DOI:10.2214/AJR.05.2182
AJR 2007; 188:1018-1025
© American Roentgen Ray Society
Subtraction Imaging: Applications for Nonvascular Abdominal MRI
Amit Newatia1,
Gaurav Khatri,
Barak Friedman and
John Hines
1 All authors: Department of Radiology, Long Island Jewish Medical Center,
270-05 76th Ave., New Hyde Park, NY 11040.
Received December 22, 2005;
accepted after revision July 31, 2006.
Address correspondence to J. Hines
(jhines{at}lij.edu).
Abstract
OBJECTIVE. In this article we will illustrate the role of
subtraction imaging for abdominal MRI applications.
CONCLUSION. Subtraction imaging has multiple applications for
imaging the mediastinum, abdomen, and pelvis. Removing any preexisting signal
of T1 unenhanced images causes contrast enhancement within a mass to become
more conspicuous on subtracted sequences. This is helpful when evaluating a
lesion with high signal on unenhanced T1-weighted sequences, where visual
detection of enhancement can be difficult on conventional MRI.
Keywords: abdominal imaging • dynamic MRI
Introduction
Subtraction imaging is a readily available technique that is
routinely used in MRI of the breast and in MR angiography. There have been
reports of subtraction imaging in the solid organs of the abdomen
[1-4],
however it may be underused in routine body MRI applications, including but
not limited to hepatic, renal, and adrenal imaging. This pictorial essay
illustrates scenarios in which subtraction imaging can be valuable in
characterizing a lesion and confidently arriving at a diagnosis. In
particular, subtraction imaging can be helpful in evaluating for the presence
of a neoplasm in hemorrhagic masses, complicated cysts, and other settings in
which determining the presence or absence of enhancement is critical.
Qualitative detection of enhancement within such lesions is often not a
straightforward task due to hemorrhagic or proteinaceous contents making them
hyperdense on CT or high signal on unenhanced T1-weighted MRI pulse sequences.
Subtraction imaging can make evaluation of these lesions more
straightforward.
Technique
Subtraction imaging is a technique whereby an unenhanced T1-weighted
sequence is digitally subtracted from the identical sequence performed after
gadolinium administration. By performing this operation, any native T1 signal
is removed and the remaining signal on the subtracted images is due solely to
enhancement.
Specific Applications
Simple Hemorrhage Versus Hemorrhagic Mass
In the setting of spontaneous hemorrhage within an intraabdominal organ, it
is imperative to search for an underlying lesion responsible for the bleeding.
Acute or subacute hemorrhage will be hyperdense on CT. On MRI, areas of high
signal will be present on unenhanced T1-weighted sequences because of the
presence of intracellular or extracellular methemoglobin. The presence of high
density on CT or bright signal on unenhanced T1-weighted MRI sequences makes
qualitative evaluation of enhancement difficult. However, any signal from
blood products will be removed on subtraction images, making enhancement
within a lesion much more conspicuous. Accordingly, a simple hematoma should
appear as a signal void on subtraction images because it will not contain
enhancing elements.
Within the liver, hepatocellular adenomas and carcinomas are the two
neoplasms that are most likely to spontaneously bleed. Other causes of
nontraumatic hepatic hemorrhage include HELLP (hemolysis, elevated liver
enzymes, and low platelet count) syndrome, coagulopathy, amyloidosis, and
peliosis hepatis [5]. Acute
flank pain secondary to spontaneous hemorrhage is a well-known presentation of
renal cell carcinoma (Fig. 1A,
1B,
1C,
1D,
1E). Nontraumatic adrenal
hemorrhage is relatively common. This can be due to a hemorrhagic mass such as
an adrenal cortical carcinoma, pheochromocytoma, myelolipoma, or metastasis or
it can be secondary to nonneoplastic causes such as anticoagulation, bleeding
diathesis (Fig. 2A,
2B,
2C), sepsis, stress, or trauma
[6]. In patients with an
equivocal history of trauma, subtraction imaging can be used to characterize a
complex splenic mass as either a hematoma or neoplasm (Fig.
