State Donald

G. Mitchell,

and exclusion of focal liver is especially difficult in pa-

with diffuse liver disease. Magnetic resonance (MR) imaging may be particularly valuable in these patients

tients.

By judicious appropriate pulse

comparison sequences,

of normal

and hypertrophic liver guished from atrophic, otherwise chyma.

abnormal Chemical

may be distinneoplastic, or hepatic paren-

shift

(lipid-sensi-

five) techniques allow definitive identification of fatty liver, including focal fatty infiltration or focal sparing. T2-weighted and T2*weighted images allow identification of iron overload, depicting malignancies as focal masses without iron. Analysis of signal intensity and internal morphology allows confident distinction between

regenerative

nodules

and

hepatocellular carcinoma in most instances, and allows diagnosis of early carcinoma within regenerative nodules. MR imaging provides capabilities

for

noninvasive

characterization

of liver tissue beyond with other noninvasive Index terms:

Liver, cirrhosis, fatty #{149}Liver, hypertrophy 761.1214 #{149} Liver neoplasms, State-of-art reviews Radiology

1992;

Art

MD

Focal Manifestations at MR Imaging’ Detection lesions

ofthe

those available modalities. 761.794 #{149} Liver, Liver, MR, MR. 761.321

#{149}

185:1-11

ofDiffuse

D

liver disease

IFFUSE

is usually

di-

agnosed by means of laboratory and histologic methods, while imaging plays a minor role at most centers. However, focal manifestations of diffuse liver disease often complicate clinical management by mimicking or obscuring malignant lesions. Magnetic resonance (MR) imaging offers us some unique opportunities to characterize hepatic tissue as part

of a comprehensive imaging examination, thereby resolving many ambiguities that have limited previous efforts to diagnose significant focal pathologic conditions in patients with diffuse

liver

will

consider

disease.

In this

review,

Disease

sequences. view the are

most

ization

useful

for specific

of hepatic

tissue.

Ti-weighted The

Images

choice

dictated tures.

rethat

character-

between

spin-echo

and gradient-echo (GRE) for optimal Ti-weighted

by system

(SE)

techniques imaging

is

software feaexperience is that motionSE Ti-weighted images

My

compensated

and

are more useful than Ti-weighted GRE images for characterization of hepatic parenchyma in most patients.

The

we

the

In this section, I will basic pulse sequences

liver

has

a shorter

Ti than

most

commonly used MR imaging techniques that are especially valuable for hepatic MR imaging and will discuss the relatively unique MR features of normal liver and their alteration with disease. We will then

other nonfatty tissues, estimated to be approximately 500 msec at 1.5 T and 320 msec at 0.5 T (i). The short Ti of liver has been attributed to its high density of endoplasmic reticulum,

explore

for binding intracellular water (2). Normal hepatic tissue therefore should have higher signal intensity than tissues less involved in protein

common

focal

manifestations

that may be associated with diffuse liver disease. Emphasis will be placed on the potential value of specific MR imaging techniques, available on most imaging units, which can distinguish unambiguously between “pseudotumors” and malignancy in patients with diffuse liver disease. My clinical experience has been at 1.5 T, but effective hepatic MR imaging appears possible over a wide range of magnetic field strengths.

MR

IMAGING

Comprehensive hepatic tissue

mation

I From the Department of Radiology, Thomas Jefferson University Hospital and Jefferson Medical College, 132 S 10th St, Philadelphia, PA 19107. Received April 23, 1992; revision requested June 2; revision received and accepted June 23. Address reprint requests to the author. 0 RSNA, 1992

Liver

from

multiple

pulse

usually

sue

nosis

pulse limited characterization, has

can often

of

if inforsequences

an appropriate

sequence by itself specificity for tisa confident diag-

be reached combination

by using of pulse

synthesis,

a large

such

surface

as spleen,

muscle, and most Hepatic signal by fatty diffusely

infiltration, increased

is because

the

area

kidneys,

malignancies. intensity is increased but

detection

of

signal intensity of fatty livers is difficult by simple inspection of Ti-weighted images. This signal

intensities

of

and fatty liver both are interbetween that of fat and most other tissues, and because there is no suitable internal standard of compan-

is integrated. This is analogous to solving a riddle, with each pulse Sequence used to answer specific questions and resolve ambiguities remaining from other sequences. Although

an individual

provides

normal mediate

TECHNIQUES

characterization is most effective

which

son to determine signal intensity

Focal

fatty

more volved

intense liver,

(see below) firm

liver

may

hepatic increased.

appear

than adjacent but chemical

may

slightly uninshift images

be necessary

to con-

this.

Abbreviations:

hepatocellular

short-tau

TR

whether is slightly

=

IIII IIUII IIUItIII IIIIUI IfliIU

repetition

GRE

carcinoma,

inversion

=

gradient

SE

recovery,

time.

