735

Differential Diagnosis of Hepatic

Tumors (Hepatoma, Hemangioma,
and Metastasis) with CT: Value of
Two-Phase Incremental Imaging

Hiroshi Honda1 Two-phase dynamic incremental CT is a technique in which CT scans are obtained
Yasuo Matsuura1 45 sec and 6 mm after commencing the rapid bolus injection of contrast medium. We
Hideo Onitsuka1 analyzed the contrast enhancement patterns of three types of hepatic tumors (72
Junji MurakamF hepatomas, 39 hemangiomas, and 28 metastases) in 139 patients to determine if any
American Journal of Roentgenology 1992.159:735-740.

Kuniuki Kaneko1 differences in the patterns are useful in the differential diagnosis of these lesions.
I Dynamic incremental CT scanning was performed after 100 ml of iodinated contrast
Sadayuki Murayama material was administered IV with a power injector at a rate of 2 mI/sec. A 1-sec
Takashi Kanematsu scanning time was used with a 1.6-sec interscan delay, which allowed table motion
KoujI Masuda1 between scans. CT scans (eight to 16 sections) were obtained 45-110 sec (early phase)
and 6-7 mm (delayed phase) after commencing the injection of contrast medium. The
enhancement patterns of hepatomas were as follows: 32% were totally hyperdense in
the early phase and totally hypodense in the delayed phase, while 24% were totally
hypodense in both phases. Most of the hepatomas (88%) appeared as totally hypodense
lesions in the delayed phase. In the case of hemangiomas, 56% were peripherally
hyperdense in the early phase; in the delayed phase, 36% were isodense and 31% were
totally hyperdense. Most hemangiomas (85%) were not totally hypodense in the early
phase, and no hemangioma was totally hypodense in both phases. In the early phase,
61% of metastases were hypodense. In the delayed phase, 57% were hypodense.
Metastases most commonly were totally hypodense in both phases (43%).
We conclude that contrast enhancement patterns of hepatomas, hemangiomas, and
metastases seen on two-phase dynamic incremental CT scans are useful in the differ-
ential diagnosis of these tumors.

AJR 159:735-740, October 1992

Dynamic incremental CT of the liver, in conjunction with bolus intravascular

administration of contrast medium, is useful in the diagnosis of liver diseases [1 2]. ,

Focal hepatic lesions have several distinct patterns on contrast-enhanced CT scans

[3]. Differences in attenuation and enhancement reflect the tumors vascularity,
size, and histology [4]. Despite these differences, several investigators have
reported overall improvement in lesion-to-liver contrast when CT is performed
within 2-3 mm after administering a bolus of contrast medium [5-7]. With recent
improvement in CT equipment, eight to 16 sections with table incrementations are
easily obtained during one suspended respiration. In addition to this dynamic
incremental scanning with bolus injection, delayed CT images can be obtained to
Received July 11 , 1991 ; accepted after revision detect and define hepatic tumors.
March 23, 1992. The purpose of this study was to compare the appearances of hepatomas,
1 Ipartment of Radiology, Faculty of Medicine, hemangiomas and metastases on dynamic incremental CT scans to determine the
Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fu- . . . . . . .

kuoka 812, Japan. Address reprint requests to H. value of thIs technique n the dIfferential diagnosis of these lesions.
Honda.
2 Department of Surgery II, Faculty of Medicine, Materials and Methods
Kyushu University, Fukuoka 812, Japan.
0361-803X/92/1594-0735 We reviewed 1 1 50 CT scans ofthe liver from 890 patients who had two-phase incremental
CAmerican Roentgen Ray Society CT scanning between July 1989 and December 1990. Of these patients, 139 had clinically or
 736 HONDA ET AL. AJR:159, October 1992