3A,
3B,
3C).
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Fig. 1B —49-year-old woman with acute flank pain. Contrast-enhanced axial CT
scan shows peripheral areas of high attenuation (arrows); however,
differentiation of enhancement versus high-density blood is difficult.
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Fig. 1C —49-year-old woman with acute flank pain. Axial T1-weighted spoiled
gradient-recalled echo (SPGR) fat-suppressed image shows heterogeneous signal
intensity (arrowheads) within area of hemorrhage.
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Fig. 1E —49-year-old woman with acute flank pain. Axial subtraction image
confirms presence of enhancing peripheral mass (black arrows) and
signal void hematoma (white arrow). Large hemorrhagic renal cell
carcinoma was found at nephrectomy.
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Fig. 2A —74-year-old man with known history of right adrenal mass who
presented for MRI for further characterization. Axial T1-weighted
fat-suppressed spoiled gradient-recalled echo (SPGR) image shows 7-cm right
adrenal mass with areas of high signal intensity suggestive of hemorrhage
(arrow). LK = left kidney.
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Fig. 2B —74-year-old man with known history of right adrenal mass who
presented for MRI for further characterization. Axial T1-weighted
fat-suppressed SPGR gadolinium-enhanced image again shows areas of high signal
intensity (arrow). It is difficult to ascertain whether this is due
to enhancement or hemorrhage. LK = left kidney.
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Fig. 2C —74-year-old man with known history of right adrenal mass who
presented for MRI for further characterization. Axial subtraction image shows
lack of enhancement within this mass (arrow) consistent with simple
hemorrhage. Because of high clinical suspicion for malignancy, patient
underwent adrenalectomy. Pathology showed presence of hemorrhage without
evidence of neoplasm. Patient was later found to have myelofibrosis. LK = left
kidney.
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Fig. 3A —72-year-old man with hemorrhagic splenic mass on CT (not shown) and
questionable history of trauma. Axial T1-weighted fat-suppressed spoiled
gradient-recalled echo (SPGR) unenhanced image through spleen shows large
heterogeneous mass with areas of high signal intensity (arrowheads)
and more central, focal hyperintense area (arrow). S = spleen.
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Fig. 3B —72-year-old man with hemorrhagic splenic mass on CT (not shown) and
questionable history of trauma. Axial T1-weighted fat-suppressed SPGR
contrast-enhanced image shows enhancement of normal splenic parenchyma
(arrows). However, it is difficult to determine whether there is
enhancement within mass. S = spleen.
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Fig. 3C —72-year-old man with hemorrhagic splenic mass on CT (not shown) and
questionable history of trauma. Subtraction image shows definite areas of
enhancement consistent with neoplasm (arrowheads). Areas of hematoma
are signal void (arrow). Hemorrhagic lymphoma was found at
splenectomy. S = spleen.
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Other clinical settings in which subtraction images may be useful to
distinguish hematoma from tumor are in the postoperative period (Fig.
4A,
4B,
4C) and in patients receiving
anticoagulation therapy.
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Fig. 4A —25-year-old woman after attempted resection of pelvic sidewall mass.
Initial pathology only showed hematoma. MRI was performed to determine
presence of residual tumor. Axial T1-weighted fat-suppressed spoiled
gradient-recalled echo (SPGR) unenhanced image shows hyperintense mass
(black arrow) in left perivesical space, displacing urinary bladder
to right. Second mass (white arrow) of mixed signal intensity is
identified posterior and inferior in relation to this mass with displacement
of rectum and lower uterine segment to right (asterisk).
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Fig. 4B —25-year-old woman after attempted resection of pelvic sidewall mass.
Initial pathology only showed hematoma. MRI was performed to determine
presence of residual tumor. T1-weighted fat-suppressed SPGR
gadolinium-enhanced image shows similar areas of high signal intensity in both
lesions (arrows).
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Fig. 4C —25-year-old woman after attempted resection of pelvic sidewall mass.