=

echo, echo,

spin

TE

=

HCC STIR

echo time,

= =

Hepatic

signal

intensity

on Ti-

weighted images can be decreased by numerous diseases, including neoplasia, edema, dense iron overload, or dense fibrosis. Altered hepatic Ti relaxation time can be detected sensilively on inversion-recovery images, by determining the inversion time necessary

to null

hepatic

parenchyma

(3). T2-weighted The

Images

liver

has a relatively

(approximately

40 msec)

short

T2

(1,4). On SE

time (TE) in the msec, most but not all hepatic signal will have decayed. On these images the liver will be minimally more intense than muscle (longer Ti, comparable T2) but much images

with

less

echo

of 80-100

range

intense

than

fat,

kidney,

or nor-

mal spleen (longer Ti and longer T2 [approximately 60 msecj) (1). Hepatic signal intensity can be increased by neoplasia or edema, or reduced by iron overload. Hepatic parenchyma is depicted well with repetition time (TR) of 2,000 msec or more, although longer TR may be necessary to depict optimally the high signal intensity of focal lesions such as hemangiomas and cysts, especially at high magnetic field strength. It is important to remember that terms

such

as “Ti-weighted”

“T2-weighted” because they

have become help categorize

sequences,

but contrast

sues

restricted

is not

and

popular pulse

between to the

tis-

relaxation

time specified in the term. If T2 and T2* relaxation times are reduced markedly, such as with heavy iron overload, hepatic signal intensity may be reduced significantly even on “Ti-weighted” images, because the “short” TE of these images may be long enough for significant T2 relaxation to occur. In fact, reduced signal

intensity

from

iron

overload

to appreciate

difficult

on heavily

weighted images because normal liver has relatively intensity.

may be

T2*weighted

T2-

even the low signal GRE

images

and intermediate or mildly T2weighted (eg, TE less than 50 msec) SE images may be more specific for

detection load,

or exclusion

since

intensity

of iron

the intermediate of normal

liver

oversignal

parenchyma

on these images is distinguished readily from the abnormal low signal intensity of iron-overloaded liver.

Chemical Chemical

allow

2

Shift shift

separation

#{149} Radiology

Images imaging

techniques

of the signals

from

triglyceride and water protons based on differences in resonance frequency (ie,

chemical

allow

shift).

an absolute

diffuse

fatty

These

from

techniques

diagnosis

infiltration

of focal

or

(5-10).

In conventional SE MR images, signal from water and triglyceride are in phase relative to each other, so that they contribute additively to the net signal intensity depicted on the final image. Opposed-phase SE images, where water and lipid signals interfere destructively, can be obtained by changing the liming of the 1800 refocusing pulse so that the phases of triglyceride

and

water

fat and

by improving

dynamic

range,

magnetization

it is less sensitive for detecting fatty liver than opposed-phase imaging (9). As an example, consider a region of liver where fat accounts for 10% and water accounts for 90% of the signal on a conventional in-phase image (Fig 1). On a fat-suppressed image, fatty liver will have approximately 90% of its original in-phase signal intensity. On the comparable opposed-phase image, liver will have only 80% of its original in-phase signal intensity (90 tional disadvantage

suppression

minus

10).

An

addi-

of current

fat-

is that

it is more

imaging

are opposite each other when the echo is formed. Pixel brightness is thus the absolute value of water signal intensity minus triglyceride signal

sensitive to magnetic field heterogeneity than is opposed-phase imaging. Although fat suppression is possible at field strengths less than i.5 T,

intensity.

this may be more challenging since the chemical shift between triglyceride and water, on which successful fat suppression depends, is less at lower field strength. Chemical shift selective fat suppres-

Signal

loss

occurs

within

voxels where both lipid and water signals are represented. This includes tissues that contain both water and lipid (eg, fatty liver and cellular bone marrow),

as

well as partial

volume

effect at interfaces between waterdominant tissues (eg, abdominal viscera) and adipose tissue. The phases of water and triglyceride are also opposed on GRE images with appropriate TE. Since there is no 180#{176} refocusing pulse to compensate for different resonant frequencies

within

a voxel,

the phase

of water

and triglyceride cyde in and out of phase with respect to each other as TE increases (11). For instance, at 1.5 T, TEs of approximately 2.1, 6.3, and 10.5 msec yield opposed-phase images, while TEs of approximately 4.2, 8.4, and 12.6 msec yield in-phase images. The difference between in-phase and opposed-phase images is greater at short

TE.

The phases of fat and water are at least partially opposed to each other on most GRE images. Therefore, fatty liver can be a cause of decreased signal intensity on these images, potentially mimicking iron overload. These two forms of diffuse liver disease can be differentiated by comparison with T2-weighted SE images; hepatic signal intensity will be normal or slightly increased with fatty liver but decreased with iron overload. The chemical shift between fat and water can also be used to decrease or eliminate the signal from fat (7,12-14). The most commonly used chemical shift fat-suppression techniques involve transmitting a narrow-band excitation pulse designed to saturate triglyceride protons selectively without affecting water protons. While fat suppression can improve image quality by reducing artifacts

sion

must

be distinguished

from

short-tau inversion recovery (STIR). On STIR images, fat is suppressed because of its short Ti rather than its chemical shift relative to water (15,16). The ability of STIR images to allow one to diagnose unambiguously fatty inifitration of the liver has not been demonstrated.

Flow- and Images

T2*weighted

GRE

GRE images are valuable for depicting abdominal vascular anatomy as high signal intensity. Bright-blood images are best when TE is minimized, but the frequent use of gradient moment nuffing to maximize vascular

signal

or greater, mentation.

ensures

that

at least Even

with with

TE is 6 msec

current these

instru-

“short”

TEs, the images are sensitive to dm1cally significant levels of iron deposilion, at least at 1.5 T. With lower field strength, sensitivity to iron is lower, but this sensitivity can be increased by using a longer TE. GRE images with TE less than 3 msec depict blood flow as high signal intensity even without gradient moment nuffing. These images are relalively

insensitive

NORMAL The

to iron,

LIVER AND HYPERTROPHY

however.

