Stephen
F. Quinn,
Hepatic Diagnostic
MD
Cavernous Sign
Many hepatic hemangiomas covered incidentally during mental
dynamic
G. Gordon
#{149}
bolus
are disincre-
computed
tomography (CT). To meet the established criteria for diagnosis with CT, however, a second CT examination with single-level dynamic bolus imaging is necessary. A prospective evaluation was performed to examine a simple sign that may be used to diagnose cavernous hemangiomas during incremental dynamic bolus CT. This sign is the visualization of foci of globular enhancement within the hemangioma, analogous to areas of puddling of contrast material seen at angiography. A total of 34 lesions in 21 patients demonstrated foci of globular enhancement. Of the 34 lesions, 32 (94%) proved to be hemangiomas. All 21 patients underwent confirmatory evaluation. Foci of globular enhancement seen during dynamic bolus CT are a strong indication that the lesion is a cavernous hemangioma. This diagnostic sign may obviate further, more expensive imaging studies. Index terms: Angioma, gastrointestinal 761.3194 #{149}Liver, neoplasms, 761.3194 neoplasms, CT, 761.1211 Radiology
1992;
tract, Liver,
#{149}
182:545-548
Benjamin,
MD
Hemangiomas: with Dynamic
C
Simple Bolus CT’
hemangiomas
are the solid hepatic lesions and have a frequency of up to 7.3% in the general population (1). Certain computed tomographic AVERNOUS
most
(CT)
common
criteria
benign
have
been
established
for
diagnosing hepatic cavernous hemangiomas (2-8). These criteria require a special session with CT that includes unenhanced imaging and contrast material-enhanced, single-level dynamic bolus imaging. To perform these, there must be prospective knowledge
of the
hemangioma.
In
mi-
practice, many hemangiomas are tially discovered during the course of incremental dynamic bolus CT, and a second CT examination or other confirmatory study must be performed to make the diagnosis of a hemangioma. At our institution, dynamic bolus CT showed areas of globular enhancement in hepatic hemangiomas that were analogous to the puddling of contrast material seen at angiography. This observation led to a prospective evaluation of the CT appearance of hepatic hemangiomas during dynamic bolus contrast enhancement to determine if the diagnostic sign of globular enhancement could obviate the need for an additional single-level dynamic bolus CT examination or other confirmatory studies.
MATERIALS
AND
METHODS
Over
a 3-year period, 1,259 contrastabdominal CT examinations performed with the dynamic bolus technique were prospectively evaluated. The examinations were performed with 150180 mL of diatrizoate meglumine (282 mg enhanced
From the Department of Radiology, Good Samaritan Hospital, 1015 NW 22nd St, Portland, OR 97210 (S.F.Q.); the Departments of Radiology and General Surgery, Division of Vascular Surgery, Oregon Health Sciences University, Portland (S.F.Q.); and the Medical College of Wisconsin, Milwaukee (G.G.B.). Received May 9, 1991; revision requested June 5; final revision received September 6; accepted September 23. Address reprint requests to S.F.Q. i: RSNA, 1992
of iodine of iodine
per milliliter)
per milliliter). ages of the liver were
or iohexol
(240 mg
Unenhanced also obtained
imin 80
patients. A 50-mL
followed
by constant
130 mL at 0.5 mL/sec.
10-15 seconds
scans,
a 3.5-second
interscan
delay,
and
a
512 x 512 matrix.
The enhancement lesions
were
patterns
evaluated.
of all hepatic
Globular enhanceto be present when less than 1 cm in
ment was considered enhancement nodules diameter were seen within the lesions during dynamic bolus imaging (Fig 1). In addition, globular enhancement was differentiated from rim enhancement. The results
of the CT examinations
mi-
were
tially interpreted by five radiologists overread by one radiologist (S.F.Q.). lesions
exhibiting
globular
and
The
enhancement
on a log sheet, and the refer-
were
noted
ring
physician
was contacted
to arrange
confirmatory studies. The attenuation of the areas of globular enhancement was reviewed retrospectively. The qualitative attenuation of each area
globular
of enhancement
pared
with
that of adjacent
cause
this was performed
quantitative be obtained. Thirty-four
attenuation lesions
ited foci of globular
in
was comvessels. Beretrospectively, values could not
21 patients
exhib-
during dynamic bolus CT. These lesions varied from 15 to 110 mm (mean, 46 mm) in diameter, with an incidence of one to three lesions (mean, 1.8) per patient. Confirmatory evidence was obtained in all patients
with
magnetic
enhancement
resonance
(MR) imaging
(n = 5), angiography (,i = 5), nuclear medicine red cell-tagged studies (n = 8) (Fig 2), surgery (n = 4), biopsy (ii = 1), evidence of no growth over 12 months (n = 3), and/or repeated CT to demonstrate classic characteristics of hemangioma (n = 3). For various reasons, some of
the patients
underwent
more than one In four patients who had previously undergone angiography, the hemangiomas were resected at the discretion of the surgeon. The MR examinations were performed free of charge, study.