Initial pathology only showed hematoma. MRI was performed to determine
presence of residual tumor. Axial subtraction image shows marked enhancement
of deep left pelvic mass (black arrows) confirming presence of
residual neoplasm. Left perivesical mass (white arrow) is now signal
void, consistent with postoperative hematoma. Pathologic reanalysis showed
desmoid tumor.
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Complex Cysts
Complex renal cysts often show high signal on unenhanced T1-weighted
sequences due to the presence of either intracystic hemorrhage or
proteinaceous debris. These cysts are hyperdense on CT. Subtraction imaging
has been shown to be highly sensitive for detection of enhancement within
these lesions and thus for accurate classification as either benign
hemorrhagic cysts or cystic renal cell carcinomas
[4] (Fig.
5A,
5B,
5C,
5D). Subtraction imaging
should be used for analysis of enhancement within this subset of cystic renal
masses on MRI because the use of quantitative measurements (region of interest
[ROI]) can result in false-negative results
[4]. MRI is also not subject to
pseudoenhancement artifact, which can limit evaluation of small
intraparenchymal renal masses on CT because of a correction process that
artifactually increases attenuation values
[7] (Fig.
6A,
6B,
6C,
6D).
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Fig. 5A —45-year-old man presenting with hematuria. Unenhanced CT scan shows
indeterminate hyperdense, exophytic renal mass (arrow) in midpole of
left kidney. MRI was performed to exclude underlying mass.
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Fig. 5C —45-year-old man presenting with hematuria. It is difficult to
visually determine whether high signal within mass (arrow) is due to
enhancement or to intrinsic T1 brightness from hemorrhage or protein.
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Fig. 6B —36-year-old man with metastatic disease to ribs and spine, without
known primary tumor. Axial T1-weighted fat-suppressed spoiled
gradient-recalled echo (SPGR) unenhanced image shows mildly hyperintense mass
in upper pole of left kidney (arrow).
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Fig. 6C —36-year-old man with metastatic disease to ribs and spine, without
known primary tumor. Axial T1-weighted fat-suppressed SPGR contrast-enhanced
image. It is difficult to determine whether high signal intensity within mass
(arrow) is due to enhancement or intrinsic high signal.
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Fig. 6D —36-year-old man with metastatic disease to ribs and spine, without
known primary tumor. Axial subtraction image clearly shows nodular internal
enhancement (arrow), consistent with small renal cell carcinoma.
Biopsy of bone lesion showed carcinoma consistent with renal origin.
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Cirrhotic Nodules
In the cirrhotic liver, a nodule that exhibits enhancement greater than
that of background liver on arterial-dominant gadolinium-enhanced images is
presumed to be a hepatocellular carcinoma because this degree of enhancement
is infrequently seen in dysplastic nodules and rarely seen in regenerative
nodules [2]. However,
regenerative and dysplastic nodules and hepatocellular carcinoma can all
exhibit high signal on unenhanced T1-weighted sequences
[2]. This can make qualitative
analysis of the degree of enhancement within these lesions difficult.
Subtraction imaging of dynamic gadolinium-enhanced sequences will remove any
preexisting T1 signal and thus facilitate detection of lesion enhancement
[2,
3].
Postablation Procedures
Radiofrequency ablation and cryoablation are being used with increased
frequency for treatment of malignancies in the liver, kidneys, and other
organs. The goal of either procedure is complete tumor necrosis.
Postprocedural cross-sectional imaging is used to analyze the lesion for the
presence of recurrent or residual neoplasm. This is a critical determination
in the management of these patients, and subtraction imaging is ideally suited
for such a role. Subtraction can make subtle enhancement within a tumor more
conspicuous and can remove high T1 signal, which is often present because of
coagulation necrosis (Fig. 7A,
7B,
7C). It can also help
differentiate the smooth, indistinct peritumoral enhancement seen in benign
posttreatment hyperemia from the discontinuous nodular enhancement of viable
tumor [4].