HEPATIC

in characterizing heif there are focal lesions, is to identify normal liver if it is present. Normal hepatic signal patic

first step

tissue,

especially

October

1992

intensity

is greater

than

tal muscle

with

sequence, ery images

except for in which

that

virtually

of skele-

every

pulse

inversion-recovthe inversion

time is selected so that hepatic signal intensity is close to its null point. On T2-weighted

images,

liver

has

signal

that is only slightly higher than that of skeletal muscle. When liver is severely damaged,

that is relatively spared may hypertrophy, occasionally with a round or

signal intensity may Ti-weighted images T2-weighted images damage is asymmetric

mental

hepatic

satory

hypertophy

intensity

oval

be reduced on and increased on (Fig 2). If the or lobar, liver

shape

may region

intensity,

In-Phase

mass (Fig

Fat-Suppressed

amount

of signal

from

water,

Opposed-Phase

increasing

contrast

between

normal

and

fatty

a.

with 3).

intensity

in b. (Images

a. Figure

by C. Tempany

Extreme

atrophy

of the right

(arrows)

Number

#{149}

1

hep-

Segmental

as a wedgeabnormal signal

of which

should

abnormal

signal

be

intensity

face may result from differential atrophy and hypertrophy. After

of intravenous

the remainder dimeglumine.

obtained to severe

ad-

contrast

A. Chako;

reprinted,

with

permission,

of the right lobe. (a) Axial SE 400/20 (TR msec/ (S), right kidney (K), and the atrophied right right lobe (R), which is nearly isointense rela-

more than that of muscle (M). (c) GRE MR imagainst tissue iron as the cause of relatively low from

reference

c.

remainder of liver. (d) SE 400/11 MR image, left lobe (M), rotated counterclockwise due

185

manifest with

18.)

d.

lobe manifesting as a focal mass. (a) Axial SE 2,500/100 MR image shows a high-signal-intensity liver (L), which has normal signal intensity. There is abundant ascites (A). (b) SE 400/11 MR image

at the posterior aspect of the the mass (arrows) as slightly less intense than minutes after administration of gadopentetate

Volume

and

b. 3.

acute

or biliary obstruction sclerosing cholan-

c. severe atrophy than the spleen of the atrophied

fat. The mass (arrows) has normal signal intensity, slightly the “mass” (arrows) as isointense with the right lobe, evidence

provided

of seg-

compen-

In livers with fatty infiltration, segmental portal vein obstruction causes focal sparing, presumably because less fat is delivered to hepatocytes (23,24). Unusual notches on the hepatic sur-

b.

Figure 2. Masslike hypertrophy of the left lobe in a patient with cirrhosis and TE msec) MR image shows a mass in the left lobe (arrows) that is more intense lobe (R). Q,) SE 2,500/100 MR image shows abnormally increased signal intensity

signal

include

the apex

ministration

liver.

five to spleen (S) and subcutaneous age (25/13, 20#{176} flip angle) shows

and

searched carefully for a tumor or other obstruction. Occasionally, atrophied liver may manifest as a focal

Figure 1. Diagramatic representation of focal fatty infiltration, demonstrating relative contrast for standard (in-phase), fat-suppressed, and opposed-phase Ti-weighted techniques. On in-phase images, fatty liver has slightly greater intensity than normal parenchyma, although this difference may be subtle. With fat suppression, intensity of the focal fat will decrease, becoming isointense or hypointense depending on the proportion of signal from triglyceride and water. With opposed-phase techniques, the signal from triglyceride is used to eliminate

an equivalent

Causes

and so on (i7-22).

atrophy shaped

IL

2) (i7).

atrophy

atitis, portal vein due to malignancy,

gitis,

[

(Fig

ofliver. ! The “mass”

=

inferior vena has a straight

cava. (c) SE 400/11 MR anterior edge (arrows)

at an inferior level. The gallbladder atrophy of the right lobe. L = lateral

(G) is situated segment, P

=

image, obtained and enhances

posterior left portal

to the medial vein.

mass

shows approximately 5 more than the

segment

Radiology

of the

#{149} 3

Figure

4.

Massive

date

lobe and

with

peripheral

hypertrophy

central

of the

portion

atrophy

cau-

of the liver,

and

increased

en-

hancement, in a patient with Budd-Chian syndrome. (a) Contrast-enhanced CT scan shows a large region of irregularly decreased attenuation relative to peripheral portions of the liver. This was considered suspicious for infiltrative neoplasm such as hepatocellular carcinoma (HCC). The low-attenuation structare indicated by the curved arrow was interpreted incorrectly as a scar or necrosis. (b) Axial SE 3,000/100 MR image normal increased signal intensity

eral liver spleen

which

(*),

(S). The

is isointense

central

has relatively

MR

relative

portion

normal

ial SE 500/11

shows abof penphof the

signal

image

to

liver

intensity.

shows

(c) Ax-

massive

hy-

pertrophy of the caudate lobe (white arrows). There is high signal intensity in the left portal vein (L) due to slow in-plane flow. The central portion of the caudate lobe (thick black

arrows)

has

higher

signal

intensity

than the remainder of the liver. The right lobe and medial segment of the left lobe (*) have decreased signal intensity, approximately isointense relative to the spleen. Note that these regions had increased enhancement in a. Thin black arrow indicates the enlarged accessory hepatic vein draining the caudate

lobe.