confirmatory
since other
they were confirmatory
performed studies.
in addition
to
The clinical
bolus of intravenous contrast material was delivered over 25 seconds with a power injector (Medrad, Pitts-
burgh),
images of 10-mm-thick contiguous sections were obtained by using 2-second
infusion
information about patients focal hepatic lesions that did globular enhancement was re-
with
solid not exhibit
viewed. of
Approximately
after the bolus was started,
The number
ing globular determined, metastases
of lesions
not exhibit-
enhancement could not be however, because of diffuse found in many patients. If
545
a.
C.
b.
Figure
1.
Hepatic
hemangiomas
exhibiting
foci of globular
enhancement.
(a) Dynamic
bolus
contrast-enhanced
mangioma in the posterior segment of the right lobe of the liver, which exhibits a conglomeration of enhancing of enhancement within a solid hepatic lesion (straight arrows). These areas of enhancement have an attenuation cent hepatic veins (curved arrow) but less than that of the aorta. (c) Less discrete foci of globular enhancement nodules is close to that of the portal veins but less than that of the aorta.
there
was a previous
diagnosis
mas
of hepatic
metastatic disease, or if a patient’s clinical history was typical of hepatic metastatic disease, no further workup was performed. In cases of uncertain diagnosis, biopsy or surgery was performed.
was
dition, tions,
patients
1,259
who
to monitor
treatment
sponse,
and
group,
(17.63%)
of this
had
metastatic
under-
re-
222 neoplasms
to
the liver. The primary sites are summarized in the Table. There were six neuroendocrine tumors but no angiosarcomas found at the primary pancreatic and gastric sites. Of the 34 lesions that exhibited foci of globular enhancement, 94% (n 32) proved to be hemangiomas and 6% (n 2) proved to be adenocarcinoma metastases from colon cancer (Fig 3). Both adenocarcinoma metasta=
=
ses were
found
in one
patient.
In four patients, there were five hemangiomas that did not exhibit the sign
diagnostic
ment. an
These
irregular
of globular
enhance-
hemangiomas exhibited rim (n 3) or diffuse en=
hancement (n 2) and were diagnosed by means of biopsy (n 4) or nuclear medicine red cell-tagged study (n 1). The lesions varied from 35 to 48 mm (mean, 41 mm) in diameter. The retrospective review of the qualitative attenuation of globular areas of enhancement showed that the attenuation in all 32 hemangio=
=
=
546
#{149} Radiology
less than
that
and hepatic that
of the
of the
veins
aorta.
but
In ad-
in the closely
adenocarcinoma approximated
portal
and
nate
lesions
nostic
testing
that
hepatic
mas.
Because hemangiomas are common in the general population, they are often seen incidentally during the course of abdominal CT examinations. Hemangiomas are most often detected during CT examinations in the
dynamic
bolus
for detecting
method lesions
(9), is used.
technique,
focal The
a
for
diagnosis of hepatic hemangiomas with dynamic bolus CT require a dedicated single-level examination after a suspected
hemangioma
is localized.
The strict CT criteria established by Freeny and Marks are that a hepatic hemangioma will (a) be of low attenuation on unenhanced images, (b) demonstrate peripheral contrast enhancement during the dynamic bolus phase of scanning, and (c) demonstrate complete isoattenuated fill-in on delayed scans obtained up to 60 minutes after administration of contrast material (7). Freeny and Marks reported that only 55% (32 of 58) of hepatic hemangiomas will meet these strict
CT criteria
(7), and
in patients
with known malignancies, approximately 86% of lesions meeting the criteria will be hemangiomas (8). This leaves a large number of indetermi-
he-
that
require
with
MR
further imaging
diag(10-
In our
experience,
94%
of lesions
be conclusive.
hepatic
criteria
hepatic
having foci of globular enhancement proved to be hepatic hemangiomas. This high correlation obviates the need for additional and more costly studies and procedures that may not
DISCUSSION
which
shows
17), biopsy (18), nuclear medicine (19,20), angiography (21), or follow-up evaluation. Our results suggest that the presence of foci of globular enhancement on dynamic bolus CT scans is an accurate indicator of hepatic hemangio-
in the two false-positive situathe attenuation of the enhanc-
of the adjacent veins.
went abdominal CT examination, 247 (19.62%) were found to have solid focal hepatic lesions. Many of these patients underwent multiple examinations
approximated
portal
ing nodules metastases
RESULTS Of the
closely
adjacent
CT scan
foci (arrow). (b) Globular areas value close to that of the adja(arrows). Attenuation of the
The foci of globular enhancement seen during dynamic bolus CT imaging are analogous to the puddling of contrast material seen during angiography
and
dynamic
contrast-en-
hanced MR imaging (22). Scatarige et al indicated that nodular enhancement with contrast-enhanced CT is suggestive of giant cavernous hemangiomas (23). The puddles of contrast material, or nodular areas of enhancement, whether they are seen at contrast-enhanced MR imaging, CT, or angiography, are thought to represent large vascular lakes that are a distinctive feature of cavernous hemangiomas (21). Gaa et al recently described nodular areas of enhancement as being a typical finding in a group of patients with
proved
hemangiomas
(24).
