AJR 2002; 178:67-73
© American Roentgen Ray Society
Assessment of Vascularity in Hepatic Tumors
Comparison of Power Doppler Sonography and Intraarterial CO2-Enhanced Sonography
Ran-Chou Chen1,2,
Wei-Tsung Chen1,
Hsing-Yang Tu1,
Nai-Yuan Cheng3,
Chung-Kwe Wang3,
Li-Ying Liao3,
Chaur-Shine Wang3 and
Pao-Huei Chen3
1
Department of Radiology, Taipei Municipal Jen-Ai Hospital, 10, Sec. 4, Jen-Ai
Rd., 106, Taipei, Taiwan.
2
Department of Radiology, School of Medicine, Taipei Medical University,
Taipei, Taiwan.
3
Department of Gastroenterology, Taipei Municipal Jen-Ai Hospital, Taipei,
Taiwan.
Received November 10, 2000;
accepted after revision July 24, 2001.
Address correspondence to R.-C. Chen.
Abstract
OBJECTIVE. The purpose of the study was to compare power Doppler
sonography with intraarterial CO2-enhanced sonography for revealing
vascularity in treated and untreated hepatic tumors.
SUBJECTS AND METHODS. Fifty-five patients with 93 liver tumors were
prospectively examined with power Doppler sonography and
CO2-enhanced sonography. These tumors included 29 hepatocellular
carcinomas in patients with no previous treatment, 26 treated hepatocellular
carcinomas, and 38 hemangiomas. The vascular depiction of power Doppler
sonography was compared with that obtained in the early phase of
CO2-enhanced sonography. The results of angiography were also
recorded for comparison.
RESULTS. In the hepatocellular carcinomas, power Doppler sonography
was the same as CO2-enhanced sonography in 18 (62%) of 29 tumors,
was inferior to CO2-enhanced sonography in nine (31%) of 29 tumors,
and was superior to CO2-enhanced sonography in two (7%) of 29
tumors. In the treated hepatocellular carcinomas, power Doppler sonography was
the same as CO2-enhanced sonography in 15 (58%) of 26 tumors and
was inferior in 11 (42%) of 26 tumors. In hemangiomas, the same vascularity
was found in both studies in 15 (39%) of 38 tumors, CO2-enhanced
sonography was superior in 22 (58%) of 38 tumors, and power Doppler sonography
was superior in one (3%) of 38 tumors. As a whole, 45% of the 93 tumors showed
better vascular depiction on CO2-enhanced sonography. However,
19.4% of tumors were hypovascular using power Doppler sonography but
hypervascular using CO2-enhanced sonography.
CONCLUSION. Power Doppler sonography is a useful technique for
screening hepatic tumor vascularity. CO2-enhanced sonography is
superior to power Doppler sonography in depicting tumor vascularity in treated
hepatocellular carcinomas and in hemangiomas, especially small
hemangiomas.
Introduction
Power Doppler sonography displays the integrated power of the Doppler
signal instead of the mean Doppler frequency shift shown in conventional color
Doppler imaging [1,
2]. Power Doppler sonography is
essentially angle-independent, does not alias, and extends the dynamic range
[3]. Its depiction of tumor
vascularity is superior to that of conventional color Doppler imaging
[2,
3]. Recent studies have shown
that contrast-enhanced sonography, with or without the harmonic method, is a
useful imaging modality for depicting tumor vascularity in liver tumors and
for showing the response to treatment of hepatocellular carcinoma
[4,
5]. However, the contrast agent
and the new machines are expensive, which limits their widespread adoption.
Another problem of contrast-enhanced sonography is the short duration of
enhancement. Therefore, power Doppler sonography is still the best choice for
depicting tumor vascularity in daily practice.
CO2-enhanced sonography is a sensitive method of detecting
hepatic tumor vascularity [3,
6]. The sensitivity of
CO2-enhanced sonography in detecting hypervascular hepatocellular
carcinoma is better than that of angiography, CT, and CT with iodized oil
[6,
7]. CO2-enhanced
sonography is also valuable for detecting the viable tumor part in treated
liver tumors [8]. Its major
disadvantage is that it is invasive. However, previous studies
[3,
6,
8,
9] indicate that
CO2-enhanced sonography can be used as a suitable reference to
evaluate the accuracy of power Doppler sonography.
The relative sensitivity of power Doppler sonography in detecting liver
tumor vascularity in comparison with CO2-enhanced sonography
remains unclear. The purpose of this study was to compare power Doppler
sonography with intraarterial CO2-enhanced sonography at the time
of angiography.