(d) Axial

Ti-weighted

GRE

image (102/2.4, 900 flip angle) obtained proximately 1 minute after administration 0.1 mmol of gadopentetate dimeglumine shows increased (*). The curved

thrombosed small

enhancement

straight

black

with

Doppler

of

indicates the vein, and the

arrow

indicates

and hepatic vessels within it (i8). The patic parenchyma

the

accessory hepatic vein lobe. Reversed flow in (R) was documented

ultrasound

(US)

and

abnormal

phase-

contrast

MR images (not shown). Flow in the vein (L) was antegrade, presumably related to shunting through a large patent paraumbilical vein (large straight black arrow) in the falciform ligament, which drains to the cluster of vessels noted anterileft

portal

orly. sion

Additional evidence of portal hypertenincludes varices in the gastrohepatic ligament (white arrows).

areas

perfusion

rium

with during

phases.

decreased

or equilib-

possible

shape hepatic

explana-

tion for this increased enhancement decreased size of hepatocytes, in-

creasing ume

the proportion

occupied

interstitial patic

by the

spaces.

arterial

material

like

a mass,

intensity

those

4

but

it should

characteristics

of normal

#{149} Radiology

may

hepatic

that should not be mistaken masses or segmental insult.

These include Reidel extending posterior ney or lateral to the

be shaped

have similar

signal to

parenchyma,

relative

sparing

patient

with

weighted

and

showed evidence

of the caudate Budd-Chiari

signal intenimage, with

lobe

(C), in a

syndrome.

GRE images

decreased intensity of increased iron

T2-

(not shown) of entire deposition.

lobe and liver to the right kidspleen.

drain site

above

or below

of obstruction.

obstruction

the

of

Budd-Chiari

may

even Although

instances,

be segmental major

veins may not be visualized thrombosed, demonstration patent central hepatic veins does may

Syndrome

The Budd-Chian volves obstruction from the sinusoidal

syndrome

in-

of venous

outflow

resulting

hypertension,

in portal

bed

of the

liver,

principal

In some

patic

blood

arteries

Markedly decreased on SE 400/20 MR

subsegmental. to

enhance dilution

Figure 5. sity ofliver

for

he-

of portal

in hepatic veins. liver

however.

and

is increased

may therefore there is less

than in portal Regenerative

is

vol-

Additionally,

deprived

which because

contrast

vascular

perfusion

parenchyma flow, more

of liver

intensity,

Awareness of the normal signal intensity of hepatic parenchyma, which is higher than that of spleen on Tiweighted images and only slightly higher than that of muscle on T2weighted images, should allow differentiation between malignancy and

Internal landmarks such as major hepatic vessels, falciform ligament, and gallbladder should be identified to determine if any segments are larger or smaller than usual. There are several anatomic variants of hepatic

portal

dynamic

One

signal

may be visible surrounding hemay have grossly

regenerative masses. This is important, so that the most pathologic liver can be sampled for biopsy.

material, computed tomographic (CT) and MR images may show increased enhancement of hepatic parenchyma

in the

d.

C.

peripherally

black arrow middle hepatic

patent and enlarged draining the caudate the right portal vein

MR

ap-

exclude

liver,

as-

cites, and progressive hepatic failure. In most cases, hepatic venous outflow is not completely eliminated, since a variety of accessory hepatic veins may

or he-

or of

be

Budd-Chian

syndrome.

not Re-

gions with completely obstructed hepatic venous outflow tend to drain by means of shunting of blood from hepatic veins and arteries to portal veins, producing reversed portal yenous liver

flow (25). These regions of the will thus be deprived of portal

October

1992

vein

supply.

tion, pend

hypertrophy, in part on

perfusion

Since

hepatic

(26,27),

drome

regenera-

and atrophy dethe degree of portal

Budd-Chiari

is typically

syn-

associated

with

at-

rophy of peripheral liver, which has especially severe venous obstruction, and hypertrophy of the caudate lobe and central liver, which are relatively spared (28). On dynamic iodine-enhanced CT

images images,

or gadolinium-enhanced the peripheral atrophic

often

a.

b.

enhances

more

hypertrophied enhancement

combination fusion (see

normal

The

increased

is presumably

due

of decreased portal above) and dilatation

hepatic

sinusoids.

central

liver,

than may

than

liver.

MR liver

The

which

to a

perof

hypertrophied

enhances

the peripheral thus resemble

or

less

atrophied liver, a focal mass (Fig

4). Massive

hypertrophy

of the

cau-

date lobe may compress an otherwise patent inferior vena cava and displace the porta hepatis anteriorly. MR im-

ages

may

also

differences Figure

6.

Multinodular

fatty

infiltration

of uncertain

cause.

(a) Contrast-enhanced

CT scan

shows several low-attenuation lesions (arrows), suggestive of metastases. (b) Standard (inphase) SE 500/li MR image shows the lesions (arrows) as high signal intensity. Hepatic signal intensity is normal, greater than that of spleen. (c) Opposed-phase Ti-weighted GRE MR image (102/2.3, 90#{176} flip angle). There is destructive interference between signals from triglyceride and water protons at TE of 2.3 msec because there is no 1800 refocusing pulse. The lesions (arrows) have opposed-phase

low

image

not show

that

does

signal intensity. The Ti-weighted images

any lesions.

reversal indicates

The liver

of liver-lesion contrast that the lesions contain

has normal

signal

between in-phase and fat. (d) SE 2,500/iOO

intensity,

slightly

greater

demonstrate

in signal

due

atrophy,

congestion,

and/or

deposition. resemble trast with

The caudate lobe a focal mass because the abnormal signal

sity of the peripheral liver

(Fig

MR

portion

Fat,

primarily

may

cytes

in the

accumulate

following

or other

may of coninten-

of the

LIVER

FATTY eride,

to

iron

5).

than

of muscle.

regional

intensity

form

exposure

chemical

of triglyc-

within

hepato-

to ethanol

toxins

or in patients

who overeat or have diabetes mellitus (29,30). Patients with advanced malignancy commonly have fatty livers, possibly due to poor nutrition and the hepatotoxic effects of chemotherapy.

