Yukio Muramatsu, Tatsuya Yamada,

MD MD

#{149} Shigeru #{149} Susumu

Nawano, Yamasaki,

MD MD

#{149} Kenichi

Early Hepatocellular MR Imaging’ All areas in hepatic lesions designated as adenomatous hyperplasia (All) with malignant foci have recently been recognized as cancer. AH with malignant foci can be classified into two types, depending on the presence of overt cancerous nodules. Lesions without macroscopic nodules are defined as early hepatocellular carcinoma (HCC), while those with a macroscopic component are defined as HCC with early components. A comparative study of early HCC and HCC with early components was performed with magnetic resonance imaging. Early HCC lesions (n = 20) were isointense (n = 11) and hyperintense (n = 9) on Ti-weighted spinecho images and isointense (n = 17), partially hyperintense (n = 2), or hypointense (n = 1) on T2-weighted spin-echo images relative to the surrounding liver. Lesions classified as HCC with early components (n =8) were hyperintense (n = 5), isointense (n = 2), and of mixed signal intensity (n = 1) on T2-weighted images. Tiweighted imaging was superior to T2-weighted imaging in depicting early HCC, but the latter could be useful in evaluating the progression of HCC in the histopathologically early stages. Index

terms:

Liver,

neoplasms, plasms,

cirrhosis,

diagnosis, MR studies,

Radiology

1991;

761.321

761.794 Liver

#{149}

#{149} Liver neo-

O

to the progress in developof various kinds of diag-

WING

ment nostic

imaging

tocellubar

modalities,

chances nodular nodules,

of removing lesions such adenomatous

(All),

atypical

lignant

All,

Atypical

All

Departments

of Diagnostic

Radiol-

partment of Pathology, National Cancer Center Research Institute, Tokyo (S.H.). Received October 2, 1990; revision requested November 14; final revision received April 22, 1991; accepted April 30. Supported in part by a Grant-in-Aid for Cancer Research from the Ministry of Health © RSNA,

Address 1991

now

(1-5). This in the

other hepatic as regenerative hyperplasia and

foci from

hepa-

can

reprint

requests

to Y.M.

#{149} Noriyuki

Moriyama,

ing

structure

MD

the

AH

with

cirrhotic

is considered

ma-

liver. an

interme-

diate stage between benign and mabignant lesions. All with malignant foci is thought to be an early stage of HCC. Consensus about the histopathologic

significance

malignant

foci has

in Japan

(6,7).

phasized the

very

well

not

achieved

constitute

differentiated

cancer.

There-

fore, we foci into

classified All with two types, depending

whether a tumor

overt cancerous areas were macroscopically

a nodule, macroscopic

with

and

early

without

defined lesions tumor nodules

components gross

HCC. Along istics

lesions

nodules

clarifying

within seen as

with as HCC

and

tumor

with

of the

malignant on

as early

the character-

magnetic

resonance

(MR)

imaging appearance of these types of HCC, we also evaluated the relationship

between

signal

intensity

and

the

of disease.

From

June

men

and

years

1989 four

[mean,

54-69

six

years

early

METHODS

to June women

62.4 years])

(20 lesions),

with

AND

patients

[mean,

61.0

components

1990,

17 patients

aged

53-71

with (all

early

men

years])

(eight

HCC

aged with

HCC

lesions),

and

contained

(Edmondson

were phy

detected (US),

means

their

of partial

operating

was

MR

imaging

at 1.5 T (MRT 200FX;

Tokyo) was used in this study. Images were obtained with a multisection spinecho (SE) technique performed with use of 600/15 or 20 (repetition time [TR] msec/ echo time [TEl msec) and 2,400/20, 60, or 80 sequences.

Section

thickness

was

lesion

that

had

not

destroyed

as a nodular the

underby-

10

mm with no intersection gap. Two and four signal acquisitions were used for the short TRITE and bong TR/TE sequences, respectively. The short TR/TE images were obtained with a field of view of 35 cm, a 256 x 256 matrix, and no phase wrap. The long TR/TE images were obtained with a field of view of 35-40 cm, a 256 x 256 matrix, and a half-encode reduction. Respiratory and electrocardiographic compensation was not used. The signal intensities and morphologic features seen with each SE sequence were retrospectively compared for early HCC and HCC with early components to reveal the characteristics of early HCC.