Using
a CT scanner with a 1-second interscan delay and an 8-second bolus time, the authors were able to see nodular areas during the arterial phase of enhancement (24). The results
of our
study
are
consistent
February
with
1992
b.
a.
Figure 3. Metastatic adenocarcinoma with foci of globular enhancement (arrows) on a dynamic bolus CT scan. The lesions were in-
correctly
diagnosed
as hemangiomas.
rent practice in many centers perform a second confirmatory once a suspected hemangioma discovered (25). This practice expensive
exercise
prevalence institution,
is to study is is an
considering
the
of hemangiomas. At our the costs of available constudies are as follows: unen-
firmatory
hanced and enhanced CT, $628; MR imaging of the abdomen, $1,133; Tc99m red cell-tagged study with single photon emission CT, $629; liver hiopsy with CT guidance, $728; and angiography, $1,605. These figures do
Figure
,
I
I
not include and hospital
d.
C.
2.
Globular
enhancement
in cavernous
hemangiomas.
(a) Dynamic
bolus
CT
scan
the costs of medication observation necessary
demonstrates a hepatic hemangioma in the dome of the liver with multiple foci of globular enhancement (arrows). (b) Corresponding axial image from a single photon emission CT Tc99m red cell-tagged study shows a focal area of increased photon activity corresponding to the hepatic hemangioma (straight arrow). Curved arrow indicates cardiac activity. (c) Dy-
for biopsies and angiography. This report has several limitations that deserve special mention. In our study, the number of proved cavern-
namic bolus CT lobe of the liver
ous
scan with
demonstrates multiple
nar image from a Tc-99m ton activity (arrows).
foci
a hepatic of globular
red cell-tagged
hemangioma enhancement
study
shows
in the medial segment of the (arrows). (d) Corresponding
a corresponding
area
of increased
and
were seen by using convencontrast material bolus methods a longer
interscan
delay.
state that the attenuation ules seen in hemangiomas that of the adjacent aorta arteries (24). Retrospective shows that the difference
Volume
182
but in our study, areas of enhance-
Number
#{149}
pho-
2
Gaa
et al
of the nodis equal to and hepatic review between our results and those of Gaa et al is probably due to variations in bolus technique and interscan delay. Our own experience showed that the hemangioma nodules had qualitative attenuation similar to that of adjacent hepatic and portal veins but less than that of the aorta. Not all hemangiomas will exhibit foci of globular enhancement, but if this simple sign is used to diagnose hemangiomas, other costly confirmatory studies can be avoided. The cur-
was
hemangiomas
the total number was underestimated. giomas
ment tional
these observations, the same nodular
left pla-
may
performing examinations omas
were
small
because
of hemangiomas Smaller heman-
have
been
missed
isoattenuated
with
adjacent normal parenchyma. hemangiomas in this study 46 mm
by
only contrast-enhanced because such hemangi-
in diameter,
the
The averaged
suggesting
that
smaller hemangiomas may not exhibit foci of globular enhancement. Some patients with multiple metastases almost certainly harbored hemangiomas, but no effort was made to evaluate all the
lesions
once
the
diagnosis
of metastatic cancer was made. The total number of hemangiomas does not include suspected hemangiomas that were not evaluated further or were misdiagnosed. The specificity and sensitivity this diagnostic sign could not
culated, because and false-negative
the true-negative values were
available.
To determine
autopsies
with
these
a point-by-point Radiology
of
be calnot values,
cone547
#{149}
lation with a recent CT examination would have to be performed. Since we did not examine any patients with angiosarcoma, and since we have inadequate data on patients with hepatomas,
we
cannot
conclude
that
these lesions. Therefore, the diagnostic sign of globular enhancement seen
study.
8.
and 9. 10.
We thank Ellen C. Pelker, Mary Alice Payne for their of this manuscript.
11.
References 1.
2.
Ishak KG, Rabin L. Benign tumors of the liver. Med Clin North Am 1975; 59:9991013. Bree RL, Schwab RE, Glazer GM, Fink-Bennett D. The varied appearances of hepatic
cavernous
3.
4.