Fatty liver may elevated hepatic Fatty

or even regional

change

be associated transaminase

with levels.

is frequently

patchy

focal, most differences

eas of decreased accumulate less

likely reflecting in perfusion;

ar-

portal flow tend to fat than better per-

areas (23,24). Thus, in focal or segmental portal obstruction, fatty fused

infiltration

may

represent

hepatic

pa-

renchyma with better portal perfusion. Diagnosis of focal hepatic lesions often difficult in patients with fatty a.

b.

Figure 7. Masslike (in-phase) SE 500/i2 intensity 900 flip

fatty

infiltration

MR image

(arrows) in the angle). The region

in a patient

shows

right lobe. (arrows)

appearance on the in-phase image ance on GRE 116/2.4, 900 flip angle gadopentetate

Volume

dimeglumine

185

Number

#{149}

(not

1

an irregular

(b) Opposed-phase has low signal

in a, indicates images shown).

obtained

with

ethanol-induced

region

with

hepatitis.

minimally

Ti-weighted intensity, which,

fatty

liver.

within

The

increased

GRE when

lesion

1 minute

had after

infiltration. On CT images, may be isoattenuating with

(a) Standard

MR image compared

a similar administration

signal (116/2.4, with its

appearof

thus

eluding

fatty

infiltration

detection

(31).

has

increased

is

metastases fatty liver,

Focal echo-

genicity on US images and low attenuation on CT images, potentially mimicking focal masses (Figs 6, 7) or

Radiology

#{149} 5

a. Figure 8. scan

b.

Pericholecystic shows irregular area

pancreatitis.

c.

fatty infiltration of low attenuation

(b) SE 3,000/50

MR

image

in a patient (arrows)

shows

high

d.

with a prior history of ethanol-induced adjacent to the gallbladder (G), suggestive

signal

intensity

(arrows)

adjacent

acute

pancreatitis.

(a) Contrast-enhanced

CT

of inflammation or other injury from gallbladder (G), suggestive of inflammation

to the

acute or

edema. Hepatic signal intensity is otherwise reduced due to transfusional iron overload. (c) Standard (in-phase) SE 500/11 image shows reduced hepatic signal intensity from iron overload (note isointensity relative to right kidney [K]), except for increased signal intensity (arrows) adjacent to the gallbladder (G). Without chemical shift images, this might have been interpreted as regional sparing from iron overload. (d) Opposed-phase Ti-weighted GRE MR image (107/2.4, 900 flip angle) shows decreased signal intensity (arrows) adjacent to the gallbladder (G). When compared with the in-phase image in c , this indicates fatty liver. Because of the short TE, iron overload has only minimal effect on hepatic

signal

intensity.

inflammation (Fig 8) (32). Focal areas of relative sparing within diffusely fatty livers mimic typical hypoechoic lesions at US (33). Since metastases

may be denser sparing

may

scans

than mimic

fatty

liver,

masses

on

focal CT

as well (31).

Imaging

focal dude

features

fatty liver a wedge

mass

effect,

mal

vascular

findings

characteristic

and

the

presence

structures,

are

absent

Regions of fatty may be especially guish

from

small

tumors

of nor-

but

these

in many

liver that difficult

malignant

or obvious sels.

of

or focal sparing inshape (Fig 9), lack of

patients.

lesions,

do not exclusion

a.

are small to distin-

show

since

mass

effect

of hepatic

yes-

b.

posed-phase Ti-weighted between wedge (arrows) and

spared

Conventional SE images are relatively insensitive to mild or moderate fatty infiltration. A suspicious zone of decreased attenuation seen on a CT

fatty

scan is likely

tensity

to represent

focal fatty

level of confidence diagnosing focal

while

satisfactory, on not seeing

however,

since

The

recommended focal or diffuse for differential

most

detecting

effective regions

posed-phase While

in-phase

6

of fatty

imaging

most

tissues

and

#{149} Radiology

in instances fatty liver diagnosis.

technique (Figs appear

opposed-phase

liver

have

for sensitive

hepatic

fat. The

greater

validation

the

fatty

are efof

has

received

literature,

is more

widely

images

avail-

in cases

of moderate

or se-

infiltration,

but

inten-

regions

of the

signal reduced images

liver

as

are com-

such lobe

adjacent

is op-

ment

(34).

dial

segment,

on

images,

vein,

involved

to the The

is commonly

the remainder

falciform

other

side

adjacent

to the

spared

of the

liga-

of the

liver

me-

portal

when

is fatty

This

portal

remainder

region

flow

of the

While hypoechoic fatty liver usually occasionally

represents

also

for

monly

creased

sparing,

may

reversal contrast

of contrast between fatty

(b).

(33,35,36).

both

sity from fatty liver is not much as on opposed-phase

(Fig 9). Certain

in-

GRE op-

identification in the

Fat-saturation

fat suppression

signal

SE and

former

latter

with

lower

techniques

fective

vere

than

by fatty infiltration, as the medial segment of the left

is

1, 9) (9). similar

will

be helpful

it relies

something. Chemical shift MR imaging techniques allow confident, unambiguous diagnosis of fatty hepatic abnormalities and are therefore in which considered

is greater

on the latter.

posed-phase

able.

GRE MR image (58/2.4, 9O flip angle) shows and remainder of liver relative to a. Note that

liver

liver

infiltration if it appears normal on T2-weighted MR images, especially if the area has slightly increased signal intensity on Ti-weighted images. The

for this method of fat is likely to be un-

c.

