AJR 2003; 180:1351-1357
© American Roentgen Ray Society
Dynamic Subtraction MR Imaging of the Liver: Advantages and Pitfalls
Jeong-Sik Yu1,2 and
Neil M. Rofsky1
1 All authors: Department of Radiology, Beth Israel Deaconess Medical Center,
330 Brookline Ave., Boston, MA 02215.
2 Present address: Department of Diagnostic Radiology, Yonsei University College
of Medicine, YongDong Severance Hospital, 146-92 Dogok-Dong, Gangnam-Gu, Seoul
135-270, South Korea.
Received September 10, 2002;
accepted after revision October 31, 2002.
Address correspondence to N. M. Rofsky.
Introduction
Gadolinium-enhanced dynamic MR imaging is a key strategy in imaging of the
liver. An optimized arterial phase imaging protocol
[1] implemented with
three-dimensional imaging techniques yields arterial phase MR examinations
that minimize partial volume artifacts and allow high-quality multiplanar
reformations [2,
3]. These innovations are aimed
toward achieving improved lesion detection and characterization as well as the
ability to generate high-quality angiograms from a single acquisition.
Subtraction of unenhanced images from gadolinium-enhanced images has been
pursued in an attempt to maximize the qualitative recognition of lesion
enhancement and vascular anatomy
[4,
5].
MR Imaging Technique
MR imaging was performed using a 1.5-T unit (Symphony or Vision; Siemens,
Erlangen, Germany) with a torso phased array coil. In all patients, a
three-dimensional spoiled gradient-echo sequence with fat suppression was used
as previously described [2].
After an unenhanced data set was obtained during end-expiration, a timing
examination was performed according to the previously described method
[1] using a 1-mL test dose of
gadopentetate dimeglumine (Magnevist; Berlex, Wayne, NJ). Before patients
underwent scanning, they were educated about the performance of end-expiration
breath-holds.
For arterial phase imaging, all patients received a 19-mL bolus of contrast
material through an arm vein with an MR-compatible power injector (Spectris;
Medrad, Pittsburgh, PA). After the arterial phase, imaging was repeated twice
at 45-sec intervals for portal vein and equilibrium phase acquisitions.
Unenhanced images were subtracted from enhanced images during arterial,
portal, and equilibrium phases on the MR console, using the system's
commercially available software. The arterial phase subtraction data set was
also used to produce maximum intensity projections with a restricted volume of
interest for MR angiography. For detailed evaluation of venous anatomy in some
patients, arterial phase images were subtracted from the portal venous phase
images.
Advantages of Subtraction Imaging
Characterization of T1 Hyperintense Lesions
Regenerative nodules, dysplastic nodules, and hepatocellular carcinomas can
all exhibit high signal intensity on unenhanced T1-weighted MR images in the
cirrhotic liver. For these lesions, arterial enhancement is often difficult to
detect using a subjective comparison of the unenhanced and enhanced images.
The presence of arterial enhancement strongly suggests the diagnosis of
hepatocellular carcinoma because contrast enhancement of other cirrhotic
nodules is rare [6]. Arterial
enhancement within a nodule can be visualized on the subtraction image as high
signal intensity exceeding that of background parenchyma (Figs.
1A,
1B and
1C). However, for most benign
and borderline cirrhotic nodules, the degree of nodular arterial enhancement
is not well delineated from background parenchyma on subtraction images.
Subtraction images are also helpful in assessing for enhancement and hence for
the viability of treated tumors, especially in lesions that may also appear
bright on T1-weighted images, such as lesions with coagulation necrosis or
internal hemorrhage (Figs. 2A,
2B).
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Fig. 1A. —64-year-old man with alcoholic cirrhosis complicated by
multifocal hepatocellular carcinomas. Transverse unenhanced volumetric
interpolated breath-hold MR image (TR/TE, 4.2/1.9; flip angle, 12°) shows
hyperintense nodule (arrow) in right lobe of liver.
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Fig. 1B. —64-year-old man with alcoholic cirrhosis complicated by
multifocal hepatocellular carcinomas. Transverse arterial phase dynamic MR
image shows hyperintense nodule (arrow) and two small enhancing
lesions (arrowheads).
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Fig. 1C. —64-year-old man with alcoholic cirrhosis complicated by
multifocal hepatocellular carcinomas. Subtracted arterial phase MR image
(B – A) shows distinct enhancement of hyperintense nodule
(arrow) and two other smaller lesions (arrowheads).
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Fig. 2A. —54-year-old man with hepatocellular carcinomas treated with
percutaneous radiofrequency ablation 6 months earlier. Transverse unenhanced
volumetric interpolated breath-hold MR image (TR/TE, 4.5/1.9; flip angle,
12°) shows 4.5-cm focus with very high signal intensity component in
center of lesion surrounded by moderately hyperintense component
(arrow) in posterior segment of right lobe of liver. Another small
hyperintense lesion (arrowhead) is also visible.
