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297

MR Imaging of the Portal Venous System: Value of Gradient-Echo Imaging as an Adjunct

Paul M. Silverman1 Richard H. Patt Brian S. Garra Steven C. Horii Cirrelda Cooper Wendolyn S. Hayes Robert

K. Zeman

to Spin-Echo

Imaging

We evaluated the use of gradient-echo (GRE) as an adjunct to spin-echo (SE) MR imaging of the portal venous system. GRE imaging was performed in 31 subjects, 15 normal volunteers and 16 patients with documented portal venous disease (15 cases) or suspected

disease

(one

case).

Eight

of 16 patients

had complete compression by tumor. Of the two other the other a falsely positive angiogram, focal

thrombus,

subjects,

GRE

intravascular subjects

signal

and

and

that

identified

scans

had

signal three

excellent

patients

could

visualization

compared

with

had

mimic

clot.

of the

surrounding

an artifact

In three

on GRE but not on SE images.

had

venous

thrombosis,

five

had

occlusion. Six patients had extrinsic venous patients, one had an arteriovenous fistula and suggesting portal vein occlusion. In normal

three

consisting

of five

portal

venous

tissues.

Nine

system

(60%)

of a curvilinear

patients

with

In all three patients

area

focal

with

high

of 15 normal of decreased

thrombus,

with occlusion,

clot

was

SE and GRE

images demonstrated similar findings. In five of the six patients with extrinsic venous compression by tumor, SE and GRE studies showed similar findings. Of the other two patients, an arteriovenous fistula was seen on GRE MR in one, and in the other, patency of the left portal vein was seen on SE and GRE images after angiography had suggested portal vein occlusion. Collateral vessels were seen in nine of 16 patients. In five of nine cases, GRE MR demonstrated more extensive collaterals than did SE MR. In summary,

GRE

MR

provides

a useful

adjunct

to standard

include high contrast between vascular structures and motion artifact, and rapid scanning within a breath-hold. AJR

157:297-302,

August

SE

MR

surrounding

imaging.

Benefits

tissues,

reduced

1991

Noninvasive accomplished

imaging of the portal venous system (PVS) has been successfully with a variety of imaging techniques, including sonography, CT, and MR imaging [1 -8]. Doppler sonography has proved to be highly accurate in determining the presence, direction, and velocity of portal blood flow, but is operator dependent [1 , 9-1 1 ]. Although contrast-enhanced CT with dynamic scanning is sensitive in identifying thrombus in the main portal vein as well as large branch vessels, suboptimal opacification of portal vessels, occasionally may limit this examination.

(SE) MR provides

Spin-echo

without

the

necessity

related artifacts, in the Received December revision March 7, 1991.

14, 1990:

accepted

after

clearly

‘All authors: Department of Radiology, Georgetown University Hospital, 3800 Reservoir Rd., NW., Washington, DC 20007. Address reprint requests

to P. M. Silverman. 0361-803X/91/1572-0297 © American

Roentgen

quences vascular

Ray Society

of using

including

anatomic

information

IV contrast

flow-related

enhancement,

portal

vein that mimic thrombus [1 2-14]. have been used in the abdomen and

structures distinguishes

[2, 1 5, 1 6]. The high-intensity the

intraabdominal

similar to that provided

material.

vasculature

However,

may produce

motion

spurious

Gradient-echo (GRE) peripheral extremities

signal produced from

signals pulse Seto image

by flowing

surrounding

by CT

and flow-

blood

stationary

tissues. Additionally, the acquisition time is significantly reduced when using GRE imaging as compared with conventional SE imaging. This allows slice acquisition during a single breath-hold, minimizing motion-related artifact. We have reviewed our experience with GRE imaging of the portal vein in 31 subjects, 1 5 normal volunteers and 1 6 patients with portal vein abnormalities. The

purpose

of the study

adjunct

to standard

Subjects

GRE imaging

as an

including patients

subjects

underwent

MR

imaging

of the

upper

abdomen

the PVS. Fifteen were normal volunteers and 1 6 were in whom portal venous abnormalities were proved on CT (13

teers, 1 0 men and five women, were 1 5-55 years old. The 16 patients, 1 1 men and five women, were 43-77 years old (mean, 60 years). Eight of the sixteen patients had intrinsic thrombus in the

PVS. Five patients had focal thrombus occlusion.