Figure 9. Fatty liver with wedge-shaped sparing, of uncertain cause. (a) Standard (in-phase) SE 500/il MR image shows a wedge of decreased signal intensity (arrows) relative to the remainder of the liver. (b) Fat-suppressed SE 500/12 MR image. The wedge is now isointense with the remainder of the liver, consistent with sparing in an otherwise fatty liver. (c) Op-

tities larger

a region

of fat located intracellular

often

has

compared

liver

de-

to the

(37).

areas represent this

within focal appearance

with

similar

quan-

inside lipid

fewer droplets

but (38).

This is because echogenicity does not directly reflect the amount of fat but rather reflects the density of acoustic interfaces, which in turn depends on the size and number of lipid droplets. Chemical shift techniques, however, are sensitive to the amount rather than the distribution of lipid within voxels. Therefore, since even large lipid droplets are much smaller than MR imaging voxels, lipid will be suppressed on chemical shift images re-

October

1992

I Figure

10.

Hemochromatosis

with

cirrhosis

and multiple nodules of HCC. (a) SE 500/li MR image shows marked reduction of hepatic

signal

intensity

due

to iron

overload,

with several focal lesions of HCC (large arrows), which do not contain iron. Small arrows indicate septa surrounding iron-overloaded regenerative nodules. (b) SE 2,500/50 MR image is more sensitive to iron. The septa and smaller nodules are not seen, obscured by blooming

hepatic

from

massively

iron-overloaded

parenchyma.

tensity

fibrous

septa

(Fig

10).

long TE, the heterogeneous field caused by intracellular these livers extends across obscuring them. HCC

gardless

of the size of lipid

In cases

of fatty

liver

droplets.

in which

a focal

hypoechoic area is produced by creased lipid droplet size rather decreased fat content, chemical imaging is expected to depict a fusely

fatty

liver.

or exclusion sible, however, son of in-phase Ti-weighted

fatty

intensity

liver

on stan-

morphology

tration

tiate

must

of focal

fatty

be examined

it from

noma,

ally all pulse skeletal overload, reference

fat within

focal

nodular

infil-

ade-

MR

imaging

liver is more muscle

decreased

hepatic

mation

of T2 relaxation

quantify useful

iron overload, parameter for

time may providing

chelation

involves

absorption

and

of dietary

iron

pancreas,

Hemochromatosis

most

confused multiple

with iron transfusions,

overload where

cumulates

primarily

within

ages,

but

should these

allow tumors

masses if HCC

chemical

shift

imaging

distinction between and lipid-containing

of focal contains

fatty infiltration. lipid, this tumor

tends to be more well defined focal fatty infiltration, is often sulated, and usually contains elements

with

high

on T2-weighted

signal

intensity

OVERLOAD

Because of the important of the liver as a digestive loendothelial organ, iron 185

than encapsome

images.

IRON

Volume

Even

Number

#{149}

1

functions and reticuis deposited

of iron

in-

use

of long

The

depiction

Heavily

of

TR SE images, and small lesions because

signal

field

iron

it the

caused

may re-

intensity

of small

T2-weighted

images

nod-

help differentiate malignant tumors from benign lesions such as hemangioma or cyst, however. If a nonsiderotic nodule in a patient with hemochromatosis is not a hemangioma or

cyst, HCC

is the most

regenerative

patients

likely

diagnosis,

nodules

contain

(45).

accumulate

heart,

contrast liver on

in these

iron.

parenchymal

gans.

on Ti-weighted images do not (40,41). Hemorrhage, melanin, and other factors may cause masses to have high signal intensity on Ti-weighted im-

or

ules.

(42). Tuiron

high

parenchymal

the

with

patients un-

excess

magnetic

duce

since

Hemochromatosis accumulation

intensity

re-

(44).

liver,

signal

help a

10).

improve

on long obscure

by hepatic

signal

phlebotomy

(Fig

not

heterogeneous

with suffiobtained, esti-

levels

high

HCC may

monitoring

hemochromatosis do not contain

images

virtu-

(43). If images short TE can be

to therapeutic

MR

TE does

and since

in patients

and many have previously

(46), causing especially relative to iron-overloaded

in-

with

Toxic

with

to

for iron overdistribution

regenerative nodule, or lipomatous tumors (39,40). Although some welldifferentiated HCCs contain lipid, HCCs

suspected mor cells

intensity ciently

creased

hyperplasia,

times

sequences,

quantifying

to differen-

HCC,

T2* relaxation

muscle is unaffected by iron skeletal muscle is a suitable tissue for detecting and

sponse

images.

tissues

allowing

than

mech-

within

be sensitive and specific load and for its regional skeletal

lesion. If a lesion has signal intensity high enough such that it is isointense to fatty liver on standard images, it should be hyperintense on opposedThe

significantly,

tense

dard Ti-weighted images, a metastasis should be visible as a low-intensity

phase

T2 and

is still poscompari-

Since

signal

reduces

of several

overload

normal

opposed-phase

images.

has increased

by means

Iron

(42). Since

by judicious

and

liver

anisms.

diagnosis

Confident

of a metastasis

inthan shift dif-

in the

is common

hemochromatosis, with HCC also

With

magnetic iron in the septa,

and

CIRRHOSIS

in the

other

or-

should

not be from iron

Cirrhosis patic fibrosis

tween ac-

involves bridging

portal

underlying

tracts,

hepatic

he-

irreversible the spaces

destroying

be-

the

architecture

(47).