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Fig. 2B. —54-year-old man with hepatocellular carcinomas treated with
percutaneous radiofrequency ablation 6 months earlier. Subtracted arterial
phase MR image shows no evidence of contrast enhancement of treated lesion
(arrow) and smaller necrotic focus (arrowhead) along
transhepatic tract of electronic probe. Heterogeneously strong enhancement of
surrounding liver resulted from extensive tumor invasion of right portal
vein.
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Detection of Hypervascular Lesions Unidentified on Contrast-Enhanced
Images
Some small enhancing lesions are not identified on contrast-enhanced images
because their signal intensity is similar to that of background liver. After
subtraction, visual conspicuity of the enhanced lesions can be increased to
facilitate the detection of focal lesions with contrast enhancement (Figs.
3A,
3B).
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Fig. 3A. —57-year-old woman with liver metastases from breast cancer.
Transverse arterial phase volumetric interpolated breath-hold MR image (TR/TE,
4.2/1.9; flip angle, 12°) shows contrast enhancement of 4-cm lesion
(arrow) between area of right and left lobe of liver. On unenhanced
images at same slice level (not shown), there were two more hypointense small
lesions adjacent to main lesion.
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Fig. 3B. —57-year-old woman with liver metastases from breast cancer.
Subtracted arterial phase MR image shows distinct enhancement of two smaller
lesions (arrowheads) as well as main lesion (arrow). Note
perihepatic high-signal-intensity rim anterior to liver.
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Visualization of Enhancing Pseudocapsules
The conspicuity of the marginal or peritumoral enhancing rim is increased
on subtraction images generated from portal or equilibrium phase images. This
finding helps characterize focal lesions with fibrotic pseudocapsules (Figs.
4A,
4B). For tumor evaluation in
patients who have undergone localized ablation therapy, the integrity of the
enhancing rim can be used as a marker of surrounding inflammatory reaction in
the acute or subacute stage after treatment
[7] (Figs.
5A,
5B). In contradistinction,
residual tumor shows irregularity or partial disruption of the rim.
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Fig. 4A. —64-year-old man with alcoholic cirrhosis complicated by
multifocal hepatocellular carcinoma. Transverse portal venous phase volumetric
interpolated breath-hold MR image (TR/TE, 4.2/1.9; flip angle, 12°) shows
one isointense lesion (arrow) and one hypointense lesion
(arrowhead), each surrounded by thin hyperintense rim.
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Fig. 4B. —64-year-old man with alcoholic cirrhosis complicated by
multifocal hepatocellular carcinoma. Subtracted portal venous phase MR image
enables more conspicuous visualization of enhancing pseudocapsules
(arrowheads) of two hepatocellular carcinomas.
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Fig. 5A. —63-year-old man with hepatocellular carcinoma treated with
percutaneous radiofrequency ablation 1 month earlier. Transverse equilibrium
phase volumetric interpolated breath-hold MR image (TR/TE, 4.5/1.9; flip
angle, 12°) shows indistinct peritumoral rim enhancement (arrow),
suggesting hyperemia without definite enhancement of tumor.
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Fig. 5B. —63-year-old man with hepatocellular carcinoma treated with
percutaneous radiofrequency ablation 1 month earlier. Subtracted equilibrium
phase MR image shows unequivocal rim enhancement (arrowheads) around
treated tumor with complete integrity.
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Delayed Enhancement of Tumor
Gradual and delayed enhancement in tumors resulting from diffusion of
contrast medium into the tumoral interstitium or intercellular sinusoids can
be easily detected on subtraction images from the equilibrium phase (Figs.
6A,
6B).
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Fig. 6A. —46-year-old woman with liver metastases from breast cancer.
Transverse equilibrium phase volumetric interpolated breath-hold MR image
(TR/TE, 4.5/1.9; flip angle, 12°) shows targetoid, inhomogeneous contrast
enhancement of 3.5-cm lesion (arrow), but signal intensity is similar
to that of background liver.
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Fig. 6B. —46-year-old woman with liver metastases from breast cancer.
Subtracted equilibrium phase MR image shows distinct enhancement of lesion
(arrow). Inner portion of tumor is more densely enhanced than outer
portion except for central necrotic focus. This pattern is compatible with
enhancement pattern of hypervascular metastatic lesion on delayed phase
contrast-enhanced imaging (not shown).