Two

of these

and three had complete

patients

had

cirrhosis.

Six

portal

patients

had

extrinsic compression of the main or proximal right or left portal vein by tumor. Abnormalities included metastases (two patients), pancreatic neoplasm (two patients), lymphoma (one patient), and hepatoma (one patient). One patient had an arteriovenous fistula and the

other afalse-positive

angiogram

suggesting

occlusion

ofthe left portal

vein. All 31 subjects underwent GRE imaging of the portal vein performed at 1 .5 T (Siemens, Magnetom, Erlangen, Germany). Fast imaging with steady-state free precession (FISP) was performed in

all 31 cases. First-order

(velocity)

flow compensation

the slice and frequency-encoding included 50/1 4/45#{176}/i (TR/TE/flip acquisition

matrix,

and

a 5-mm

sec for each breath-hold holding their fast-low-angle

FLASH acquisition

was applied in

directions. FISP scan parameters angle/excitation), a 256 x 256 slice

thickness.

Imaging

time

was

16

image. Five of the patients who had difficulty

breath for this time had additional GRE imaging with shot (FLASH) imaging, requiring only 9 sec per image.

technical

parameters

matrix,

and

included

a 5-mm

slice

30/i 0/30#{176}/i , a 128 x 128 thickness.

Maximum-intensity-

projection (MIP) angiographic MR images in the coronal plane were produced in eight patients to supplement standard GRE images. MIPs were calculated on a 256 x 256 grid from a stack of twodimensional GRE slices. Images were viewed at rotational angles from -30#{176}to +30#{176} from the coronal plane at fixed 6#{176} intervals. Reconstruction time was approximately 5 sec per view for a total time

of approximately

1 mm depending

on the

number

of raw

images

used.

Standard

SE imaging was performed 256 x 256 matrix, and a routine 1 0-mm

coverage Thirteen

by using 500/i 5/4 or 8, a thickness to provide enough

to include the entire liver. Six of the 15 volunteers

of the i 6 patients of the

underwent i

and iS

SE imaging.

6 patients

underwent

with a GE 9800 scanner (General imaging. In all cases, enhanced

CT of the upper abdomen

Electric, Milwaukee, WI) before MR scans were obtained dynamically

with a power injector, i .0-i .2 mI/sec (Mark IV, Medrad, Pittsburgh, PA). Scans were obtained at i -cm intervals as part of the standard examination sonographic

of the

upper

evaluation,

abdomen. including

Eight color

of the Doppler

patients flow

also

had

assessment

(Ultramark 9, Advanced Technology Laboratories, Bothell, WA) and four patients had angiographic assessment of the liver and PVS. GRE and SE scans in the volunteers were reviewed to assess the normal appearance of the main portal vein and its major radicles.

GRE scans were also specifically

assessed

for any potential

artifacts

that might be confused with thrombus. In the i 6 patients with portal vein abnormality, GRE imaging was compared with SE imaging in i 5 of i6 patients and with CT scans in 1 3 of i 6 patients. Scans were compared to assess the presence and extent of intrinsic portal vein thrombosis, extrinsic vascular compression, and portal vein collaterals. Detailed statistical analysis was not feasible because of the small number of patients studied. In the five patients with thrombus, the CT criterion for thrombus was a focal

area of decreased hancement.

In three

to identify

in the other

cases), Doppler sonography (eight cases), and angiography (four cases). Angiography was false-positive in one case. The 1 5 volun-

vein

inability

density patients,

in the PVS surrounded total occlusion

a patent

main

portal

vein

and

numerous

enhancing

periportal collaterals. In the six patients with extrinsic portal venous compression, CT demonstrated porta hepatis adenopathy in four (two with pancreatic neoplasm, one with metastatic disease, and one with lymphoma) and intrahepatic metastases and primary hepatoma

of the PVS.

and Methods

Thirty-one

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was to evaluate

SE imaging

by contrast

was established

en-

by the

two.