RESULTS Sixteen

lesions

cases

were

Four

lesions

20 lesions

of early

found

beside

were were

HCC main

solitary. detected

echo,

In comparison

TE

=

echo

time,

with

TR

=

in 13 tumors.

Nine with

Abbreviations: AH = adenomatous sia, HCC = hepatocellular carcinoma,

defined

system

Toshiba,

examination. was

proved

hepatectomy.

aging.

HCC

II and/or

ultrasonogra-

existence

10 patients (seven men and three women aged 45-76 years [mean, 61.3 years]) with untreated overt HCC (10 lesions) were studied with MR imaging and pathologic Early

5ev-

grade

at operative

and

A superconducting

of AM be-

foci

and

III). The early HCCs ranged from 0.8 to 2.7 cm in diameter (average, 1 .4 cm), and the HCCs with early components ranged from 0.9 to 3.4 cm in diameter (average, 2.0 cm). Overt HCCs ranged from 2.7 to 12.0 cm in diameter (average, 6.2 cm). All lesions

by

et al (6) em-

components

malignant

with

been

Sakamoto

that

sides

of AH

hepatic

eral areas of well-differentiated HCC (Edmondson grade I or grade I and II) (8) in a thin trabecular or acinar formation. However, these areas were not barge enough to be recognized macroscopically. HCC with early components was defined as an early HCC lesion with macroscopically detect-

able nodules

181:209-213

ogy (Y.M., SN., K.T., N.M., T.Y.) and Surgery (S.Y.), National Cancer Center Hospital, Tsukiji 5-1-1, Chuo-ku, Tokyo 104, Japan; and the De-

and Welfare.

(HCCs)

be detected and removed has bed to an improvement

(13 the

small

carcinomas

PATIENTS

From

MD MD

Carcinoma:

progression

761.1214

Takayasu, Hirohashi,

#{149} Setsuo

repetition

of the MR

im-

surround-

hyperpla-

SE

=

spin

time.

209

ing

hepatic

were were

parenchyma,

hyperintense isointense

quences. Seventeen (Fig ib), two were small area within

and

one

was

nine

lesions

(Figs la, 2a) and with SE 600/15 sewere

isointense

hypenntense the

in a

tumor

(Fig

hypointense

2b),

with

SE

2,400/60 or 80 sequences. Pseudocapsubes and a nodule within a nodule appearance were

detected

ic,

at gross

2c) or MR

were HCC

examination

imaging.

11

not

(Figs

All lesions

found to be webb-differentiated at histopathobogic examination:

15 were one was

with and

Edmondson Edmondson

grade grade

I (Fig I and

the

grade

I area

predominant,

four

were

grade

I and

id), II

II with

a.

b.

the

grade I area more predominant and the grade II area only slightly recognized (Fig 2d). Fatty components were recognized within tumors in 17 of the 20 lesions (Table 1). On the other hand, seven of eight lesions nents

of HCC with were detected

ing.

Six were

early with

hyperintense,

one

isointense, and one was with a central hypointense

(Fig 3a) with SE 600/15 Five were hyperintense, pointense

with

nodule,

compoMR imag-

and

sequences. one was

a central

two

was

hyperintense nodule

hy-

hyperintense

were

isointense

with

SE 2,400/60 A pseudocapsule

or 80 sequences (Table 2). was detected in lesion (lesion 7). But a nod-

only one ube in nodule

appearance

was

seen

in

three lesions (lesions 4-6) at gross examination (Fig 3b, 3c), and two of these lesions showed mixed signal intensity patterns on MR images. All lesions in this group were well-differ-

entiated and had

HCC overt

Edmondson

HCC

except nodules grade

in addition

II and/or

to the

as hyperintense

T2-weighted lesions had

grade

were

masses

images.

detected

on 10 on

Pseudocapsubes

in nine

of these

lesions.