TABLE 1: Number of Tumors of Each Histologic Type by Tumor patients with hemangiomas, and 1 2 of the 28 patients with metas-
Size tacos were men.
Contiguous axial 1-cm-thick sections were obtained by using a
Tumo r Diamete r (cm)
Histologic Type Total Toshiba TCT-900S scanner (Tokyo, Japan). Dynamic incremental
s2 2-4 >4 scanning was performed after 100 ml of iopamidol (61 .2% iodine,
300 mg I/mI) was administered at 2 mI/sec with a power injector. In
Hepatoma 23 25 24 72
Hemangioma 21 11 7 39 the early phase, scanning was begun 45 sec after commencing the
Metastasis 4 12 12 28 injection. A 1-sec scanning time was used with a 1 .6-sec interscan
delay, which allowed table motion between scans. Eight to 16 scans
Total 48 48 43 139
were obtained in suspended respiration during 20-40 sec. Oxygen
inhalation was used when necessary in five patients. When scans of
the entire liver could not be obtained during the initial suspended
respiration, additional scans were obtained after 10-1 5 sec of respi-
histopathologically diagnosed hepatic tumors that were seen on early- rations. In the delayed phase, scanning was begun 6 mm after the
or delayed-phase images or both. Seventy-two patients had hepato- contrast medium was administered by using the same technique as
mas, 39 had hemangiomas, and 28 had metastases from various with the early-phase images.
primary malignant tumors. The sizes of tumors as measured on CT The two-phase images were retrospectively reviewed. The CT
scans were 2 cm or less (48 patients), 2-4 cm (48 patients), or more appearances of each tumor on each of the phased images were
than 4 cm (43 patients) (Table 1). categorized in five groups according to the degree and pattem of
of the 72 patients with hepatomas, histologic proof of the lesion enhancement in comparison with surrounding hepatic parenchyma
was obtained during surgery in 46, by direct biopsy in 21 and at ,
(Fig. 1): totally hyperdense, peripherally hyperdense, centrally hyper-
autopsy in five. In the 39 patients with hemangiomas, five cases were dense, mixed density, totally isodense (undetected), and totally hy-
proved by surgery and 34 were proved by sonography, MR imaging, podense. When more than one tumor was present, the largest ones
American Journal of Roentgenology 1992.159:735-740.

angiography, and clinical follow-ups of at least 1 year. Of the 28 were selected for evaluation because they were the ones most
patients with hepatic metastases, nine cases were proved at surgery frequently present in biopsy samples.
and five were proved by direct biopsies. Fourteen cases were diag- Angiographic findings in 39 hepatomas also were studied to clarify
nosed because the patients had histories of primary malignant tu- the characteristic CT findings. Angiography was performed via the
mors, abnormal serologic laboratory findings such as carcinoem- celiac artery and selectively via the right or left hepatic artery by using
bryonic antigen for colonic carcinoma, and serial radiographic findings iopamidol injection rates of 7 mI/sec and 3-4 mI/sec. respectively.
that showed progressive enlargement of the lesions. The most oem-
mon sites of origin of metastases were carcinomas of the colon and
rectum (1 2 cases). Other primary malignant neoplasms were carci- Results
nomas of the stomach (seven cases); gallbladder (two cases); and
Table 2 shows the enhancement patterns of each of the
kidney, lung, ovary, hypopharynx, pancreas, and esophagus (one
case each). One metastasis was from gastnnoma of the pancreas. tumors on the early- and delayed-phase images. Among 29
The patients with hepatomas were 33-84 years old (mean, 61 tumors that appeared to be totally hyperdense in the early
years), those with hemangiomas were 34-71 years old (mean, 52 phase, 25 (86%) were hepatomas. The single metastasis that
years), and those with metastases were 43-82 years old (mean, 57 was totally hyperdense in the early phase was from a gastri-
years). Fifty-six of the 72 patients with hepatomas, 20 of the 39 noma. Of 25 tumors that appeared to be totally hyperdense