In one

patient,

an arteriovenous

fistula

was

confirmed

by angiography; in the other, a false-positive angiogram suggested occlusion of the left portal vein. The false appearance of occlusion

was related to a portion of the vessel being seen “end on” angiographically and confirmed nine

of the

i

to be patent

6 patients,

by CT and Doppler

collateral

sonography.

In

vessels were seen on at least one

imaging study (CT, sonography, or angiography). In patients with collaterals, the extent of collateralization, including periportal, mesenteric, perisplenic, retroperitoneal, and pencholecystic collaterals, was evaluated on SE MA, GRE MA, and CT. When Doppler sonography

(eight

patients)

or angiography

(four

patients)

was

performed,

the information from these studies agreed with CT findings. In all patients, MA, CT, and Doppler sonographic examinations were performed within 2 weeks of one another. All studies were reviewed by two

observers,

with

tion consisted parison with

performed

consensus

achieved

in each

case.

Initial

evalua-

of direct assessment of SE MA and GRE MR. ComCT, Doppler sonography, and angiography was also

when these examinations

were available.

Results

GRE imaging was performed in all normal volunteers and showed high signal intensity in all the major intraabdominal vascular structures, including the PVS. In all cases, the main, left, and right

portal

veins

were

subjects,

a linear

or curvilinear

intensity

was noted

in the portal

imaged

successfully.

In nine

area of decreased

signal

vein (Fig. 1). In four cases,

it

was isolated to the main portal vein, and in five cases it extended into the right or left branches of the main portal vein.

Standard

SE imaging,

performed

in six of nine

volun-

teers, confirmed this as an artifact by demonstrating a normal PVS. Supplemental scanning in the coronal plane also confirmed the artifactual nature of this decreased signal. Intrinsic PVS thrombus or occlusion was demonstrated in eight of 1 6 patients. When thrombus was seen on SE images,

it appeared as an area of high signal intensity replacing the normal flow void in the portal vein; on GRE images, it was seen as an area of decreased signal these areas of clot were separate

intensity. On SE images, from regions of artifact

generated from pulsatile flow within adjacent vessels. In three of the five patients with focal thrombus, thrombus was demonstrated on GRE imaging but failed to be confidently identified on SE imaging (Figs. 2 and 3). In one case in which CT clearly demonstrated thrombus in the main portal vein and superior mesenteric vein, GRE and SE imaging were not conclusive. In the other case, thrombus was identified on both

SE and GRE MR. In the three cases with complete

occlusion

of the portal vein, SE and GRE imaging showed similar findings, including failure to identify the main portal vein and numerous periportal collaterals (Fig. 4). Two of these patients had findings consistent with a diagnosis of cavernous trans-

formation

of the portal vein.

Six patients had extrinsic compression of the main or proximal right or left portal vein by tumor. In five of six patients with extrinsic portal vein compression, similar findings were

demonstrated

on SE and GRE imaging

with

5). In one case,

identify

CT (Fig.

the extrinsic

on SE imaging.

compression

Although

GRE

that correlated

imaging

of the

right

was portal

GRE and SE imaging

well

unable vein

to

seen

both showed

Fig. 1.-Artifact on axial GRE MR image. A, Axial GRE 50/14/45#{176} MR image of normal volunteer shows curvilinear artifact in main and right portal veins (arrowheads). B, Coronal GRE image does not substantiate any consistent defect in portal venous system.

Subtie lucencies

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signal

Intensity

lack sharp margins seen

and low

with thrombus.

Fig. 2.-Portal vein thrombus equivocal on SE but diagnostic on GRE MR images. A, CT scan at level of main portal vein (arrow) shows low attenuation in main portal vein consistent with thrombus. B, SE 500/15 MR image shows spurious signal within aorta (curved arrow). Lack of clear flow void in aorta and main portal vein (straight arrow) does not allow confident diagnosis of portal vein thrombosis. C, GRE 50/14/45#{176} MR image. High signal in aorta (curved arrow) indicates flowing blood, and distinct lack of signal in main portal vein (straight arrow) is consistent with thrombosis. Dramatic contrast between flowing blood and clot allows a more confident diagnosis of portal vein thrombosis.