loendothelial cells of the liver and spleen, sparing hepatocytes, pancreas, and other parenchyma. Although he-

Many cirrhotic livers have prolonged Ti, T2, or both, presumably secondary to inflammation (48,49). Mild iron deposition also occurs in many cirrhotic

mochromatosis

livers,

potentially

signal

intensity.

cannot

reticu-

be differenti-

ated from reticuloendothelial load by simple inspection signal intensity, examination

overof hepatic of pan-

creatic

intensity

can

and

splenic

usually

make

distinction

dothelial

signal

this

distinction.

is significant,

iron

overload

This

as reticuloen-

is less

toxic

than hepatocellular overload. Cirrhosis is common in patients with hemochromatosis. In these

tients, low-signal-intensity tive nodules are sometimes on MR images with short trasted

with

intermediate-signal-in-

pa-

regeneradepicted TE, con-

Regenerative

heterogeneous

(50), and have

been

ii%

(5i).

times

hepatic

Nodules

Regenerative grossly distorted hepatocellular tive nodules been found

decreasing

nodules hepatic

result from architecture,

regeneration,

and

dysplasia. Regeneralarger than 5 mm have in 37% of cirrhotic livers

nodules found

These

hypoechoic

larger

than

iO mm

in approximately

nodules relative

are someto cirrhotic

Radiology

#{149} 7

liver

on

US

images,

mimicking

ance

HCC

of these

nodules

at MR-guided

not aware of any reports of MR ages of nodular transformation.

(52).

biopsy

Because of superior soft-tissue contrast, MR imaging can depict regenerative nodules with greater clarity than other imaging modalities. On T2weighted images, regenerative nodules often have low signal intensity relative to high-signal-intensity in-

livers should be distinguished from a rare hyperplastic condition of the liver called nodular transformation, or nodular regenerative hyperplasia (55). This disorder, characterized by multiple hyperplastic nodules devel-

flammatory

or damaged

oping

within

with these than

mimic

cirrhosis

fibrous

liver (Fig ii) TR and short nodules with

septa

(53). SE images TE may show greater clarity

might

be useful.

Regenerative

long SE

nodules

in cirrhotic

a noncirrhotic

even

if present

tend

to be absent

liver,

clinically.

Iron

in uninvolved

in the

im-

can

and

fat,

liver,

nodules.

I am

Hyperplastic

Nodules

Some large (macroregenerative) nodules in cirrhotic livers have plastic histologic characteristics, ing

to terms

hyperplasia” dysplasia

such

as “adenomatoid

(56,57). or frank

dyslead-

Discrete

foci of

malignancy

can

occur within macroregenerative ules (Fig 13) (51).

nod-

images with long TR and long TE, since these latter images have decreased signal-to-noise ratio. Approximately

25%

of regenerative

accumulate

iron

rounding

more

nodules

than

hepatic

parenchyma

their

identification

facilitating

the

sur(54),

as

areas of low signal intensity on T2weighted SE images or T2*weighted GRE images (Fig 12) (53). As biopsy of regenerative nodules may disclose normal hepatic architecture and cause a false-negative

diagnosis

suspected

Figure

of having

11.

Large

in patients

cirrhosis,

regenerative

avoid-

nodule

with-

b.

a.

out MR evidence of iron. (a) SE 500/12 MR image shows an unencapsulated lesion (arrows) with homogeneous signal intensity, slightly higher than that of adjacent hepatic parenchyma. The left lobe (*) has especially decreased signal intensity. (b) SE 500/14 MR image signal

with fat suppression intensity of the lesion

due to fat content. shows rows)

the regenerative as having

low

shows that high (arrows) is not

(c) SE 2,500/100 MR image nodule (straight arsignal

intensity

relative

to adjacent hepatic parenchyma, which has heterogeneously increased signal intensity due to severe damage from cirrhosis. A second regenerative nodule (curved arrow) was obscured on a and b due to peripheral signal reduction. (d) GRE 25/13 MR image with 200 flip angle shows the lesions as isointense relative

to adjacent

dence

against

intensity

hepatic

iron

parenchyma,

as the cause

evi-

of low signal

on c.

\

:

(1

\

-

‘‘a: I

.

I

i:;-----

,,

(#{149}

t

,

;i;i

!

I

.

i.#{149}#{149}r

#{149} -

a.

b.

Figure (b) GRE

Regenerative 25/13 MR image

original

magnification,

8

--

12.

#{149} Radiology

c.

nodules with increased iron. (a) SE 2,500/100 with 20#{176} flip angle shows the nodules (arrows) x200)

of a regenerative

nodule

shows

hepatocellular

MR image shows with low signal iron

numerous intensity.

low-signal-intensity (c) Histologic section

nodules (Prussian

(arrows). blue stain;

as blue.

October

1992

Close

monitoring

of patients

with

nodules

ties,

may i2

with large

MR

be prudent.

large

In one

regenerative

biopsy.

larged

by

the

examination,

time

se-

and of

All 12 lesions of the

had

en-

malignancy was diagnosed in 10 (59). Some recommend

with US guidnodules (56).

Large regenerative nodules that accumulate iron (46,54,58) or fat (60) appear

to have

tential topsy

greater

than

other

series

noted

malignant

nodules.

po-

One

malignant

effects

growth

associated

nantly with

au-

foci

(58).

to the

consisting

or high

signal

shows a rust-colored nodule magnification, x 100) shows

from

liver transplant blue stain; original

focus

patient

remains

well 2 years

intensity

(Fig

nodules

also

after

liver

(black dense

transplantation.

regenerative a small focus arrow), staining

(Reprinted,

14.