Subjects and Methods
From May 1997 to January 1999, 55 patients with 93 hepatic tumors were
prospectively examined with power Doppler sonography and
CO2-enhanced sonography. Twenty-two of these patients (29 tumors)
had previously untreated hepatocellular carcinoma, 14 patients (26 tumors) had
hepatocellular carcinoma that had already been treated by transarterial
embolization or transarterial embolization plus percutaneous ethanol
injection, and 19 patients (38 tumors) had hemangiomas. The size of the tumors
ranged from 1.0 to 7.6 cm (average, 3.2 cm). All hepatocellular carcinomas
were confirmed by needle biopsy and histologic diagnosis. All hemangiomas were
confirmed by angiography, dynamic CT, and more than 12 months of follow-up
studies, including MR imaging or sonography.
All patients were examined with power Doppler sonography before angiography
was performed, and all patients underwent CO2-enhanced sonography
after angiography. Power Doppler sonography was performed using a 3.5-MHz
color Doppler convex probe (Gateway; Diasonics, San Jose, CA) and software
(Tru color Angio; Diasonics).
The same radiologist examined all patients. The tumors were first
localized, and then the best scanning plane was selected. The vascular
depiction of the greatest dimension of the tumor and the regional liver
vessels was noted for comparative study. Color gain was adjusted by selecting
the highest value before color noise first became apparent in the imaging
background. The flow patterns seen on power Doppler sonography were classified
into four types: peripheral vessels, intratumoral vessels, peripheral spots,
and intratumoral spots. The term "vessels" was used to refer to
feeding, peritumoral, and intratumoral vessels of irregular courses and
calibers [10] (Figs.
1A and
1B). The term
"spots" referred to vascular lesions with dotted color or
CO2 signals [11]
(Figs. 1C and
1D).
After digital subtraction angiography was performed, the catheter was
placed in the hepatic propria artery. Three to six milliliters of pure
CO2 was injected as a bolus through the catheter under realtime
gray-scale sonographic monitoring of the liver tumor. The images of the early
(immediate, within seconds) to late phases (5 min) of dynamic
CO2-enhanced sonography and of the delayed phase (until
CO2 washout or 30 min) were recorded. The vascular branches were
well identified by the flow of the CO2 in the vessels in the early
arterial phase. Because the echogenic vascularities in the late phase were
similar to the tumor stain, the early phase of CO2-enhanced
sonography was chosen for comparison.
The power Doppler sonography signal was graded as absent (0), weak (1),
medium (2), or strong (3). The grade of the CO2 enhancement was
categorized as negative enhancement (0), iso- to slight enhancement (1),
moderate enhancement (2), or marked enhancement (3, >50% of the tumor).
Negative enhancement (grade 0) was defined as an isoechoic area in the tumor
with echoic peripheral liver parenchyma showing in the early CO2
phase. Two radiologists separately conducted a subjective comparison to
determine whether power Doppler sonography or CO2-enhanced
sonography better depicted the tumor vascularity. Disagreements were resolved
by consensus. However, the depictions of the vascularity between the two scans
were generally clear. If a decision as to which one was better could not be
made, it was assumed that the two modalities provided the same results. The
results of angiography were evaluated for comparison. The results of iodized
oil CT, dynamic CT, or follow-up angiography were evaluated for tumors with
discrepant findings between power Doppler sonography and
CO2-enhanced sonography.
Fisher's exact test and the Student's t test were used for
comparison of data among the imaging modalities and diagnostic groups as
appropriate.
Results
In the hepatocellular carcinoma group, the vascularity shown on power
Doppler sonography was the same as that on CO2-enhanced sonography
in 18 (62%) of 29 tumors (Fig.
1A,1B,1C,1D).
The vascularity detected on CO2-enhanced sonography was superior to
that detected by power Doppler sonography in nine (31%) of 29 tumors (Fig.
2A,2B,2C,2D,2E,2F).
Among the nine tumors with superior vascularity on CO2-enhanced
sonography, three were hypovascular on power Doppler sonography but
hypervascular on CO2-enhanced sonography. Angiography, iodized oil
CT, or follow-up angiography confirmed additional vascularities in these three
tumors. Two (7%) of 29 hepatocellular carcinoma tumors showed more extensive
vascularity on power Doppler sonography. Power Doppler sonography of these two
tumors showed venous flow in the additional flow noted on power Doppler
sonography, and angiography showed negative tumor enhancement.
