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509

Color Liver

Doppler Tumors

Flow

Imaging

of

.

Sachiko Tanaka1 Tsugio Kitamura Makoto Fujita Katsumi Nakanishi Shi”eru Okuda

A differential

diagnosis

.

of liver tumors was attempted on the basis of the pattern of on color Doppler flow images. The study comprised

blood flow within and around tumors patients

with liver mass

lesions:

20 patients

had hepatocellular

carcinoma,

six had

hemangiomas, four had metastatic liver cancers, one had cholangiocellular carcinoma, had focal fatty liver, and three had liver cysts. A basket pattern (a fine blood-flow network surrounding the tumor nodule) was observed in 15 (75%) of the 20 hepatocellular carcinomas. An image of vessels within the tumor (blood flow that runs into and branches within the tumor) was observed in 13 (65%) of the 20 hepatocellular carcinomas. These two findings were observed only in hepatocellular carcinomas; even when the

tumor

In the

was

patients

smaller with

than

multiple

2 cm

meandering around the tumor a “spot” pattern (color-stained seen. Our

experience

pearance AJR

suggests

on color Doppler 154:509-514,

March

in diameter,

these

findings

that

metastases,

a “detour”

hepatocellular

carcinomas

were

observed

frequently.

pattern (a dilated portal vein nodules) was observed. In three of the six hemangiomas, dots or patches in the central region of the tumor) was

hepatic

have

a characteristic

ap-

flow images. 1990

The diagnostic accuracy of sonography for hepatocellular carcinoma has been well established [i 2]. Moreover, a close correlation has been shown between the sonographic image of hepatocellular carcinoma and its microscopic features [3]. Furthermore, sonographically guided percutaneous biopsy permits diagnosis of some small tumors that cannot be visualized by angiography [4]. At present, however, angiography is generally recognized as being second to histologic diagnosis as the method for final diagnosis of hepatocellular carcinoma. If both the tumor image and blood-flow image could be displayed on a single sonogram by using color Doppler flow imaging, it would be possible simultaneously to obtain information that can be gained with sonography, hepatic arteriography, hepatic venography, and portography. This would be extremely useful in the differential diagnosis of hepatic tumors. However, according to published reports [5, 6], color Doppler flow imaging has not been able to provide information comparable to that obtained by using angiography because the color display of ,

Received July 18, 1989; accepted September 19, 1989. This work was supported aid for Cancer

Research

(63-1)

after revision

slow

blood

flow on Doppler imaging is inadequate. color Doppler equipment capable of displaying relatively slow blood flow was used, and the differential diagnosis of liver tumors was made on the basis of the color blood-flow pattern within and around the tumor. In this study,

in part by a grant-infrom the Ministry of

Health and Welfare of Japan. ,

All authors:

The

Center

for

Adult

Diseases,

Osaka, 3-3, Nakamichi, 1 -chome, Higashinari-ku. Osaka 537, Japan. Address reprint requests to S. Tanaka. .

Subjects

0361-803X/90/1543-0509 © American Roentgen

sonography. These six hemangiomas,

Ray Society

and Methods

The study

comprised

35 patients

included 20 four metastatic

in whom

masses

in the liver were

hepatocellular carcinomas liver cancers (two from

(encapsulated the stomach

confirmed

by routine

type in all cases), and two from the

:

TANAKA

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5i0

Fig. 1.-Basket

pattern

ET AL.

AJR:1 54, March 1990

in hepatocellular carcinomas. show blood flow surrounding mass (A and B) and in a prominent

A-C, Color Doppler flow images tumor (arrows, C).

.

..

It

.

2.

-

net-shaped

pattern

slightly

removed

from center

of

.

-.

,

.-

Fig. 2.-Small

hepatocellular

carcinoma.

A, Sonogram shows hypoechoic 1.3-cm lesion. B and C, Color Doppler flow images show pulsating blood two directions and surrounds tumor nodule (basket pattern). shown (arrow). A

flow, which approaches lesion from Sampling point of pulsed wave is

COLOR

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AJR:1 54, March 1990

Fig. 3.-Hepatocellular

DOPPLER

OF

LIVER

5i i

TUMORS

carcinoma.