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Differentiation Between Malignant and Bland Thrombi in the Portal
Vein
Contrast enhancement of portal vein thrombi helps distinguish malignant
portal vein thrombosis from bland (nonenhancing) thrombosis in the cirrhotic
liver [8]. Increased
conspicuity of contrast enhancement is seen on subtraction images, which also
assists in determining the extent of tumor thrombi as distinguished from bland
thrombus (Figs. 7A,
7B,
7C and
7D).
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Fig. 7A. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Transverse portal venous
phase volumetric interpolated breath-hold MR image (TR/TE, 4.2/1.9; flip
angle, 12°) shows marked expansion of left portal vein by malignant tumor
thrombus (arrow) with lower signal intensity distinguished from
background liver.
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Fig. 7B. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Transverse portal venous
phase MR image obtained at level 4 cm below A shows
low-signal-intensity bland thrombus (arrow) in main portal vein.
Inhomogeneous enhancement of hepatocellular carcinoma mass
(arrowhead) is also seen in left lobe.
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Fig. 7C. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Subtracted portal venous
phase obtained at same level as A reveals contrast enhancement in tumor
thrombus (arrow) with similar degree of contrast enhancement in
background liver.
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Fig. 7D. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Subtracted portal venous
phase MR image obtained at same level as B shows dark signal of bland
thrombus (arrow), representing absence of contrast enhancement, that
can be easily distinguished from enhancing tumor thrombus in C.
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Detailed Assessment of Vascular Anatomy
Suppression of background signals by subtraction of unenhanced images from
the arterial phase images increases the vessel-to-background contrast, thus
permitting better visualization of small arterial branches (Figs.
7E and
7F). Subtraction of the
arterial phase data set from the venous phase data set (the latter containing
both arteries and veins) can generate high-quality
maximum-intensity-projection MR venograms (Figs.
7G,
7H,
7I).
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Fig. 7E. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Coronal nonsubtracted
maximum-intensity-projection MR image obtained during arterial phase with
restricted volume of interest shows celiac axis, superior mesenteric artery,
and renal arteries.
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Fig. 7F. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Arterial phase subtracted
MR angiogram shows that suppression of background signal results in better
visualization of peripheral branches of right hepatic artery (arrows)
and splenic artery (arrowhead) than E.
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Fig. 7G. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Nonsubtracted
maximum-intensity-projection MR image obtained during portal venous phase
shows arterial and venous structures (arrowhead) with substantial
background signal that obscures some venous anatomy. Asterisks = kidneys.
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Fig. 7H. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. Subtraction image yielded
from subtraction of unenhanced data set from portal venous phase data set
allows improved visualization of veins (arrows) and also shows
arterial structures (arrowheads) and kidneys
(asterisks).
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Fig. 7I. —31-year-old man with B-viral cirrhosis complicated by
hepatocellular carcinoma and portal vein thromboses. This image resulted from
subtraction of arterial phase data set from portal venous phase data set. It
shows splenic and splanchnic venous confluence into main portal vein
(black arrow) up to level of obstruction by bland thrombus better
than G and H. Suppression of overlapping signals from arterial
components and contrast enhancement of kidneys yield improved details of
venous structures, including hepatic veins (white arrow).
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Pitfalls of Subtraction Imaging
Erroneous Coregistration Between Unenhanced and Enhanced Source
Images
A certain degree of slice misregistration is physiologically inevitable,
although this factor is not problematic for most examinations that are
performed using end-expiration breath-holds. A hyperintense, nonenhancing
lesion on unenhanced images could erroneously be designated as an enhancing
lesion with poor image coregistration and could yield a false impression of a
hypervascular tumor (Figs. 8
and 9A,
9B,
9C,
9D). As an alternative,
hypointense lesions on unenhanced images subtracted by hepatic parenchyma on
contrast-enhanced images can yield hyperintense pseudolesions on subtraction
images (Figs. 8 and
10A,
10B). Adjacent slices with
marked hypointense and hyperintense lesions of identical size and position on
subtracted images are indicators of axial misregistration (Figs.
9A,
9B,
9C,
9D and
10A,
10B).
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Fig. 8. —Schema of misregistration and erroneous determination of
enhancement between unenhanced and contrast-enhanced source images. On upper
row images, level of contrast-enhanced image is lower than level of unenhanced
image. In this case, high-signal lesion on unenhanced image (1) is subtracted
from isointensely enhanced liver parenchyma on contrast-enhanced image, which
can result in signal void artifact (2) on subtracted image. Also at more
inferior level, normal unenhanced liver parenchyma is subtracted from
hyperintense (but not enhanced) lesion that is present on contrast-enhanced
image set. This results in appearance of hyperintense nodule (3) on subtracted
image giving false impression of hypervascular tumor. To contrary, hypointense
lesion (4) on unenhanced image when subtracted from normally enhanced
parenchyma can create hyperintense signal (5) at more superior level and
hypointense signal on more inferior level after subtraction. On lower row
images, level of contrast-enhanced image is higher than unenhanced image, and
same effect yields reciprocal result compared with upper row images.