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Fig. 7A —65-year-old cirrhotic man after radiofrequency ablation for
hepatocellular carcinoma. Axial T1-weighted fat-suppressed spoiled
gradient-recalled echo (SPGR) unenhanced image shows heterogeneous but mostly
hyperintense mass (arrowheads).
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Fig. 7B —65-year-old cirrhotic man after radiofrequency ablation for
hepatocellular carcinoma. Axial T1-weighted fat-suppressed SPGR
contrast-enhanced image shows areas of high signal intensity (arrows)
that could be compatible with either hemorrhagic necrosis or tumor recurrence.
Arrowheads indicate mass.
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Fig. 7C —65-year-old cirrhotic man after radiofrequency ablation for
hepatocellular carcinoma. Axial T1 subtraction image shows conspicuous area of
nodular enhancement, consistent with tumor recurrence (arrow).
Arrowheads indicate mass.
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Other Applications
Subtraction imaging may also be useful for imaging the gallbladder in
situations in which the differential diagnosis is between tumefactive sludge
versus wall thickening from neoplasm. Whereas sonography using color or power
Doppler or CT performed with and without contrast material can suggest the
diagnosis of neoplasm by showing the presence of either blood flow or
enhancement within the area in question, MRI with subtraction imaging can aid
in making a more confident diagnosis. This is especially true in cases of
early carcinoma (Fig. 8A,
8B,
8C,
8D) when there is no
detectable extramural disease.
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Fig. 8A —67-year-old man with fever secondary to Escherichia coli
bacteremia. Contrast-enhanced axial CT image shows softtissue density along
posterior wall of gallbladder (arrowheads). Differential diagnosis
includes tumefactive sludge or gallbladder neoplasm.
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Fig. 8B —67-year-old man with fever secondary to Escherichia coli
bacteremia. Axial T1-weighted fat-suppressed spoiled gradientrecalled echo
(SPGR) unenhanced image shows isointense polypoid lesion (arrow)
along posterior wall of gallbladder.
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Fig. 8D —67-year-old man with fever secondary to Escherichia coli
bacteremia. Axial subtraction image shows avid enhancement of mass
(arrow), highly suspicious for gallbladder neoplasm. Localized
gallbladder cancer was found at cholecystectomy.
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Finally, a potentially important future indication for subtraction was
recently described by Ajaj et al.
[8], who showed the utility of
subtraction imaging in increasing sensitivity and decreasing readout time of
dark-lumen MR colonography in a study of 20 patients in whom the lesions were
confirmed on conventional endoscopy.
Pitfalls of Subtraction Imaging
An imperative technical principle of subtraction imaging is to keep all
parameters constant on the unenhanced and contrast-enhanced images. This
includes TR, TE, flip angle, slice thickness, matrix, and zero interpolation
factor. It is also essential that the patient's position remain unchanged
within the magnet during the unenhanced and contrast-enhanced sequences. The
patient should be able to maintain a breath-hold throughout the acquisition,
and the breath-hold should be reproducible from sequence to sequence. Not
fulfilling one or more of these criteria will result in misregistration
artifact and image degradation on the subtraction series.
Imaging at end expiration may yield more consistent data sets than imaging
at end inspiration [9].
Misregistration artifact can be identified by high signal intensity that
outlines enhancing structures. If this occurs, subtracting individual images
rather than entire data sets can be useful. The radiologist can select a
single image from the unenhanced series and a single image from the
gadoliniumenhanced series that corresponds to the identical anatomic level.
The technologist can then subtract these selected images, which may reduce the
degree of misregistration.
Conclusion
Subtraction MRI is an excellent technique for evaluating hemorrhagic masses
or lesions with high signal intensity on unenhanced T1-weighted sequences,
such as complicated cysts or hepatic nodules. Moreover, there are additional
clinical scenarios in which it is essential to determine the presence or
absence of enhancement within a mass. These include postablation therapy and
evaluation for residual tumor versus postsurgical change. In these situations,
the body imager should consider subtraction MRI as a useful problem-solving
technique that can aid in arriving at a confident diagnosis.
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Abstract
Introduction