0 1) 0
A B C

0
Fig. 1.-Various enhancement patterns of
tumors: totally hyperdense (A), peripherally hy-
D E F perdense (B), centrally hyperdense (C), mixed
density (D), totally isodense (E), and totally hy-
podense (F).
 AJR:159, October 1992 TWO-PHASE CT OF HEPATIC TUMORS 737

TABLE 2: Enhancement Pattern of Each Tumor on Two-Phase mixed density in six (8%), and peripheral hyperdensity in five
Images
(7%). In the delayed phase, total hypodensity was the most
N o. of Findings (%) common pattern, seen in 63 cases (88%), followed by total
isodensity in six (8%), total hyperdensity in one (1 %), central
Phase/Pattern Hepatomas Hemangiomas Metastases
hyperdensity in one (1 %), and mixed density in one (1 %). No
(n = 72) (n = 39) (n = 28)
hepatoma appeared to have peripheral hyperdensity in the
Early
delayed phase. Total hyperdensity in the early phase and total
Totally hyperdense 25 (35) 3 (8) 1 (4)
Peripherally hyperdense 5 (7) 22 (56) 8 (29) hypodensity in the delayed phase were the most common
Centrally hyperdense 7 (1 0) 5 (1 3) 0 appearances in hepatomas (Fig. 2), seen in 23 (32%) of 72
Mixed density 6 (8) 2 (5) 1 (4) cases, followed by total hypodensity in both phases in 17
Totally isodense 9 (1 3) 1 (3) 1 (4) (24%). Ten (59%) of 1 7 hepatomas that appeared to have
Totally hypodense 20 (28) 6 (1 5) 17 (61)
total hypodensity in both phases were 2 cm or less in diam-
Delayed eter, but only four (1 7%) of 23 hepatomas that appeared to
Totally hyperdense 1 (1) 12 (31) 0
Peripherally hyperdense 0 7 (1 8) 3 (11)
be totally hyperdense in the early phase and totally hypodense
Centrally hyperdense 1 (1) 0 2 (7) in the delayed phase were 2 cm or less in diameter. Forty-
Mixed density 1 (1 ) 4 (10) 1 (4) three (60%) of 72 hepatomas enhanced totally or partially in
Totally isodense 6 (8) 14 (36) 6 (21) the early phase (totally hyperdense, peripherally hyperdense,
Totally hypodense 63 (88) 2 (5) 16 (57) centrally hyperdense, and mixed density). Thirty-seven (51%)
of 72 hepatomas enhanced totally or partially in the early
phase and showed total hypodensity in the delayed phase.
in the early phase and totally hypodense in the delayed phase, In the 39 hemangiomas, peripheral hyperdensity was the
American Journal of Roentgenology 1992.159:735-740.

23 (92%) were hepatomas. Twenty-two (63%) of 35 tumors most common pattern in the early phase, seen in 22 (56%) of
that were peripherally hyperdense on the early-phase images 39 cases, followed by total hypodensity in six (1 5%), central
were hemangiomas. However, seven tumors that were pa- hyperdensity in five (1 3%), total hyperdensity in three (8%),
ripherally hyperdense in the early phase and totally hypodense mixed density in two (5%), and total isodensity in one (3%).
in the delayed phase were not hemangiomas. Of the 11 In the delayed phase, total isodensity was the most common
tumors that appeared to be totally isodense in the early phase, pattern, seen in 14 (36%) of 39 hemangiomas, followed by
nine (82%) were hepatomas, one was a hemangioma, and total hyperdensity in 1 2 (31 %), peripheral hyperdensity in
one was a metastasis. Of the 26 tumors that appeared to be seven (18%), mixed density in four (10%), and total hypo-
totally isodense in the delayed phase, six (23%) were hepa- density in two (5%). The pattern of central hyperdensity was
tomas, 1 4 (54%) were hemangiomas, and six (23%) were not seen in any hemangioma on delayed-phase scans.
metastases. Nine tumors (100%) that appeared to be totally In the 28 metastases, total hypodensity was the most
isodense in the early phase and totally hypodense in the common pattern in the early phase, seen in 17 (61 %) of 28
delayed phase were hepatomas. Of the 13 tumors that ap- cases, followed by peripheral hyperdensity in eight (29%),
peared to be totally hyperdense in the delayed phase, 12 total hyperdensity in one (4%), mixed density in one (4%),
(92%) were hemangiomas. and total isodensity in one (4%). No metastases had central
In the 72 hepatomas, total hyperdensity was the most hyperdensity in the early phase. In the delayed phase, total
common pattern in the early phase, seen in 25 (35%) of 72 hypodensity was the most common pattern, seen in 16(57%)
cases, followed by total hypodensity in 20 (28%), total iso- of 28 metastases, followed by total isodensity in six (21 %),
density in nine (1 3%), central hyperdensity in seven (10%), peripheral hyperdensity in three (1 1 %), central hyperdensity