548
hemangiomas
#{149} Radiology
12.
Itai Y, Ohtomo hepatic masses:
Freeny
K, Kokubo significance
Dytumors.
T, et al. CT of of prolonged AJR 1986; 146:
enhancement.
PC, Marks
13.
15.
Hepatic
16.
WittenbergJ, Stark DD, Forman BH, et al. Differentiation of hepatic metastases from hepatic hemangiomas and cysts by using MR imaging. AJR 1988; 151:79-84.
17.
Lombardo DM, Baker ME, Spritzer CE, Blinder R, Meyers W, Herfkens RJ. He-
hemangi-
Foley WD.
Dynamic
hepatic
resonance
imaging
18.
19.
CT. Radiol-
ogy 1989; 170:617-622. Glazer GM, Aisen AM, Francis JR. et al. Hepatic cavernous hemangioma: magnetic resonance imaging. Radiology 1988; 155: 417-420. Itai Y, Ohtomo K, Furui S, Yamauchi T, Minami M, Yashiro N. Noninvasive diagnosis of small cavernous hemangioma of the liver: advantage of MRI. AJR 1985; 145: 1195-1199. Stark DD, Felder RC, WittenbergJ, et al.
20.
21.
22.
of cavernous
23.
ages: importance
24.
criteria.
of size-specific
AJR 1990;
quantita-
155:61-66.
Choi BI, Han MC, Kim CW. Small hepatocellular carcinoma versus small cavernous hemangioma: differentiation with MR imaging at 2.0 T. Radiology 1990; 176:103-106. Ohtomo K, Itai Y, Yoshikawa K, Kokubo T, ho M. Hepatocellular carcinoma and cayernous hemangioma: differentiation with MR imaging. Radiology 1988; 168:621-623.
patic hemangiomas vs metastases: MR differentiation at 1.5 T. AJR 1990; 155:55-59. Cronan JJ, Esparza AR, Dorfman GS, Ridlen MS, Paolella LP. Cavernous hemangioma of the liver: role of percutaneous biopsy. Radiology 1988; 166:135-138. Tumeh 55, Benson C, NagelJS, English RJ, Herman BL. Cavernous hemangioma of the liver: detection with single-photon emission computed tomography. Radiology 1987; 164:353-356. Birnbaum BA, Weinrab JC, Megibui AJ, et al. Definitive diagnosis of hepatic hemangiomas: MR imaging versus Tc-99m-la-
beled red blood
hemangiomas of the liver: tissue specific characterization. AJR 1985; 145:213-222. Itoh K, Saini S, Hahn PF, Imam N, Ferrucci JT. Differentiation between small hepatic hemangiomas and metastases on MR imtive
14.
WM.
oma: dynamic bolus CT. AJR 1986; 147:71 1719. Freeny PC, Marks WM. Patterns of contrast enhancement of benign and malignant hepatic neoplasms during bolus dynamic and delayed CT. Radiology 1986; 160:613-618.
Magnetic
with sonography,
computed tomography, magnetic resonance imaging and scintigraphy. RadioGraphics 1987; 7:1153-1175. Ashida C, Fishman EK, Zerhouni EA, Herlong FH, Siegelman 55. Computed tomography of hepatic cavernous hemangioma. J Comput Assist Tomogr 1987; 11:455460. Barnett PH, Zerhouni EA, White RI, Siegelman SS. Computed tomography in the diagnosis of cavernous hemangiomas of the liver. AIR 1980; 134:439-447.
5, Tasaka A. of hepatic
729-733. 7.
U
Acknowledgments: Lynda E. Holte, and help in the preparation
T, Itai Y, Furui CT densitometry
and delayed
may in our
Araki namic
AJR 1980; 135:1037-1043. 6.
the
globular enhancement sign is useful in distinguishing hemangiomas from
at dynamic bolus CT, if present, prove useful, but the sensitivity specificity were not determined
5.
cell SPECT.
Radiology
1990; 176:95-101. McLoughlin MJ. Angiography in cavernous hemangioma of the liver. AJR 1971; 113:50-55. Hamm B, Fischer E, Taupitz M. Differentiation of hepatic hemangiomas from metastases by dynamic contrast-enhanced MR imaging. J Comput Assist Tomogr 1990; 14:205-216. Scatarige JC, Kenny JM, Fishman EK, Herlong FH, Siegelman SS. CT of giant cayernous hemangioma. AJR 1989; 149:83-85. Gaa J, Saini S, Ferrucci JT. Perfusion characteristics of hepatic cavernous hemangi-
oma using intravenous CT angiography. EurJ Radiol 1991; 12:228-233. 25.
Nelson
RC, ChezmarJL.
proach to hepatic 1990;
Diagnostic
hemangiomas.
ap-
Radiology
176:11-13.