DISCUSSION HCC

has

multiple

(7,8).

sis is closely

rebated

AH is a proliferative tential to become

210

#{149} Radiology

of a 1.9-cm-diameter

mass

(lesion

18 in Table

1) in the right

lobe of the liver

in a 62-year-old

man. (a) Ti-weighted MR image (600/15) shows a hyperintense pattern. (b) T2-weighted MR image (2,400/60) shows an isointense pattern. (c) Cross section of surgical specimen shows mass (arrows) similar in configuration to the surrounding liver. Pseudocapsule was not seen. (d) Micrograph shows well-differentiated HCC (Edmondson grade I) with acinar structure (arrows) and thin trabecular pattern within the mass (hematoxylin-eosin

stain;

original

magnification,

diagnosed

as early

usually

accompanied

borderline

x200).

Therefore,

atypical

or

this mass

can be differentiated

from

AH and

HCC.

Hepatocarcinogeneto AH,

because

lesion with poHCC (9) and is

by

foci that

cannot

mined to be cancerous ous foci (7,8,10). The

defined as atypical latter as AH with there

are

with

the

and/or cancerformer has been

All (7) and the malignant foci. But

histopathologic

definition

be deter-

problems

of AH with

malig-

nant foci. Sakamoto et ab (7) reported that all the areas of AH with malignant foci were cancerous. Kanai et ab (8) defined a hepatic nodular lesion

with histopathobogic

stages in the course of carcinogenesis or progression in the cirrhotic liver (7). Several types of HCC in the histopathologically earlier stage have been

discovered

Images

III

peripheral

images. Six of these a hypointense pattern

Ti-weighted

1.

for one (lesion 3) composed of

grade I area (Fig 3d). Fatty components were recognized within tumors in seven of these eight lesions. All lesions of overt HCC were

shown

d.

C.

Figure

macroscopically

cancerous scopically,

areas early

ferentiated

and

pia

such

or acinar

as a thin

formation

undetectable as early HCC. MicroHCC is very well dif-

shows

structural

trabecular

and

aty-

pattern

increased

cel-

bubarity with slight nuclear atypia; but it differs from overt HCC in that it has no pseudocapsule and shows no destruction of underlying liver structure

(7,8). On the other hand, HCC with early components has been judged to be a more progressive disease than early HCC because an overt HCC nodule within a tumor is large enough to be detected at gross examination (7) and usually shows hypervascularity (ii). However, a means of diagnosing these types of HCC with use of radiologic imaging has not been established. MR imaging is useful in diagnosing overt HCC, AH, and regenerative nodules (4,5,12,13). Generally,

HCC

shows

a hypo-

overt

or isointense

pat-

tern on Ti-weighted images and a hyperintense pattern on T2-weighted images (5). AH and regenerative nodules show a hyperintense pattern on Ti-weighted images and a hypoin-

tense pattern (12,13).

On

on T2-weighted the

other

hand,

images early

October

HCC

1991

b.

a.

C.

e.

d. Figure

2.

Images

of a 1.7-cm-diameter

mass

(lesion

17 in Table

1) in the right

lobe of the liver in a 62-year-old

image (600/15) shows a hyperintense pattern (arrow) with a central hypointense spot. (b) However, only a hyperintense area on the T2-weighted image (2,400/60). (c) Cross section of surgical specimen shows an mass without a pseudocapsule. (d) Histologic section shows fatty change (J) and Glison sheath (g) within shows well-differentiated HCC (Edmondson grade I) around Glison sheath (g) that shows remodeling of lularity with slight nuclear atypia (hematoxylin-eosin stain; original magnification, x 100). Therefore, this

mainly pattern

showed a hyperon Ti-weighted

an isointense

pattern

images

study.