In the treated hepatocellular carcinomas, tumor vascularity on power
Doppler sonography was the same as that on CO2-enhanced sonography
in 15 (58%) of 26 tumors, whereas CO2-enhanced sonography was
superior in 11 (42%) of 26 tumors (Fig.
3A,3B,3C).
Six of these tumors showed hypovascularity on power Doppler sonography but
hypervascularity on CO2-enhanced sonography. One of these six
tumors was hypervascular on angiography, and two showed slight vascularity on
angiography, whereas iodized oil CT showed iodized oil retention in areas of
additional vascularity detected on CO2-enhanced sonography. The
remaining three tumors showed tumor size enlargement and hypervascularity on
follow-up dynamic CT.
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Fig. 3C. —Hepatocellular carcinoma in 65-year-old man after two
transcatheter arterial embolizations. CO2-enhanced sonogram shows
heterogeneous enhancement (arrow) in peripheral and central portions
of tumor. Echogenic areas (arrowheads) around mass might be result of
arterioportal shunting of peripheral feeder vessels in this area.
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Hemangiomas showed the same vascular depiction on power Doppler sonography
and CO2-enhanced sonography in 15 (39%) of 38 tumors (Fig.
4A,4B,4C),
and showed higher vascularity on CO2-enhanced sonography in 22
(58%) of 38 tumors. All but one of these 22 tumors showed unequivocal
hypervascularity on angiography. The tumor that was not seen on angiography
was located in the lateral tip of the left lateral segment and was
superimposed with the vascularity of the gastric fundus. Dynamic CT identified
this tumor as hypervascular. One (3%) of the 38 hemangiomas showed higher
vascularity on power Doppler sonography
(Table 1). A flashing artifact
on power Doppler sonography was noted in this tumor, and angiography and
CO2-enhanced sonography were similar in the tumor.
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TABLE 1 Subjective Assessment of Tumor Vascularity Revealed on
CO2-Enhanced Sonography (CO2S) and Power Doppler
Sonography (PDS)
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The different vascularity between power Doppler sonography and
CO2-enhanced sonography was significant in both hemangiomas and
treated hepatocellular carcinoma (p < 0.05). However, no
significant difference was found between these two techniques for
hepatocellular carcinoma (p = 0.15).
The same degree of vascular depiction was found in both examinations in 48
(52%) of 93 tumors (including hepatocellular carcinomas, treated
hepatocellular carcinomas, and hemangioma). However, when the hypervascular
rate was compared instead of the degree of tumor vascularity, only 18 (19.4%)
of 93 tumors showed hypervascularity on CO2-enhanced sonography but
hypovascularity on power Doppler sonography. Two tumors (2.2%) showed
hypervascularity on power Doppler sonography but hypovascularity on
CO2-enhanced sonography. The remaining 73 tumors (78.5%) showed
hypervascularity on both power Doppler sonography and CO2-enhanced
sonography (although the degree of vascularity was not the same in some
tumors) or hypovascularity on both examinations. The comparison of results for
hypervascularity and hypovascularity on power Doppler sonography and
CO2-enhanced sonography is summarized in
Table 2.
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TABLE 2 Assessment of Tumor Vascularity: Comparison of CO2-Enhanced
Sonography (CO2S), Power Doppler Sonography (PDS), and
Angiography
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The tumors were divided into two groups according to tumor size (>2 cm:
45 tumors; <2 cm: 48 tumors). Compared with power Doppler sonography,
additional vascularity was detected on CO2-enhanced sonography in
42 of 93 tumors (15 tumors > 2 cm, and 27 < 2 cm). The results are
summarized in Table 3. The
major discrepancy between these two examinations was in the detection of small
hemangiomas, with superior vascularity on CO2-enhanced sonography
in 17 (74%) of 23 small hemangiomas (p<0.05, Fisher's exact
test).
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TABLE 3 Comparison of CO2-Enhanced Sonography (CO2S) and
Power Doppler Sonography (PDS) for Assessing Tumor Vascularity According to
Tumor Size
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Four types of flow pattern were detected on power Doppler sonography:
peripheral vessels, intratumoral vessels, peripheral spots, and intratumoral
spots (Fig.
5A,5B,5C,5D).