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Fig. 9A. —56-year-old man with benign or borderline cirrhotic nodules
unchanged during 11 months of MR imaging follow-up with slice misregistration
between unenhanced and contrast-enhanced source images. Transverse unenhanced
volumetric interpolated breath-hold MR image (TR/TE, 4.5/1.9; flip angle,
12°) shows small hyperintense nodule (arrow).
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Fig. 9B. —56-year-old man with benign or borderline cirrhotic nodules
unchanged during 11 months of MR imaging follow-up with slice misregistration
between unenhanced and contrast-enhanced source images. Subtracted arterial
phase MR image obtained at same level as A shows low signal
(arrow) corresponding to hyperintense nodule on A. Hypointense
area resulted from erroneous subtraction of T1 hyperintense nodule from normal
enhanced liver parenchyma on contrast-enhanced image obtained 1 cm below
A (not shown).
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Fig. 9C. —56-year-old man with benign or borderline cirrhotic nodules
unchanged during 11 months of MR imaging follow-up with slice misregistration
between unenhanced and contrast-enhanced source images. Subtracted arterial
phase MR image obtained 1 cm above A shows hyperintense nodule
mimicking hypervascular tumor (arrow). High-signal lesion resulted
from erroneous subtraction of unenhanced liver parenchyma by hyperintense (but
nonenhancing) nodule on arterial phase image (not shown).
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Fig. 9D. —56-year-old man with benign or borderline cirrhotic nodules
unchanged during 11 months of MR imaging follow-up with slice misregistration
between unenhanced and contrast-enhanced source images. Six-month follow-up
subtracted arterial phase MR image shows eccentric hyperintense
(arrow) and hypointense (arrowheads) area corresponding to
hyperintense nodule on A and arterial phase image (not shown) due to
slight misregistration between source images in transverse plane.
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Fig. 10A. —55-year-old man with hepatitis C viral cirrhosis. Transverse
arterial phase volumetric interpolated breath-hold MR image (TR/TE, 4.5/1.9;
flip angle, 12°) shows small cyst (arrow) in left lobe of
liver.
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Fig. 10B. —55-year-old man with hepatitis C viral cirrhosis. Subtracted
arterial phase MR image obtained 0.5 cm above A shows hyperintense
nodule (arrow) mimicking hypervascular tumor. Subtracted arterial
phase image (not shown) obtained at same level as A showed small signal
void corresponding to small cyst on A.
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When the degree of slice misregistration is smaller than the lesion,
eccentric or ringshaped pseudolesions can appear, depending on the direction
of the erroneous coregistration (Figs.
9D and
11). For lesions located in
the marginal subcapsular area of the liver, the lesions tend to be erroneously
subtracted by extrahepatic structures. In cases of small lesions, recognition
of the lesion and the corresponding high-or low-signal-intensity pseudolesions
on subtraction images is more difficult in lesions in the subcapsular portion
than in centrally located lesions.
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Fig. 11. —Artifact resulting from erroneous misregistration on
nonenhanced subtracted arterial phase volumetric interpolated breath-hold MR
image (TR/TE, 4.5/1.9; flip angle, 12°) of 32-year-old woman with
polycystic liver and kidney disease. All eccentrically white signals
(arrowheads) on posterior portion of each hypointense lesion in right
lobe of liver result from slight axial and transverse misregistration between
nonenhanced and contrast-enhanced source images.
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Coarsening of Background Signals in Cirrhotic Liver
In the cirrhotic liver, the gross and microscopic structural distortions of
liver parenchyma and vascular systems yield inhomogeneous perfusion of the
liver after contrast administration. This finding is particularly seen on the
arterial phase of contrast administration. Heterogeneous parenchymal
enhancement when coupled with imperfect slice coregistration can limit the
confident detection of small, subcentimeter nodules on the subtraction images,
even if very thin sections inherent to three-dimensional acquisitions have
been used.
Conclusion
Properly coregistered dynamic subtraction MR imaging can facilitate the
assessment of focal liver lesions and a detailed evaluation of vascular
structures. However, an inevitable limitation for evaluation of small focal
hepatic lesions originates from the erroneous coregistration between the
unenhanced and contrast-enhanced images. Careful review of both the source and
subtraction images is crucial to avoid a false determination of focal lesion
enhancement. The development of userfriendly, reliable error–correction
processing strategies for subtraction imaging is needed to fully exploit the
advantages of subtraction techniques and to minimize the pitfalls.
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Introduction
MR Imaging Technique