February
1992
F. Quinn,
Hepatic Diagnostic
MD
Cavernous Sign
Many hepatic hemangiomas covered incidentally during mental
dynamic
G. Gordon
#{149}
bolus
are disincre-
computed
tomography (CT). To meet the established criteria for diagnosis with CT, however, a second CT examination with single-level dynamic bolus imaging is necessary. A prospective evaluation was performed to examine a simple sign that may be used to diagnose cavernous hemangiomas during incremental dynamic bolus CT. This sign is the visualization of foci of globular enhancement within the hemangioma, analogous to areas of puddling of contrast material seen at angiography. A total of 34 lesions in 21 patients demonstrated foci of globular enhancement. Of the 34 lesions, 32 (94%) proved to be hemangiomas. All 21 patients underwent confirmatory evaluation. Foci of globular enhancement seen during dynamic bolus CT are a strong indication that the lesion is a cavernous hemangioma. This diagnostic sign may obviate further, more expensive imaging studies. Index terms: Angioma, gastrointestinal 761.3194 #{149}Liver, neoplasms, 761.3194 neoplasms, CT, 761.1211 Radiology
1992;
tract, Liver,
#{149}
182:545-548
Benjamin,
MD
Hemangiomas: with Dynamic
C
Simple Bolus CT’
hemangiomas
are the solid hepatic lesions and have a frequency of up to 7.3% in the general population (1). Certain computed tomographic AVERNOUS
most
(CT)
common
criteria
benign
have
been
established
for
diagnosing hepatic cavernous hemangiomas (2-8). These criteria require a special session with CT that includes unenhanced imaging and contrast material-enhanced, single-level dynamic bolus imaging. To perform these, there must be prospective knowledge
of the
hemangioma.
In
mi-
practice, many hemangiomas are tially discovered during the course of incremental dynamic bolus CT, and a second CT examination or other confirmatory study must be performed to make the diagnosis of a hemangioma. At our institution, dynamic bolus CT showed areas of globular enhancement in hepatic hemangiomas that were analogous to the puddling of contrast material seen at angiography. This observation led to a prospective evaluation of the CT appearance of hepatic hemangiomas during dynamic bolus contrast enhancement to determine if the diagnostic sign of globular enhancement could obviate the need for an additional single-level dynamic bolus CT examination or other confirmatory studies.
MATERIALS
AND
METHODS
Over
a 3-year period, 1,259 contrastabdominal CT examinations performed with the dynamic bolus technique were prospectively evaluated. The examinations were performed with 150180 mL of diatrizoate meglumine (282 mg enhanced
From the Department of Radiology, Good Samaritan Hospital, 1015 NW 22nd St, Portland, OR 97210 (S.F.Q.); the Departments of Radiology and General Surgery, Division of Vascular Surgery, Oregon Health Sciences University, Portland (S.F.Q.); and the Medical College of Wisconsin, Milwaukee (G.G.B.). Received May 9, 1991; revision requested June 5; final revision received September 6; accepted September 23. Address reprint requests to S.F.Q. i: RSNA, 1992
of iodine of iodine
per milliliter)
per milliliter). ages of the liver were
or iohexol
(240 mg
Unenhanced also obtained
imin 80
patients. A 50-mL
followed
by constant
130 mL at 0.5 mL/sec.
10-15 seconds
scans,
a 3.5-second
interscan
delay,
and
a
512 x 512 matrix.
The enhancement lesions
were
patterns
evaluated.
of all hepatic
Globular enhanceto be present when less than 1 cm in
ment was considered enhancement nodules diameter were seen within the lesions during dynamic bolus imaging (Fig 1). In addition, globular enhancement was differentiated from rim enhancement. The results
of the CT examinations
mi-
were
tially interpreted by five radiologists overread by one radiologist (S.F.Q.). lesions
exhibiting
globular
and
The
enhancement
on a log sheet, and the refer-
were
noted
ring
physician
was contacted
to arrange
confirmatory studies. The attenuation of the areas of globular enhancement was reviewed retrospectively. The qualitative attenuation of each area
globular
of enhancement
pared
with
that of adjacent
cause
this was performed
quantitative be obtained. Thirty-four
attenuation lesions
ited foci of globular
in
was comvessels. Beretrospectively, values could not
21 patients
exhib-
during dynamic bolus CT. These lesions varied from 15 to 110 mm (mean, 46 mm) in diameter, with an incidence of one to three lesions (mean, 1.8) per patient. Confirmatory evidence was obtained in all patients
with
magnetic
enhancement
resonance
(MR) imaging
(n = 5), angiography (,i = 5), nuclear medicine red cell-tagged studies (n = 8) (Fig 2), surgery (n = 4), biopsy (ii = 1), evidence of no growth over 12 months (n = 3), and/or repeated CT to demonstrate classic characteristics of hemangioma (n = 3). For various reasons, some of
the patients
underwent
more than one In four patients who had previously undergone angiography, the hemangiomas were resected at the discretion of the surgeon. The MR examinations were performed free of charge, study.