Fig. 3.-Portal vein thrombus identified on GRE but not SE MR images. A, CT scan shows clot in portal vein (solid arrows) with patent lumen medially (arrowhead). Subtle evidence of perisplenic arrows). B, SE 500/15 MR image shows artifact. Clot could not be diagnosed confidently. Note high-signal artifact (arrowhead) in area CT and Doppler sonography and a relative signal void in area of documented clot (arrows). Perisplenic collaterals are not seen. C, GRE 50/14/45#{176}image shows findings similar to those on CT with clot peripherally (solid arrows) and a patent lumen medially collaterals are best seen on GRE image (open arrows).

collaterals with

is seen

documented

(arrowhead).

(open flow

on

Perisplenic

SILVERMAN

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300

ET

AL.

AJR:157,

Fig. 4.-Occluded main portal vein and extensive collaterals seen on SE and GRE MR images. A, CT scan shows extensive periportal collaterals (solid arrows) due to occlusion of main portal vein. Low-attenuation areas disease. Retroperitoneal, mesenteric, and perisplenic collaterals are present (open arrows). B and C, SE 500/15 (B) and GRE 50/14/45#{176} (C) MR images show findings similar to those seen on CT, with numerous arrows). Additional collaterals appear as on CT (open arrows).

in liver represent periportal

August

1991

metastatic

collaterals

(solid

Fig. 5-Extrinsic compression of portal vein by lymphoma. GRE compared with SE MR shows poorer contrast between tumor and liver. A, SE 500/15 MR image shows lymphomatous tumor (1) to port. hepatis with compression of main portal vein (arrow). Tumor (T) is of low signal intensity. B, GRE 50/14/45#{176} image shows findings similarto those seen on SE MR with very mild portal vein compression (arrow). However, contrast between tumor (T) and adjacent liver is not as good.

extrinsic displayed

portal vein compression the tumor responsible

in five of six patients, GRE for the venous compression

less well than SE imaging did because of the poorer contrast between tumor and surrounding normal tissue on GRE images. In one patient, an arteriovenous fistula seen on GRE imaging

was confirmed

false-positive vein was

angiographically.

angiogram

shown

The patient

suggested

to have a patent

occlusion

in whom

a

of the left portal

vein on both

SE and GRE

MR.

Incidentally noted in three of 16 patients was focal signal within the main portal vein on standard SE imaging unrelated to areas of thrombus or vascular compression that potentially could have given the false impression of thrombus. In each

case, the GRE study, CT, or color Doppler flow sonography was normal in this segment of portal vein. The linear or curvilinear low-intensity area encountered on GRE images in normal volunteers was seen similarly in the patient group but was readily recognized as artifactual by its typical appear-

ance, correlation

In nine of the 1 6 patients,

at least one imaging

collateral

technique

vessels

were

(CT, sonography,

shown

by

In four cases, GRE and SE images were judged to be in showing these vessels. In five cases, GRE images

better

defined

presence

of collaterals

and

showed

better.

MIP imaging

did not provide

information

beyond that provided by GRE imaging, but coronal images did enhance the display of abnormalities, especially in patients with extensive

collaterals.

with other imaging normal

studies,

and experience

volunteers.

Discussion

more

extensive collateralization than was appreciated on standard SE MR (Fig. 6). CT scans were obtained in six of nine patients. In those patients, CT and GRE showed collaterals to a similar extent in four patients, whereas in two cases GRE showed the collaterals

in examining

or angiog-

raphy). similar

the

gained

The application of MR imaging in evaluating the abdominal vasculature provides a noninvasive imaging technique additional to CT and sonography. Standard assessment with SE imaging produces a typical signal void, “black-blood” phenomenon. The presence of high-intensity signal within the main portal vein is suggestive of thrombus, and the absence of a main

portal

suggestive

vein and demonstration

of complete

of tortuous

portal vein thrombosis

collaterals

is

[1 7, 1 8). The

MR

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AJA:157, August 1991

Fig. 6.-Improved

depiction

of collateral

vessels

OF

PORTAL

with GRE MR images

VENOUS

and maximum-intensity

MR images. A, SE 500/15

301

SYSTEM

MR image shows portal vein occlusion (solid arrow) and collaterals (open portal vein mimics ascites but represents a confluence of distinct collaterals. B, GRE 50/14/45#{176} image shows portal vein thrombosis (solid arrow) and more extensive C, MIP angiographic image, coronal plane, shows extensive collateralization (arrows).