Some tumors showed mixed or negative signals. One hemangioma showed a diffuse
homogeneous pattern. The flow patterns of the hepatocellular carcinomas,
treated hepatocellular carcinomas, and hemangiomas are summarized in
Table 4. Most (26; 68%) of the
38 hemangiomas showed peripheral spots. Fifteen (52%) of the 29 hepatocellular
carcinomas showed intratumoral vessels. Ten (38%) of the 26 treated
hepatocellular carcinomas were hypovascular. Most of the signals seen on power
Doppler sonography were also seen on CO2-enhanced sonography except
for one hemangioma and two hepatocellular carcinomas
(Table 1).
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TABLE 4 Pattern of Vascular Depiction on Power Doppler Sonography (PDS) and
Early-Phase CO2-Enhanced Sonography (CO2S)
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On CO2-enhanced sonography, all but two hemangiomas showed
peripheral spots in the early arterial phase and centripetal fill-in during
the late phase. The remaining two tumors showed homogeneous enhancement in the
early and late phases. All tumors were monitored with CO2-enhanced
sonography for 30 min. Delayed washout (a duration of enhancement > 30 min)
was noted in all hemangiomas. Peripheral spotty enhancement was seen in only
three of 26 treated hepatocellular carcinomas. None of the hepatocellular
carcinomas showed this pattern before treatment. None of the hepatocellular
carcinomas and treated hepatocellular carcinomas showed delayed washout. The
washout time for these two groups ranged from 10 to 15 min.
Discussion
Power Doppler sonography has several advantages over color Doppler
sonography. In power Doppler sonography, the background noise is of uniformly
low power. Power Doppler sonography can be performed with higher gains than
color Doppler sonography. Power Doppler sonography is much less
angle-dependent and is not subject to aliasing
[2]. Most studies have
concluded that power Doppler sonography is superior to color Doppler
sonography in the depiction of vascularity in many organs and tumors
[12,13,14,15].
The difficulty in using power Doppler sonography is that it is much more
susceptible to motion artifacts
[12]; sometimes it is
difficult to determine whether the color signal is inside the tumor.
CO2-enhanced sonography was first reported in 1986
[16]. Other researchers have
used the microbubble method, or the direct gas method. In our study, the
direct gas method was used because the enhancement is more obvious.
CO2 sonography is a good modality for detecting tumor vascularity,
with a sensitivity of 90-100%
[3,
17]. Previous studies have
shown it to be better at depicting vascularity than angiography, CT, and CT
with iodized oil [6].
CO2-enhanced sonography has been shown to be useful both in
differential diagnosis [3,
18] and in determining tumor
viability [8]. However,
CO2-enhanced sonography is performed through an intraarterial
catheter into the hepatic artery, and its invasive character limits its
usefulness.
Because CO2-enhanced sonography is a valuable tool in detecting
tumor vascularity [3,
6,
17], it could be regarded as a
good reference for power Doppler sonography analysis. In our study, we found
that 52% of all 93 tumors depicted the same degree of tumor vascularity on
both power Doppler sonography and CO2-enhanced sonography. Nearly
all vascularity seen on power Doppler sonography was also noted on
CO2-enhanced sonography except in three tumors (two hepatocellular
carcinomas and one hemangioma). In these two hepatocellular carcinomas, the
additional vascularities were the result of venous flow. The hemangioma was
located in the left medial segment near major vessels. It showed a diffuse
homogeneous pattern on power Doppler sonography but peripheral spotted
enhancement on CO2-enhanced sonography, whereas angiography showed
similar results to CO2-enhanced sonography. Angiography also showed
hypovascularity in these two hepatocellular carcinomas.
CO2-enhanced sonography was superior to power Doppler sonography in
showing arterial flow, but it was inferior to power Doppler sonography in
revealing venous blood flow, which might explain why no difference was seen in
the visualization of vascularity of hepatocellular carcinomas using the two
techniques. The vascularity noted in power Doppler sonography might have been
due to flashing artifacts.
Other studies have shown that power Doppler sonography is superior to color
Doppler sonography in showing the vascularity of hemangiomas
[18,
19]. However, it is still
uncertain whether all the signals displayed by power Doppler sonography are
caused by true flow [15]. In
our study, when power Doppler sonography was compared with
CO2-enhanced sonography in 38 hemangiomas, only one tumor showed a
flashing artifact. These results indicate that most (97%) of the signals
detected on power Doppler sonography are accurately depicted on
CO2-enhanced sonography. In addition, CO2-enhanced
sonography was superior to power Doppler sonography in approximately 58% of
cases in this study. The vascularity of hemangiomas on CO2-enhanced
sonography was similar to that observed on angiography, with approximately
97.6% of the vascularity seen on CO2-enhanced sonography also seen
using angiography. This finding suggests that most of the signals displayed by
power Doppler sonography are true signals if the study is properly performed.