confirmatory
since other
they were confirmatory
performed studies.
in addition
to
The clinical
bolus of intravenous contrast material was delivered over 25 seconds with a power injector (Medrad, Pitts-
burgh),
images of 10-mm-thick contiguous sections were obtained by using 2-second
infusion
information about patients focal hepatic lesions that did globular enhancement was re-
with
solid not exhibit
viewed. of
Approximately
after the bolus was started,
The number
ing globular determined, metastases
of lesions
not exhibit-
enhancement could not be however, because of diffuse found in many patients. If
545
a.
C.
b.
Figure
1.
Hepatic
hemangiomas
exhibiting
foci of globular
enhancement.
(a) Dynamic
bolus
contrast-enhanced
mangioma in the posterior segment of the right lobe of the liver, which exhibits a conglomeration of enhancing of enhancement within a solid hepatic lesion (straight arrows). These areas of enhancement have an attenuation cent hepatic veins (curved arrow) but less than that of the aorta. (c) Less discrete foci of globular enhancement nodules is close to that of the portal veins but less than that of the aorta.
there
was a previous
diagnosis
mas
of hepatic
metastatic disease, or if a patient’s clinical history was typical of hepatic metastatic disease, no further workup was performed. In cases of uncertain diagnosis, biopsy or surgery was performed.
was
dition, tions,
patients
1,259
who
to monitor
treatment
sponse,
and
group,
(17.63%)
of this
had
metastatic
under-
re-
222 neoplasms
to
the liver. The primary sites are summarized in the Table. There were six neuroendocrine tumors but no angiosarcomas found at the primary pancreatic and gastric sites. Of the 34 lesions that exhibited foci of globular enhancement, 94% (n 32) proved to be hemangiomas and 6% (n 2) proved to be adenocarcinoma metastases from colon cancer (Fig 3). Both adenocarcinoma metasta=
=
ses were
found
in one
patient.
In four patients, there were five hemangiomas that did not exhibit the sign
diagnostic
ment. an
These
irregular
of globular
enhance-
hemangiomas exhibited rim (n 3) or diffuse en=
hancement (n 2) and were diagnosed by means of biopsy (n 4) or nuclear medicine red cell-tagged study (n 1). The lesions varied from 35 to 48 mm (mean, 41 mm) in diameter. The retrospective review of the qualitative attenuation of globular areas of enhancement showed that the attenuation in all 32 hemangio=
=
=
546
#{149} Radiology
less than
that
and hepatic that
of the
of the
veins
aorta.
but
In ad-
in the closely
adenocarcinoma approximated
portal
and
nate
lesions
nostic
testing
that
hepatic
mas.
Because hemangiomas are common in the general population, they are often seen incidentally during the course of abdominal CT examinations. Hemangiomas are most often detected during CT examinations in the
dynamic
bolus
for detecting
method lesions
(9), is used.
technique,
focal The
a
for
diagnosis of hepatic hemangiomas with dynamic bolus CT require a dedicated single-level examination after a suspected
hemangioma
is localized.
The strict CT criteria established by Freeny and Marks are that a hepatic hemangioma will (a) be of low attenuation on unenhanced images, (b) demonstrate peripheral contrast enhancement during the dynamic bolus phase of scanning, and (c) demonstrate complete isoattenuated fill-in on delayed scans obtained up to 60 minutes after administration of contrast material (7). Freeny and Marks reported that only 55% (32 of 58) of hepatic hemangiomas will meet these strict
CT criteria
(7), and
in patients
with known malignancies, approximately 86% of lesions meeting the criteria will be hemangiomas (8). This leaves a large number of indetermi-
he-
that
require
with
MR
further imaging
diag(10-
In our
experience,
94%
of lesions
be conclusive.
hepatic
criteria
hepatic
having foci of globular enhancement proved to be hepatic hemangiomas. This high correlation obviates the need for additional and more costly studies and procedures that may not
DISCUSSION
which
shows
17), biopsy (18), nuclear medicine (19,20), angiography (21), or follow-up evaluation. Our results suggest that the presence of foci of globular enhancement on dynamic bolus CT scans is an accurate indicator of hepatic hemangio-
in the two false-positive situathe attenuation of the enhanc-
of the adjacent veins.
went abdominal CT examination, 247 (19.62%) were found to have solid focal hepatic lesions. Many of these patients underwent multiple examinations
approximated
portal
ing nodules metastases
RESULTS Of the
closely
adjacent
CT scan
foci (arrow). (b) Globular areas value close to that of the adja(arrows). Attenuation of the
The foci of globular enhancement seen during dynamic bolus CT imaging are analogous to the puddling of contrast material seen during angiography
and
dynamic
contrast-en-
hanced MR imaging (22). Scatarige et al indicated that nodular enhancement with contrast-enhanced CT is suggestive of giant cavernous hemangiomas (23). The puddles of contrast material, or nodular areas of enhancement, whether they are seen at contrast-enhanced MR imaging, CT, or angiography, are thought to represent large vascular lakes that are a distinctive feature of cavernous hemangiomas (21). Gaa et al recently described nodular areas of enhancement as being a typical finding in a group of patients with
proved
hemangiomas
(24).