Fig. 2.-64-year-old man with hepatoma.

A, Early-phase incremental CT scan shows 4-
cm-diameter hepatcma to be totally hyperdense.
B, Delayed-phase incremental CT scan
shows tumor to be totally hypodense.
 738 HONDA ET AL. AJR:159, October 1992

in two (7%), and mixed density in one (4%). No metastases ment on celiac angiograms were more than 4.5 cm in diame-
showed total hyperdensity on delayed-phase images. Al- ter. Angiograms were available for review in 22 of the 23
though total hypodensity in both phases was the most com- hepatomas that were totally hyperdense on early-phase CT
mon appearance of metastases (1 2/28, 43%) (Fig. 3), 24% scans and totally hypodense on delayed-phase CT scans.
(1 7/72) of hepatomas also had that pattern in both phases Twenty (91 %) of the 22 hepatomas enhanced on celiac
(Fig. 4). angiograms. Three of these were more than 4.5 cm in diam-
In the early phase, 8% of all tumors (1 1/139) were totally eter. Another two enhanced on angiograms ofthe right branch
isodense and in the delayed phase, 19% (26/1 39) were totally of the proper hepatic artery.
isodense. Nine (1 3%) of 72 hepatomas, one (3%) of 39
hemangiomas, and one (4%) of 28 metastases were totally
isodense in the early phase and seen only in the delayed Discussion
phase (Fig. 5). Six (8%) of 72 hepatomas, 14 (36%) of 39
hemangiomas, and six (21 %) of 28 metastases were totally The evolution of techniques for contrast enhancement with
isodense in the delayed phase. CT has paralleled improvement in CT technology. As rapid
Angiograms of hepatomas that showed the patterns of CT scanning with scanning rates of eight to 1 6 scans per
total hyperdensity on early-phase CT scans and total hypo- suspended respiration became possible, the rate of injection
density on delayed-phase CT scans were compared with of contrast medium was increased. In this study, early-phase
angiograms of hepatomas that showed total hypodensity in scanning was started 45 sec after the beginning of injection,
both phases. Fifteen (88%) of 17 hepatomas that were totally as described previously [8]. Within 5 mm after bolus injection,
hypodense in both phases did not enhance on celiac angiog- 80% of contrast material has already escaped from the vas-
raphy and 10 (59%) did not enhance even with selective cular space into the interstitial space [9]. Equilibrium between
American Journal of Roentgenology 1992.159:735-740.

angiography of the right or left branch of the proper hepatic the two spaces is attained within 2-5 mm [7, 9, 10]. In this
artery. Another two hepatomas (12%) that showed enhance- study, 50 sec was needed to inject 1 00 ml of contrast material.

Fig. 3.-58-year-old man with metastatic tu-

mor from colonic carcinoma.
A and B, Early- (A) and delayed- (B) phase
incremental CT scans show 4-cm-diameter me-
tastasis to be totally hypodense.

Fig. 4.-68-year-old woman with hepatoma.