A and B, Color Doppler flow

images

show

basket pattern. Within abundant blood flow surrounding tumor nodule, one image shows pulsating

wave

pattern

(A); the other

exhIbits

a constant wave pattern (B). Sampling points of pulsed wave are shown (arrows). C, Hepatic angiogram shows that pulsating wave Is from a feeding artery supplied from anterior inferior branch of hepatic artery. 0, Portogram shows that constant wave pattern is anterior inferior branch of portal vein (arrows), which is dislocated by tumor mass. C

D

colon), one cholangiocellular carcinoma, one focal fatty liver, and three liver cysts. Histologic diagnosis was made, after sonographic examination, with tissues obtained by surgery or by sonographically guided

fine-needle

aspiration

biopsy

in 1 0 of the 20 cases

of hepa-

tocellular carcinoma, all four cases of metastatic cancer, and the one case of cholangiocellular carcinoma. Angiography was performed in all cases except those of focal fatty liver, liver cyst, and two of the four metastases. The final diagnosis was made with histologic examination and/or angiography in all cases except those of focal fatty liver and liver cyst, which were clinically diagnosed by using sonographic follow-up. The size of the tumor in the 20 hepatocellular

carcinoma cases ranged from 1 .0 to 7.0 cm in diameter. The equipment used was a Quantum angiodinography unit with 7.5- and 5.0-MHz linear-array probes (Quantum Medical Systems, lssaquah, WA) and an SSA-270A unit with 3.75-MHz sector-array probes (Toshiba, Tokyo, Japan). Because the minimal Doppler frequency shift capable of color imaging is 150 Hz with both machines, the slowest blood flow that theoretically can be shown in color is 1.5 cm/sec at 7.5 MHz, 2.3 cm/sec at 5.0 MHz, and 3 cm/sec at 3.75 MHz.

Results

Hepatocellular

Carcinoma

A basket pattern, that is, a fine blood-flow network surrounding the tumor nodule, was observed in i 5 (75%) of the 20 hepatocellular carcinoma cases. At the center of the tumor, blood flow was seen surrounding the periphery of the mass (Fig. i). In the region slightly removed from the center, abundant blood flow was observed in a net-shaped pattern. In this pattern, vessels cling to the tumor and develop many fine branches around or within the tumor nodule. This basket pattern was observed in all of the five hepatocellular Carcinomas smaller than 2 cm in diameter (Fig. 2). When the bloodflow wave pattern was examined, constant waves could be seen in all i5 cases; in i2 (80%), the blood flow also showed pulsating waves. In comparison, angiography showed these waves to be part of the feeding arteries surrounding the tumor and the portal vein running along the periphery of the tumor (Fig. 3).

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512

TANAKA

ET AL.

AJR:154,

March

1990

Fig. 4.-Vessels in tumor. A and B, Color Doppler images show blood flow running and branching within tumor in both relatively large (A) and small (B) hepatocellular carcinomas. Arrows delineate tumor lesions.

Fig. 5.-Hemangioma. A, Sonogram shows 3-cm mass (arrows) in livernear gallbladder (GB). B, Color Doppler flow image shows red spot in center of tumor. C and D, Hepatic angiograms show chdracteristic findings of hemangioma with extensive pooling in center of tumor.

An image of vessels within the tumor, that that runs into the tumor mass from the branches within the tumor, was observed in i 20 cases of hepatocellular carcinoma (Fig. 4). with routine sonography, it was evident with

is, blood flow periphery and 3 (65%) of the In comparison color Doppler

flow sonography that the vessels in the tumor ran along septa within the tumor. The blood flow within the tumor showed a pulsating wave pattern in all cases. Comparison with the angiogram suggested that this pattern represented tumor vessels.

Fig. 6.-Metastases with detour pattern. A, Sonogram shows multiple metastatic tumors. B, Color Doppler color flow image shows dilated intrahepatic portal vein meandering in liver.

Unlike basket pattern,

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to tumor

blood flow does not cling

but detours.