Using
a CT scanner with a 1-second interscan delay and an 8-second bolus time, the authors were able to see nodular areas during the arterial phase of enhancement (24). The results
of our
study
are
consistent
February
with
1992
b.
a.
Figure 3. Metastatic adenocarcinoma with foci of globular enhancement (arrows) on a dynamic bolus CT scan. The lesions were in-
correctly
diagnosed
as hemangiomas.
rent practice in many centers perform a second confirmatory once a suspected hemangioma discovered (25). This practice expensive
exercise
prevalence institution,
is to study is is an
considering
the
of hemangiomas. At our the costs of available constudies are as follows: unen-
firmatory
hanced and enhanced CT, $628; MR imaging of the abdomen, $1,133; Tc99m red cell-tagged study with single photon emission CT, $629; liver hiopsy with CT guidance, $728; and angiography, $1,605. These figures do
Figure
,
I
I
not include and hospital
d.
C.
2.
Globular
enhancement
in cavernous
hemangiomas.
(a) Dynamic
bolus
CT
scan
the costs of medication observation necessary
demonstrates a hepatic hemangioma in the dome of the liver with multiple foci of globular enhancement (arrows). (b) Corresponding axial image from a single photon emission CT Tc99m red cell-tagged study shows a focal area of increased photon activity corresponding to the hepatic hemangioma (straight arrow). Curved arrow indicates cardiac activity. (c) Dy-
for biopsies and angiography. This report has several limitations that deserve special mention. In our study, the number of proved cavern-
namic bolus CT lobe of the liver
ous
scan with
demonstrates multiple
nar image from a Tc-99m ton activity (arrows).
foci
a hepatic of globular
red cell-tagged
hemangioma enhancement
study
shows
in the medial segment of the (arrows). (d) Corresponding
a corresponding
area
of increased
and
were seen by using convencontrast material bolus methods a longer
interscan
delay.
state that the attenuation ules seen in hemangiomas that of the adjacent aorta arteries (24). Retrospective shows that the difference
Volume
182
but in our study, areas of enhance-
Number
#{149}
pho-
2
Gaa
et al
of the nodis equal to and hepatic review between our results and those of Gaa et al is probably due to variations in bolus technique and interscan delay. Our own experience showed that the hemangioma nodules had qualitative attenuation similar to that of adjacent hepatic and portal veins but less than that of the aorta. Not all hemangiomas will exhibit foci of globular enhancement, but if this simple sign is used to diagnose hemangiomas, other costly confirmatory studies can be avoided. The cur-
was
hemangiomas
the total number was underestimated. giomas
ment tional
these observations, the same nodular
left pla-
may
performing examinations omas
were
small
because
of hemangiomas Smaller heman-
have
been
missed
isoattenuated
with
adjacent normal parenchyma. hemangiomas in this study 46 mm
by
only contrast-enhanced because such hemangi-
in diameter,
the
The averaged
suggesting
that
smaller hemangiomas may not exhibit foci of globular enhancement. Some patients with multiple metastases almost certainly harbored hemangiomas, but no effort was made to evaluate all the
lesions
once
the
diagnosis
of metastatic cancer was made. The total number of hemangiomas does not include suspected hemangiomas that were not evaluated further or were misdiagnosed. The specificity and sensitivity this diagnostic sign could not
culated, because and false-negative
the true-negative values were
available.
To determine
autopsies
with
these
a point-by-point Radiology
of
be calnot values,
cone547
#{149}
lation with a recent CT examination would have to be performed. Since we did not examine any patients with angiosarcoma, and since we have inadequate data on patients with hepatomas,
we
cannot
conclude
that
these lesions. Therefore, the diagnostic sign of globular enhancement seen
study.
8.
and 9. 10.
We thank Ellen C. Pelker, Mary Alice Payne for their of this manuscript.
11.
References 1.
2.
Ishak KG, Rabin L. Benign tumors of the liver. Med Clin North Am 1975; 59:9991013. Bree RL, Schwab RE, Glazer GM, Fink-Bennett D. The varied appearances of hepatic
cavernous
3.
4.