A and B, Early- (A) and delayed- (B) phase
incremental CT scans show 7-cm-diameter hep-
atoma to be totally hypodense.

A B
 AJR:159, October 1992 TWO-PHASE CT OF HEPATIC TUMORS 739

Fig. 5.-56-year-old man with hepatoma.

A, Early-phase incremental CT scan shows 2-
cm-diameter hepatoma to be totally Isodense
(undetectable).
B, Delayed-phase incremental CT scan shows
hepatoma as totally hypodense (arrow). -- .- L #{149}.-#{149} #{149}:

[rJT:::b 4:-

/
1 k...
ii .- -

Accordingly, the delayed-phase images were obtained 6 mm less vascular than the hepatomas that are totally hyperdense
after the injection was started. in the early phase and totally hypodense in the delayed phase.
Hepatomas are known to enhance in proportion to the Even when the hepatomas were hypervascular and enhanced
American Journal of Roentgenology 1992.159:735-740.

degree of uptake of contrast medium, and because of their on celiac angiograms, CT showed two relatively large hepa-
hypervascular nature, they enhance earlier than the surround- tomas as totally hypodense in both phases. This may be
ing hepatic parenchyma does. Metastases, especially those because of the smaller volume of contrast material that flows
from adenocarcinomas of the gastrointestinal tract, usually into the hepatoma during CT than during angiography. During
enhance less and take up contrast material more slowly [5, the early phase (45-90 sec after initiation of the contrast
6, 1 1 1 2]. After the administration
, of iodinated contrast injection), the hepatic parenchyma is enhanced by portal blood
material as a bolus injection, dynamic CT scanning results in flow. If the tumor is not appreciably enhanced because the
improved delineation of tumor vascularity, venous shunting, volume of contrast material is less than the necessary volume
venous occlusion, and hepatic lobar or segmental flow ab- to enhance the hepatoma more than hepatic parenchyma, the
normalities [2, 1 3-1 7]. Hepatomas, supplied by hepatic arte- tumor may appear less dense than the hepatic parenchyma.
rial branches, become maximally hyperdense during the ar- After IV administration of contrast material, all or part of
terial phases of dynamic scanning sequences, then rapidly the rim of hemangiomas shows an increase in density on CT,
become less dense as portal flow to the liver becomes dom- exceeding the enhancement of the normal liver. Delayed CT
inant [8, 18, 1 9]. This pattern is well seen on dynamic incre- scans reveal progressive contrast enhancement of the central
mental CT and delayed-phase CT scans of hepatomas. On parts of the hemangioma owing to the gradual accumulation
the early-phase images in our study, 35% of hepatomas and slow washout of contrast material [23]. Hepatic heman-
enhanced totally and 25% enhanced partially (total, 60%). In giomas are best distinguished from other solid hepatic masses
the delayed phase, 88% were less dense than the surrounding by administering contrast material and by performing dynamic
hepatic parenchyma. CT scanning with delayed scans at 1-4 mm [24]. Although
However, 26% of hepatomas were less dense than hepatic the peripherally hyperdense pattern was seen in the early
parenchyma in both phases. Fifty-nine percent of the hepa- phase and various patterns were seen in the delayed phase,
tomas that were hypodense in the early phase were not seen the peripheral hyperdensity in the early phase was seen in
even with selective angiography. Tumors not seen on angio- less than 60% of hemangiomas, as has been reported [25].
grams are characterized as being smaller than 2 cm and well The high percentage (36%) of hemangiomas that were Un-
differentiated, and as having fatty metamorphosis, severe detected in the delayed phase reinforces the advantage of
liver cirrhosis, or necrosis [20-22]. These pathologic charac- using bolus injections and incremental CT. The lower density
teristics might cause the poor enhancement on early-phase of the tumor relative to the surrounding hepatic parenchyma
images and poor visibility on angiograms. The hepatomas in both phases strongly suggests that such a tumor is not a
that were totally hypodense in both phases were more often hemangioma.
(59%) small (<2 cm) than were the hepatomas that were Most secondary tumors of the liver are hypovascular. Among
totally hyperdense in the early phase and totally hypodense the primary neoplasms that tend to give rise to hypervascular
in the delayed phase (1 7%). Most of the hepatomas that were metastases are carcinoids; leiomyosarcomas; choriocarcino-
totally hypodense in both phases did not enhance on celiac mas; and carcinomas of renal, thyroid, adrenal, and pancreatic
angiography, while more than 90% of the hepatomas that islet cell origins. Some metastatic melanomas and occasional
were totally hyperdense in the early phase and totally hypo- metastases from carcinomas of the colon and breast also are
dense in the delayed phase did enhance. This was because hypervascular. In our study, the metastasis from the gastri-
the hepatomas that are totally hypodense in both phases are noma had totally hyperdense and totally hypodense patterns
 740 HONDA ET AL. AJA:159, October 1992