Fig. 7.-Solitary small metastatic lesion. A, Sonogram shows hypoechoic lesion (arrows) in left lobe of liver. B, Color Doppler flow image shows no blood flow within and around C, Parenchymal phase of hepatic artenogram shows tumor staining

tumor (arrows). (arrows).

In four of the 20 hepatocellular carcinoma cases, no blood flow could be seen near the tumor. Of these four cases, hypovascularity was also observed angiographically in one. In the remaining three cases, adequate color imaging could not be done, probably because the tumor was located too deep within the liver.

Hemangioma In three (50%) of the six cases of hemangioma, the bloodflow image showed a spot pattern, that is, dots or patches, in the central region of the tumor nodule (Fig. 5). In all three of these cases, comparatively extensive pooling was noted in the central region of the tumor on angiography.

Metastatic

Liver Cancer

Of the four cases of was observed in two another with a colon the liver. The portal

metastatic liver cancer, a detour pattern cases (one with a gastric primary and primary) with multiple tumor masses in vein within the liver was dilated and

meandered around the tumor nodules (Fig. 6). Unlike the basket pattern observed in hepatocellular carcinoma. a dilated portal vein did not develop branches to the tumor nodule, but detoured around the nodule and left the nodule without changing the diameter of the vessel. Each of the two cases in which a detour pattern was not observed had a single mass (i .3 and 2.5 cm in maximal diameter). Both masses were resected. Hepatic angiography in these two cases revealed no tumor vessels or feeding artery, but tumor staining was observed (Fig. 7). Other

Cases

In the

one

case

of cholangiocellular

carcinoma,

color

Dop-

pIer imaging could not visualize the blood flow within or around the tumor. This tumor was located deep within the liver, and even a routine B-mode image was unclear unless the far gain level was adjusted to a high setting. Hepatic angiography revealed a hypovascular tumor in this case. No blood flow could be observed in the case of focal fatty liver or the three cases of liver cyst.

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Basket

vessels

Pattern

Tumor

in

Spot

Detouring

Pattern

Pattern

due to arteriovenous shunting. In our study, we also observed a fast pulsating blood flow of 70-90 cm/sec in maximal velocity in feeding arteries entering the tumor, which form part of the basket pattern. Furthermore, in addition to the pulsating wave, a constant wave could be detected in the periphery in hepatocellular carcinoma. Comparing the blood flows shown on the color image with angiographic findings, we found

Fig. 8.-Schematic

pulsating

wave

constant

wave

of blood flow In liver tumors as shown

presentation

by color Doppler flow imaging.

Hepatic

Masses

A schematic presentation served in space-occupying Figure 8. The basket pattern the 20 cases of hepatocellular of vessels in the tumor was findings were not observed cancer,

or other

(50%) was

cases.

of the six cases seen

multiple

in metastatic

of the blood-flow patterns oblesions of the liver is shown in was observed in i 5 (75%) of carcinoma and the appearance seen in 1 3 cases (65%); these in hemangioma, metastatic liver

The

spot

pattern

of hemangioma, liver

cancers

was

seen

and the detour in which

there

in three

pattern were

masses.

Discussion Color Doppler flow imaging, developed by Namekawa et al. [7], was originally used to evaluate the dynamics of blood flow in the heart and large blood vessels. Its application to liver tumors was initiated in 1 985 by Sukigara et al. [5], who reported successful color imaging of the arteries running in the margin of and within the tumor in two cases of advanced hepatocellular carcinoma. Merritt [8] observed increased vascularity in most cases of metastatic liver cancer. However, there have been no reports in the literature on attempts to use color Doppler flow imaging in the differential diagnosis of various types of liver tumors. The results of our study suggest that the basket pattern and the appearance of vessels in the tumor are Characteristic color Doppler flow imaging patterns of hepatocellular carcinoma. These findings were observed in many hepatocellular carcinomas, but not in hemangiomas or metastatic liver cancers. Ueno et al. [6] reported that visualization of blood flow as a pulsating wave in the margin of or inside a tumor was characteristic of hepatocellular carcinoma. They also reported that hepatocellular carcinomas smaller than 2 cm in diameter showed no color Doppler blood flow. In our study, the basket pattern was observed in all of five hepatocellular carcinoma tumors smaller than 2 cm in diameter, and the vessels were visualized in the tumor in three of the five. The difference in findings presumably is due to the sensitivity of the equipment used for Doppler frequency shifts. Thus, even lower and finer blood flows probably could be visualized in color if adequate instruments are developed. Taylor et al. [9] reported that high-velocity Doppler signal was detected in hepatocellular carcinoma tumors when pulsed-wave Doppler sonography was used; they suggested that this signal was associated with large pressure gradients