HCC,

rows)

with

nodular

active

cirrhosis.

with signs of malignancy heterogeneity. Most

Note

that

hepatic

signal

is almost

unlikely.

185

#{149} Number

1

causes focus nodule,

cyst,

As small

differentiated,

13)

such

as these

can

mor,

and

such

as a-fetoprotein,

a as

are

fail

usually

of nodules

to disclose

markers

hi-

for HCC,

are usually

nor-

mal in patients with small tumors (61). Since regenerative nodules are delineated and characterized best by

If

MR may

nodule. of relatively

with

may

of a within such

biopsy

serologic

mdi-

are extremely

HCCs

well

imaging, be useful

MR guidance in selected

(a) SE 2,500/50 MR image increased signal intensity a small pale regenerative

permission,

as high

contrast-enhanced with the remainder

from

reference

for biopsy patients.

shows numerous (small arrow).

focus (white nodules (N),

as that

MR images. (a) SE 2,500/100 MR image of the liver, which has increased signal

of subcutaneous

fat. (b) TI-weighted

flip angle shows the mass (large arrows) as increased signal intensity relative to the remainder of the sion is noted posteriorly (small arrow). (c) Image obtained with same parameters used for b, less than lion of gadopentetate dimeglumine. The mass (arrows) enhances less than the remainder of the liver,

Vnlij

potential

perbe

arrow). sparing

(c) Histoa small

58.)

c.

on T2-weighted and of the mass is isointense

intensity

Other

Alternatively, might

high-signal-intensity low-signal-intensity

which contains of iron in the

b.

a. Figure

focus

is considered a and if no other le-

evident. treatment

an intranodular

exhibit rapid growth and malignant potential (41,60). Regenerative nodules should be examined carefully for internal foci. such lesions are found, it might be prudent to proceed directly to sur-

(b) Gross

(Prussian of HCC (C). The

cated.

nodat MR

nodule of interme-

dysplastic

if the patient surgical risk

sions are cutaneous

of a predomi-

HCC within a large iron-containing of which (large arrows) contains

specimen

gery good

(54).

within siderotic appearance

low-signal-intensity a small internal Fatty

iron-accu-

nodules tumor-en-

or to the rapid with regeneration.

Figure 13. Pathologically proved small low-signal-intensity nodules, the largest logic section

large

of iron

HCC occurring ules has a unique

diate

percutane-

ous injection of ethanol ance into large dysplastic

hancing

imaging,

follow-up

and

eventually investigators

19 of 26 (73%)

mulative-regenerative This may be due

nodules

were detected at sonography diagnosed as benign by means

guided

within

imaging

regenerative

GRE

102/2.3

shows

a mass

intensity

MR image

(ar-

due

to

with

liver. A second high-signal-intensity 1 minute after intravenous administrawhich is evidence of malignancy.

Radiology

900

le-

#{149} 9

normal

HCC

Examination morphology

of signal intensity and on MR images may be for distinguishing between

helpful

HCC and regenerative

or hyperplastic nodules are often hyperintense on Ti-weighted MR images and isointense or hypointense on T2-weighted MR images; they are rarely if ever hyperintense on T2-weighted images (57). While most HCCs have high signal intensity on T2-weighted images, some welldifferentiated HCCs have signal characteristics resembling those of hyperplastic nodules (40,62), consistent with the histologic similarity between these two lesions. nodules.

obstruction

Hyperplastic

Careful analysis phology is essential

HCC. Internal

of internal morfor diagnosing

foci

signs

of malignancy;

the

former occur in early, well-differentiated HCC, and the latter occur with more advanced tumors. Benign nodules have smooth margins and lack capsules (Fig ii). Enhancement

patterns

for benign

are

malignant nodules. nodules are supplied by the portal vein, similar the remainder of the liver, while HCCs are supplied almost exclusively by the

hepatic

enhances

artery.

Thus,

liver

1.

to

2.

3.

the

portal venous phase following a bolus of contrast material (Fig 14) (63). Arterial portography is even more reliable for this differentiation (64). This distinction is not absolute, however, since early, well-differentiated HCC often retains some portai perfusion, and benign dysplastic nodules have relatively increased arterial per-

4.

fusion.

Additionally,

7.

severe

cirrhosis

portal

perfusion

patients have

with

arterial perfusion. Nodular hepatic parenchyma may be noted in patients with sarcoidosis (65), although it may be difficult to determine whether the nodularity is due to granulomas or coincidentally present cirrhosis.

CONCLUSION Normal hepatic parenchyma has Ti and T2 relaxation times that differ from those of many normal and ab#{149} Radiology

6.

he-

patic

10

5.

decreased

and increased

I am indebted

12.

vessels.

to Simon

13.

14.

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slat Tomogr 16.

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15.

Allen-Moore

early

often

hepatic

tography; Ludlle Aquillone and Peter Natale for technical assistance; Drs Hie-Won Hann, Santiago Munoz, Paul Martin, and Michael Moritz for clinical collaboration and abundant case referrals; and Drs Raphael Rubin and Juan Palazzo for pathologic correlation.

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during

patho-

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of major

Acknowledgments: Vinitski, PhD,

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Under

MR imaging is a versatile modality that can identify hepatic parenchymal damage, accumulation of fat or iron, and abnormal vessels, thereby providing numerous parameters for detecting and characterizing focal, diffuse, and vascular hepatic alterations. Judidous use of MR imaging should help clarify hepatic diagnosis, in many cases preventing confusion due to focal manifestations of diffuse liver disease. #{149}

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