projection

arrows)

(MIP)

in periportal

collateralization

images

area. Low-Intensity (open

arrows)

area around

than SE Images

occluded

does.

signal

[20]. The sequential two-dimensional acquisition method is favored over three-dimensional techniques, which are particularly sensitive to motion, as they require minutes of aCquisi-

be undetected.

Respiratory

and motion

strating

a persistently

high

signal

on late echoes

in throm-

between

with SE

create

and therefore

high contrast

compared

major pitfall in this type of imaging is caused by high signal from flow-related enhancement occurring within patent vasculature that mimics thrombus. Clot may rarely lack increased artifacts may also superimpose high signal intensity artifacts onto vascular structures, making it difficult to assess their patency. In one study, 14 patients with portal vein thrombosis were evaluated by CT, SE MR, and sonography [1 9]. Acute or subacute thrombi were hyperintense on both Ti - and T2weighted images. Chronic thrombi (greater than 5 weeks’ duration) were hyperintense in eight of 1 1 cases on T2weighted images. Although all patients had thrombosed portal vessels, MR more effectively showed the extent of thrombosis and periportal collateralization than did CT or sonography. Heavily T2-weighted, triple-echo imaging enhanced the ability to differentiate flow-related artifacts from thrombi by demon-

extremely

angiographic

flowing

blood

and

surrounding tissues. They are occasionally subject to prominent high-intensity artifacts from these vascular structures

tion rather than being accomplished within a single breathhold. In standard SE imaging, spins must remain within the slice long enough to be exposed to both 90#{176} and 180#{176} RF

pulses. With relatively rapid blood flow, washout effects dommate so that high-velocity moving spins flow out of the plane of section, yielding characteristic black-blood images. In contrast,

GRE imaging

does

not require

a 1 80#{176} refocusing

pulse,

and echoes can be received sooner after each excitation. Blood entering a slice is more fully magnetized, with each slice acting as an entry slice with flow-related enhancement. Washout effects are minimized and flowing blood generates a stronger signal. When flow compensation techniques are applied, the phase shifts that would normally result in subsequent dephasing and signal loss are minimized. In most cases, correcting for first-order “velocity” phase shifts is adequate

bosed vessels. These images, however, were significantly compromised by their poor signal-to-noise ratio. In the present study, portal venous thrombosis was seen in eight patients. In three of five patients, GRE MR showed focal thrombus not appreciated on the SE MR image. In the three patients with portal vein occlusion and in five of six patients with extrinsic portal vein compression, SE and GRE images were comparable in showing the abnormality. However, in five of nine patients with collateral vessels caused by portal vein compromise, GRE imaging more completely dem-

spins,

dimin-

ishing the bright-blood effect [15]. The high-contrast signal produced by flowing blood GRE imaging well suited to construction of MIP images. produce an angiographic effect that can enhance the of vascular disease (Fig. 6). The MIP program used

makes These display selects

onstrated

the maximum-intensity

the extent

of collateralization.

A significant

benefit

of GRE imaging compared with SE imaging was the ability to image the porta hepatis rapidly and selectively with singleslice breath-hold images, as an adjunct to the much longer SE examination. The

recent

development

of practical

techniques

for

MR

angiography has allowed further clinical application in assessing the abdominal vasculature, especially the PVS [2, 15, 16]. The “bright-blood” images produced by GRE imaging

because

additional

the TE and accentuate

compensatory

washout

voxel

gradients

would

of high-intensity

in the projected

prolong

ray, and there-

fore background signal is not additive as would occur with standard summation imaging [21]. Projectional images have the advantage

offacilitating

viewing

by displaying,

on a single

image,

the path of tortuous vessels that would otherwise need to be traced on numerous sequential images. In evaluating portal venous disease, MIPs can be a useful method of display without tual distortions

requiring invasive angiography. characteristic of these images

Some should

artifacbe rec-

]. A consistent distortion is an artifactual decrease width since the edges of vessels are less intense

ognized

[21

in vessel than

their

central

areas.