similar to those of hepatomas. In cases of hypervascular vs. infusion.AJR 1981;137:351-358

8. Foley WD. Dynamic hepatic 1989;170:617-622
CT. Radiology
malignant tumors in other organs, biopsy is necessary. One
9. Kormano M, Dean PB. Extravascular contrast material: the major compo-
of the common patterns of metastasis identified with CT after nent of contrast enhancement. Radiology 1976;121 :379-382
a bolus injection of contrast material is a rim of contrast 10. ltai Y, Ohtomo K, Kokubo T, et al. CT of hepatic masses: significance of
enhancement around a less dense central zone. This report- prolonged and delayed enhancement. AJR 1986;146:729-733
1 1 . Sager EM, Scheel B, Talle K. Increased detectability of liver metastases
edly occurs in 35% of these lesions [26]. In our study, rim
by the use of contrast enhancement in computed tomography: a compar-
enhancement was seen as peripheral hyperdensity in the early ison between the precontrast, the immediate postcontrast and the one
phase with similar frequency (29%). The metastases could be hour postcontrast scan. Acta Radio! 1985;26:369-372
detected more readily in the early phase (96%) than in the 12. Dean PB, Violante MA, Mahoney JA. Hepatic CT contrast enhancement:
delayed phase (79%). However, because the variety of met- effect of dose, duration of infusion, and time elapsed following infusion.
Invest Radiol 1980;15:158-161
astatic origins was limited in this study, more study of hepatic 13. Tada S, Fukuda K, Aoyagi Y, Harada J. CT of abdominal malignancies:
metastases might be necessary. dynamic approach. AJR 1980;1 35:455-461
In summary, delayed images assisted in the detection of 14. Inamoto K, Sugiki K, Yamasaki H, Miura T. CT of hepatoma: effects of
8% of all tumors and 13% of hepatomas. A lesion that is portal vein obstruction. AJR 1981;136:349-353
1 5. Pauls CH. Ultrasound and computed tomographic demonstration of portal
totally hyperdense or totally isodense on early-phase images
vein thrombosis in hepatocellular carcinoma. Gastrointest Radio!
and totally isodense on delayed-phase images is almost al- 1981;6:281 -283
ways a hepatoma. Even if a lesion showed peripheral hyper- 16. Nishikawa J, ltai Y, Tasaka A. Lobar attenuation differences of the liver on
density in the early phase, total hypodensity in the delayed computed tomography. Radiology 1981;141 :725-728
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lobar or segmental distribution detected by dynamic computed tomogra-
We conclude that, although bolus injection with incremental
phy. Radiology 1982;144:835-839
CT scanning is known to be useful for the quantitative diag- 18. Hosoki T, Chatani M, Mon S. Dynamic computed tomography of hepato-
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tumors. Dynamic CT of hepatic masses with intravenous and intraarterial contrast
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20. Takayasu K, Shima Y, Muramatsu Y, et al. Angiography of small hepato-
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