that

the blood

flow

that

creates

the basket

pattern

is the portal vein displaced around mass lesions and feeding arteries surrounding tumor nodules. Also, the blood flow within the tumor displayed by color imaging is the pulsating tumor vessel running within the tumor. In small metastatic lesions in which tumor vessels cannot be observed by angiography and can be identified only by tumor staining at the parenchymal phase, color Doppler imaging of the blood flow was not possible. Merritt [8] reported that abundant blood flow was observed in most liver metastases; in our study, however, abundant portal blood flow was found running along the space between mass lesions only in cases with multiple tumor nodules. Proliferation of pulsating tumor vessels could not be detected in any cases. This is in agreement with the hepatic angiographic finding that most cases of liver metastases from adenocarcinoma are not hypervascular. In some hemangiomas, a spot pattern was observed in the central region of the tumor. This seems to coincide with the pooling observed in angiography. Ishida et al. [1 0] also reported that constant wave was recorded in the hypoechoic areas within hemangiomas. However, it is difficult to explain blood flow in the pooling site, and this should be pursued further. Color Doppler flow imaging provides information on blood flow that supplements the information gained by routine sonography, and thus is useful in the differential diagnosis of liver tumors. However, color imaging of blood flow was insufficient when the tumor was located deep within the liver. We look forward to further improvements in equipment so that we can achieve color imaging of much slower and finer blood flow and also image deep-seated tumors. REFERENCES

1 . Tanaka 5, Kitamura T, Ohshima A, et al. Diagnostic accuracy of ultrasonography for hepatocellular carcinoma. Cancer 1986;58:344-347 2. Tanaka 5, Kitamura T, Nakanishi K, Okuda 5, Kojima J, Fujimoto I. Recent advances in ultrasonographic diagnosis of hepatocellular carcinoma. Cancer 1989:63:1313-1317

3. Tanaka

S. Kitamura

T, lmaoka

5, Sasaki Y, Taniguchi

H, Ishiguro

S.

Hepatocellular carcinoma: sonographic and histologic correlation. AJR 1983;140:701 -707 4. Tanaka 5, Kitamura T, Kasugai H, Okano Y, Tatsuta M, Okuda S. Early diagnosis of hepatocellular carcinoma: usefulness of ultrasonically guided fine-needle aspiration biopsy. JCU 1986;14: 11-16 5. Sukigara M, Takamoto 5, Komazaki T, et al. Observation of the hepatoma

by the real-time two-dimensional echography: its clinical significance and prospect (English abstr). Acta Hepatol Jpn 1985;26:747-752 6. Ueno N, Yamanaka T, Kimura K. Visualization of blood flow in abdominal tumors by the ultrasonic pulsed Doppler method (English abstr). Nippon Shokakibyo Gakkai Zasshi 1989:86:1292-1298 7. Namekawa K, Kasai C, Tsukamoto M, Koyano A. Imaging of blood using autocorrelation. Ultrasound Med Biol 1982;8[suppl 1 ]: 138 8. Merritt CRB. Doppler color flow imaging. JcU 1987;15:591-597

flow

9. Taylor KJW, Ramos I, Morse 55, Fortune KL, Hammers L, Taylor CR. Focal liver masses: differential diagnosis with pulsed doppler US. Radiology 10.

1987;164:643-647 Ishida H, Morikava P. Nizawa M, Naganuma 5. Arakawa H, Masamune 0. L’apport du Doppler a emission puls#{233}e dans l’exploration des tumeurs du foie. JEMU 1988;178-185

Color Doppler flow imaging of liver tumors.

A differential diagnosis of liver tumors was attempted on the basis of the pattern of blood flow within and around tumors on color Doppler flow images...
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