The

decreased

intensity

of the pe-

ripheral portion of vessels is related in part to partial-volume effect and in part to different flow velocities in vessels. A

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periodic

linear

dark

“striping”

artifact

may

occur

when

vessels

course obliquely between sections owing to the maximum signal intensity being shared between contiguous sections [21}. Thus, although these images provide a high-contrast angiographic

display,

individual

these

cross-sectional

pitfalls

GRE

require

slices

referral

for accurate

to

the

interpreta-

tion. Artifacts may significantly compromise the assessment of portal venous disease on MR. In three of our patients, artifactual signal in the PVS on SE imaging could have been mistaken for thrombus. In these cases, correlation with GRE imaging

and

with

other

imaging

techniques

correctly

attribute

this to artifact.

routinely

available

at the initiation

allowed

Presaturation of this study,

us to

pulses,

hepatic

arterial

flow.

Selective

although provided

presaturation

of portal

less degraded by motion poorer contrast between

artifact tumor

and normal tissues. The appearance of tumor on GRE imaging is variable and complex depending on the specific parameters used, which affect the relative contribution of Ti , T2, and T2* weighting. Increased sensitivity to magnetic susceptibility inherent in GRE imaging also compromises image quality, especially

from

artifacts

related

to curvilinear

artifact

imaging.

artifactual

The

to bowel

gas and clips.

A linear

frequently

on GRE

was encountered

able from previous

nature

of this

was

usually

recogniz-

experience

with normal volunteers and from correlation with other studies. A possible explanation of this effect is referred to as flow separation. Laminar streaming of flowing blood may occur on one side of a vessel, whereas

flow on the opposing side may be relatively slower. The rapidly flowing blood is freely replaced with fresh unsaturated spins that

appear

bright,

whereas

rated

blood

appears

darker.

the slowly A less

flowing,

likely

more

explanation

satuwould

be flow-related displacement. When blood is flowing obliquely through the scanning plane it occupies one location initially when molecules are excited and a different position later when they are encoded for readout. Because GRE images are acquired rapidly, blood would not move a sufficient distance

to make

this

a likely

explanation.

The limitations

of GRE

imaging, including poor contrast with surrounding tissues, difficulty in identifying vascular margins, and flow artifact, do not allow it at the present time to function as a gold standard for assessing

portal

In summary, imaging

of the

venous

GRE imaging portal

venous

thrombosis.

can be a useful adjunct system.

The

nondiagnostic

standard

SE imaging.

This imaging

Because thrombus generally appears as an area of decreased signal rather than increased signal, as with standard SE imaging, these images are less subject to the common pitfall of high-intensity artifacts mimicking clot. Additionally, angiographic MIP images provide a unique display that may complement standard single-slice images in demonstrating vas-

cular impression, encasement, GRE images provide limited with SE imaging

normal tissues, SE imaging.

and collateralization. anatomic resolution

and suboptimal

making

contrast

them unsuitable

between

However, compared tumor

and

as a replacement

for

not

venous flow would require specific presaturation of blood flow perpendicular to the course of the portal vein. GRE vascular images are not as susceptible as SE images to respiratory motion or pulsatile vascular artifact mimicking clot. In the six cases of extrinsic compression of the PVS by tumor, GRE imaging techniques, than SE imaging,

undergo

technique provides significant flexibility compared with standard SE MR because a few slices at a specific anatomic level can be performed to rapidly investigate potential disease.

can minimize

or eliminate high-signal artifact in blood vessels when applied perpendicularly to the direction of flow. However, even when such pulses are applied, they are routinely used to eliminate flow in the aorta and inferior vena cava and diminish respiratory artifact. Presaturation pulses may also be useful in elimmating

that they can be performed rapidly, as single breath-hold images that can be used in sick patients who might otherwise

images

to SE provide

high contrast between flowing blood, clot, and surrounding tissues. GRE imaging techniques allow marked flexibility in

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