548
hemangiomas
#{149} Radiology
12.
Itai Y, Ohtomo hepatic masses:
Freeny
K, Kokubo significance
Dytumors.
T, et al. CT of of prolonged AJR 1986; 146:
enhancement.
PC, Marks
13.
15.
Hepatic
16.
WittenbergJ, Stark DD, Forman BH, et al. Differentiation of hepatic metastases from hepatic hemangiomas and cysts by using MR imaging. AJR 1988; 151:79-84.
17.
Lombardo DM, Baker ME, Spritzer CE, Blinder R, Meyers W, Herfkens RJ. He-
hemangi-
Foley WD.
Dynamic
hepatic
resonance
imaging
18.
19.
CT. Radiol-
ogy 1989; 170:617-622. Glazer GM, Aisen AM, Francis JR. et al. Hepatic cavernous hemangioma: magnetic resonance imaging. Radiology 1988; 155: 417-420. Itai Y, Ohtomo K, Furui S, Yamauchi T, Minami M, Yashiro N. Noninvasive diagnosis of small cavernous hemangioma of the liver: advantage of MRI. AJR 1985; 145: 1195-1199. Stark DD, Felder RC, WittenbergJ, et al.
20.
21.
22.
of cavernous
23.
ages: importance
24.
criteria.
of size-specific
AJR 1990;
quantita-
155:61-66.
Choi BI, Han MC, Kim CW. Small hepatocellular carcinoma versus small cavernous hemangioma: differentiation with MR imaging at 2.0 T. Radiology 1990; 176:103-106. Ohtomo K, Itai Y, Yoshikawa K, Kokubo T, ho M. Hepatocellular carcinoma and cayernous hemangioma: differentiation with MR imaging. Radiology 1988; 168:621-623.
patic hemangiomas vs metastases: MR differentiation at 1.5 T. AJR 1990; 155:55-59. Cronan JJ, Esparza AR, Dorfman GS, Ridlen MS, Paolella LP. Cavernous hemangioma of the liver: role of percutaneous biopsy. Radiology 1988; 166:135-138. Tumeh 55, Benson C, NagelJS, English RJ, Herman BL. Cavernous hemangioma of the liver: detection with single-photon emission computed tomography. Radiology 1987; 164:353-356. Birnbaum BA, Weinrab JC, Megibui AJ, et al. Definitive diagnosis of hepatic hemangiomas: MR imaging versus Tc-99m-la-
beled red blood
hemangiomas of the liver: tissue specific characterization. AJR 1985; 145:213-222. Itoh K, Saini S, Hahn PF, Imam N, Ferrucci JT. Differentiation between small hepatic hemangiomas and metastases on MR imtive
14.
WM.
oma: dynamic bolus CT. AJR 1986; 147:71 1719. Freeny PC, Marks WM. Patterns of contrast enhancement of benign and malignant hepatic neoplasms during bolus dynamic and delayed CT. Radiology 1986; 160:613-618.
Magnetic
with sonography,
computed tomography, magnetic resonance imaging and scintigraphy. RadioGraphics 1987; 7:1153-1175. Ashida C, Fishman EK, Zerhouni EA, Herlong FH, Siegelman 55. Computed tomography of hepatic cavernous hemangioma. J Comput Assist Tomogr 1987; 11:455460. Barnett PH, Zerhouni EA, White RI, Siegelman SS. Computed tomography in the diagnosis of cavernous hemangiomas of the liver. AIR 1980; 134:439-447.
5, Tasaka A. of hepatic
729-733. 7.
U
Acknowledgments: Lynda E. Holte, and help in the preparation
T, Itai Y, Furui CT densitometry
and delayed
may in our
Araki namic
AJR 1980; 135:1037-1043. 6.
the
globular enhancement sign is useful in distinguishing hemangiomas from
at dynamic bolus CT, if present, prove useful, but the sensitivity specificity were not determined
5.
cell SPECT.
Radiology
1990; 176:95-101. McLoughlin MJ. Angiography in cavernous hemangioma of the liver. AJR 1971; 113:50-55. Hamm B, Fischer E, Taupitz M. Differentiation of hepatic hemangiomas from metastases by dynamic contrast-enhanced MR imaging. J Comput Assist Tomogr 1990; 14:205-216. Scatarige JC, Kenny JM, Fishman EK, Herlong FH, Siegelman SS. CT of giant cayernous hemangioma. AJR 1989; 149:83-85. Gaa J, Saini S, Ferrucci JT. Perfusion characteristics of hepatic cavernous hemangi-
oma using intravenous CT angiography. EurJ Radiol 1991; 12:228-233. 25.
Nelson
RC, ChezmarJL.
proach to hepatic 1990;
Diagnostic
hemangiomas.
ap-
Radiology
176:11-13.
February
1992