Our results indicate that CO2-enhanced sonography is superior to
power Doppler sonography in detecting the vascularity of hemangiomas.
The accurate depiction of tumor vascularity is extremely important in the
treatment of hepatocellular carcinomas. The appearance of vascularity in a
treated tumor indicates that the tumor is still viable
[8]. We evaluated 26 treated
hepatocellular carcinomas and found that 15 showed the same degree of vascular
depiction under both power Doppler sonography and CO2-enhanced
sonography. Among the remaining 11 tumors, six showed hypervascularity on
CO2-enhanced sonography but hypovascularity on power Doppler
sonography. The other five showed hypervascularity on both power Doppler
sonography and CO2-enhanced sonography, but CO2-enhanced
sonography depicted more vascularity than power Doppler sonography in these
five tumors. Although only 58% of tumors showed the same degree of vascularity
on power Doppler sonography and CO2-enhanced sonography, power
Doppler sonography identified 77% of hypervascularity identified by
CO2-enhanced sonography in treated hepatocellular carcinomas. The
results of angiography for treated hepatocellular carcinomas was similar to
the results seen on power Doppler sonography. However, iodized oil CT, dynamic
CT, and other follow-up studies showed that the tumors with discrepant results
between power Doppler sonography and CO2-enhanced sonography were
viable. Other researchers have also found that angiography is inferior to
CO2-enhanced sonography in revealing tumor vascularity
[6,
7], especially in treated
hepatocellular carcinoma [8].
The sensitivity of power Doppler sonography is not equal to that of the
invasive CO2-enhanced sonography. However, when only the
hypervascular and hypovascular rates were compared instead of the degree of
tumor vascularity, 78.5% of all tumors in this study displayed the same
results regardless of the method used.
CO2-enhanced sonography was better than power Doppler sonography
for the detection of tumor vascularity in 45% of our tumors. However, because
CO2-enhanced sonography is an invasive study, it cannot be used
routinely. For this reason, the role of power Doppler sonography in revealing
tumor vascularity and viability remains important in routine follow-up.
Further therapy might be indicated for tumors with positive power Doppler
sonography signals, whereas tumors with negative power Doppler sonography
signals would require further evaluation.
We also compared the difference between power Doppler sonography and
CO2-enhanced sonography in tumors greater than and those less than
2 cm and found a statistically significant difference in hemangiomas. Most of
the tumors with inferior signals on power Doppler sonography were small (<2
cm) hemangiomas, which might have been a result of the low flow velocity in
hemangiomas. CO2-enhanced sonography was superior to power Doppler
sonography in the slow-flow areas.
The vascular patterns of all the tumors were also recorded in this study.
Most hemangiomas (68%) showed peripheral spots on power Doppler sonography.
For untreated tumors, this peripheral spotted pattern was seen exclusively in
hemangiomas. Most hepatocellular carcinomas (65.5%) showed intratumoral or
peripheral vessels. The intratumoral or peripheral vessel pattern was not seen
in hemangiomas. The different flow pattern between hemangiomas and
hepatocellular carcinomas may have been the result of differences in vascular
patterns of these tumors and the slow flow of the hemangiomas
[20]. Power Doppler sonography
might be helpful in differentiating hepatocellular carcinomas and
hemangiomas.
Nearly all hemangiomas showed peripheral spots and the fill-in phenomenon
on CO2-enhanced sonography. Only two small lesions showed
homogeneous enhancement through the early and late phases. All tumors showed
delayed washout. These features were not identified in the other two groups.
These findings indicate that CO2-enhanced sonography is valuable in
diagnosing hemangiomas
[10].
In summary, CO2-enhanced sonography was superior to power
Doppler sonography in depicting vascularity in treated hepatocellular
carcinomas and in hemangiomas, especially small hemangiomas. However, no
significant difference was found between these two methods in evaluating
hepatocellular carcinoma. Power Doppler sonography has certain advantages,
including noninvasiveness and ease of use in daily practice. Most vascular
signals on power Doppler sonography in our study were true signals except for
the flashing artifact noted near the major vessels in a hemangioma. Our
findings suggest that power Doppler sonography is a useful imaging modality
for screening tumor vascularity and hepatocellular carcinoma viability after
treatment and in routine screening and follow-up of hepatocellular carcinoma
patients.
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Abstract
Introduction