HCCs aged

in our

in our while

ing treatment) intense pattern imaging. differentiate

on T2-weighted All of the overt (which were im-

study the

or isointense images and

patient

was

demonstrated at T2-weighted

Therefore, early

HCC within

a hyper-

nodules. can be

into two subtypes macroOne has dominant early and small, central overt

nodules

and

a nodule

has

a nodule

appearance

(lesions

and a mixed on MR images

signal intensity (lesions 4 and

181

#{149} Number

4-6

1

in Table

2)

pattern 6 in Ta-

this

subtype

can

be

differentiated from both early HCC and overt HCC with MR imaging. The other subtype (lesions i-3, 7, and 8 in Table 2) has a large overt and scanty early components

HCC

nodule that

were recognized in the periphery of the lesions. Only overt HCC nodules within a tumor could be recognized as hyperintense images. Therefore, may stage

represent than the

The sion

a more former.

has

signal

not

fully

85%

images

of early

HCCs

(cs) and

celHCC.

pattern and 100% of HCCs with early components not having a nodule within a nodule appearance and 100% of overt HCCs had a hyperintense pattern on T2-weighted images. Therefore, we conclude that the signab intensity pattern on T2-weighted images gression

is closely rebated to HCC proand that the presence of a

for

nosis

(12,13). had

(arrows).

structure

Gen-

progres-

erably, AH and regenerative have a hypointense pattern

weighted

mass

(e) Micrograph increased can be diagnosed as early

as

studied.

between

been

cord

MR

the mass is seen yellow-white

pattern

progressive

intensity

the mass

(a) Ti-weighted within shaped,

hyperintense pattern on T2-weighted images depends on the gross size of overt nodules composed of Edmondson grade II or grade III HCC within a tumor. MR imaging is sensitive in the diag-

areas on T2-weighted the latter subtype

relationship and

HCC at gross

examination

Volume

receiv-

it is possible to HCC from overt

HCC, Afl, and regenerative HCC with early components classified scopicably. components

not

bbe 2). Therefore,

woman.

a small part irregularly

nodules on T2-

In our an

study,

isointense

of early

hepatic pattern

extremely erably,

HCC

because

malignant

tumors with a hyperintense on Ti-weighted images are rare, except for HCC. GenT2-weighted

imaging

is useful

Radiology

#{149} 211

in detecting

overt

HCC

(5).

Ti-

weighted imaging was superior to T2-weighted imaging in detection of early HCC in our study. However, ii of the 20 early HCC lesions were not detected due to isointensity on both Ti- and T2-weight#{235}d images. Consequently, other modalities such as computed tomography and/or US or operative US are also necessary to screen for them. Generally, tumors show a hyperin-

tense pattern on Ti-weighted images because of bleeding or fatty degeneration. In our study, there was not one case in which a clear bleeding focus

a.

b.

existed within a tumor, but fatty degeneration was observed in almost all of the lesions. However, except for one lesion (lesion i9), distinct differences

in the

degree

of fatty

compo-

nents were not observed between hyper- and isointense lesions on Tiweighted images, so we could not attribute the hyperintensity simply to the fatty components. Furthermore, evidence of shortening of Ti by a paramagnetic substance could not be obtained. This has an

study shows that iso- or hyperintense

early

Ti-weighted

images

and

tense

with

or without

pattern

hyperintensity ages.

HCC pattern partial

on T2-weighted

Therefore,

we

conclude

of their

patterns

on T2-weighted

imthat

early HCC is an intermediate between AH and overt HCC HCC with early components standpoint

on

an isoin-

signal

lesion and/or from the

2.

3.

U

Yumoto Y, Jinno K, Tokuyama K, et al. Hepatocellular carcinoma detected by iodine oil. Radiology 1985; 154: 19-24. Matsui 0, Kadoya M, Suzuki M, et al. Dynamic sequential computed tomography during arterial portography in the detection of hepatic neoplasms. Radiology 1983; 146:721-727.

Makuuchi al.

M, Hasegawa

The

Figure

H, Yamazaki

S,

Table 1 Relationship HCC

5.

7.

et

HeRadiDi-

tologic studies. Radiology 1986; 159:371377. Sakamoto M, Hirohashi S, Shimosato Y. Early stages of multistep hepatocarcinogenesis: adenomatous hyperplasia and early hepatocellular carcinoma. Human Pathol 1991; 22:172-178. Kanai T, Hirohashi S, Upton MP, et al. Pa-

8.

212

of small hepatocellular

carcinoma:

a proposal for new gross Cancer 1987; 60:810-819.

classification.

