesions may be explained by the reduction in
contrast produced by the background echogenicity of the baffles. The cause of
the fluid-fluid levels is undoubtedly sedimenting RBCs in a large,
slow-flowing vascular space.
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