Edmondson

PE.

#{149} Radiology

HA, Steiner

Primacy

(lesion 4 in Table 2) near right hepatic vein in a (600/15) shows hyperintense pattern (arrows)

MR Imaging

Findings

Diameter

(cm)

and

Histopathologic

Fmndings* SE 2,400/60

Sequence

or 80

4

bsointense Isointense Isointense Isointense

5 6 7

1.0 1.1 i.1

Hyperintense Isointense Hyperintense

Isointense Isointense Hyperintenset

8 9 10 11 12 13 14 15 i6 17 18 19

1.2 1.2 1.2 1.2 1.4 1.4 1.5 1.6 1.6 1.7 1.9 2.0 2.7

Isointense Isointense Hyperintense Hypermntense Isointense Hypenntense Isointense Isointense Isointense Hyperintense Hypermntense Hyperintense Hyperintense

Isointense Isointense Isointense Isointense Isointense Isointense Isointense Isointense Isointense Hyperintense Isointertse Isointense Hypermntense

The signal intensity of the lesion was compared t - = not detected, + = mild, + + = moderate, t Lesion was only partially hyperintense. S Grade I area predominant. *

I area

predominant

in Early

Histopathologic

Results

Edmondson Grade

Isointense Isointense Isointense Isointense

20

Results

Sequence

0.8 0.8 0.9 1.0

Grade car-

between

1 2 3

use of operative ultrasound as an resection in patients with hepacarcinoma. World J Surg 1987;

Ito K, Nishimura K, Togashi K, et al. patocellular carcinoma: MR imaging. ology 1987; 164:21-25. Ebara M, Ohto M, Watanabe Y, et al.

thology

mass

SE 600/15 Lesion

agnosis of small hepatocellular carcinoma: correlation of MR imaging and tumor his6.

of a 1.7-cm-diameter

MR Imaging

11:615-621. 4.

Images

65-year-old man. (a) TI-weighted MR image with a central hypointense area. (b) Cross section of surgical specimen shows a mass (arrows) with a nodule within a nodule pattern. (c) Histologic section shows a mass (arrowheads) with necrosis (n) in central nodule due to transcatheter arterial embolization, but another area within the mass is viable (v). (d) Micrograph shows necrotic area (ii) corresponding to the central nodule in c. This area was thought to be a “ghost” HCC of Edmondson grade II. A welldifferentiated HCC of Edmondson grade I showing remodeling of cord structure (cs) and foci of acinar structure is seen on the left side of the image (hematoxylin-eosin stain; original magnification, x40). Therefore, this mass can be diagnosed as HCC with early components.

aid to liver tocellular

3.

intensity

images.

References 1.

d.

C.

with

and

that

+ + +

and grade II area only slightly

I I I I I

+

I I

+

I I I I I I I I I I I I I

of the surrounding =

Fatty Changet

+ +

++ + + +

and

IP

+ + + + +

and and

W II’

and

IP

and

IV

+ -

+ + +

+ + ++ +

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severe.

recognized.

October

1991

9.

cinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 1954; 7:462-503. Tsuda H, Hirohashi 5, Shiosato Y, et al. Clonal

origin

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adenomatous

by-

perpbasia of the liver and clonal identity with hepatocellular carcinoma. Gastroenterology 1988; 95:1664-1666. 10.

Arakawa Emergence

M, Kage M, Sugihara 5, et al. of malignant lesions within

adenomatous rhotic

liver.

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208. 11.

12.

Matsui 0, Kadoya M, Kaneyama 1, et al. Benign and malignant nodules in cirrhotic liver: distinction based on blood supply.

Radiology 1991; 178:493-497. Matsui 0, Kadoya M, Kameyama T, et al. Adenomatous hyperplastic nodules in the cirrhotic liver: differentiation from hepatocellular

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1

with MR imaging.

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Radiology

#{149} 213

Early hepatocellular carcinoma: MR imaging.

All areas in hepatic lesions designated as adenomatous hyperplasia (AH) with malignant foci have recently been recognized as cancer. AH with malignant...
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