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Original Report |
1 All authors: Dipartimento di Scienze Radiologiche, Policlinico Umberto I –Università "La Sapienza," V. le Regina Elena, Rome 324 00161, Italy.
Received April 19, 2004;
accepted after revision July 1, 2004.
Address correspondence to P. Ricci
(paolo.ricci{at}uniroma1.it).
Abstract
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CONCLUSION. SonoVue-enhanced real-time low-mechanical-index sonography provides specific contrast-enhancement patterns of different benign focal liver lesions, allowing accurate characterization. Findings on SonoVue-enhanced sonography correlate well with those obtained on gadobenate dimeglumine–enhanced MRI.
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Sonography, because it is safe, inexpensive, quick, and easily accessible, is the first-line imaging technique for liver evaluation. However, baseline sonographic examination has several limitations in lesion characterization, requiring the need for second-level diagnostic studies (helical CT, MRI) [1, 2]. Color Doppler sonography shows promises of better diagnostic performance with the analysis of Doppler sonography spectra in or around tumors, although artifacts represented by respiratory or cardiac activity limit the diagnostic accuracy [1, 3].
IV sonographic contrast agents, consisting of tiny microbubbles confined to intravascular spaces and not leaking through the vessel wall, can enhance Doppler sonography signals and overcome these limitations [4]. Although these contrast agents increase the reflectivity of blood and enhance spectral and color Doppler signals, even contrast-enhanced color Doppler sonography is associated with artifacts such as color blooming and oversaturation. Moreover, overlapping between color Doppler patterns of benign and malignant lesions has been shown [5].
Harmonic sonography is a new technique that uses microbubble contrast agents and produces fewer artifacts. Tanaka et al. [6] reported that the combination of Levovist (SH U 508A, Schering) and second harmonic imaging software (the so-called intermittent imaging) allows a dynamic sonography protocol with which the contrast-enhancement patterns of different liver lesions can be assessed.
Recently, the development of second-generation contrast agents and dedicated software allows real-time examination and easier definition of enhancement patterns [7–9]. These microbubble agents use insoluble gases such as sulfur hexafluoride or perfluoropropane to achieve better stabilization of microbubbles in vivo. Microbubbles can survive multiple capillary passages after IV injection, giving significant contrast enhancement in the left heart and the arterial system and in the venous system after the second capillary passage.
The aim of our study was to evaluate the dynamic pattern of enhancement of real-time sonography using a second-generation contrast agent (SonoVue, Bracco) in a population of patients with focal liver lesions characterized as benign on gadobenate dimeglumine–enhanced MRI. Sonographic findings of enhancing patterns were compared with findings of dynamic contrast-enhanced MRI performed after the IV injection of gadobenate dimeglumine.
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In all four liver adenomas, sonographically guided biopsy was obtained for diagnostic confirmation.
After the study was approved by the institutional review board, we obtained written consent from each patient before contrast-enhanced sonography was performed.
Sonography Protocol
Patients were examined using an Esatune scanner (Esaote) equipped with
dedicated software (CnTI – Contrast Tuned Imaging, Esaote) and C530
convex or PA420 phased-array probes (Esaote). The sonographic examinations
included conventional gray-scale imaging to identify anatomic landmarks and
real-time low-mechanical-index (0.06–0.10) continuous scanning after the
administration of a bolus of SonoVue. Contrast-enhancement patterns were
assessed twice during a 30-min interval. SonoVue was administered as an IV
fast bolus of 2.4 mL, followed by 3 mL of saline flush. A single marker lesion
was identified, measured, and evaluated. When more lesions were identified on
conventional sonography, a single marker lesion, the larger and more
conspicuous one, was considered for characterization. When different lesions
revealed similar dimensions and conspicuity, the more superficial was
selected. Patients with more lesions were evaluated on a lesion-by-lesion
basis.
During contrast-enhanced evaluations, the entire vascular phase was continuously studied, consisting of an arterial phase (15–45 sec after the injection), a portal venous phase (50–90 sec), and a late phase (90 sec to 4–5 min). Our scanning technique was stationary in the region of the lesion, allowing the visualization of macro- and microcirculation of the lesion, as a result of the blood pool characteristics of SonoVue. In some cases, we performed flash scanning (i.e., high-mechanical-index fast scanning), which allows microbubble destruction, to evaluate reperfusion during the arterial phase in lesions showing strong enhancement and during the portal phase only in lesions showing contrast enhancement during this phase. Reperfusion after flash scanning during the portal phase must be considered pathognomonic for focal nodular hyperplasia.
All examinations were digitally recorded and subsequently analyzed off-line.
MRI Protocol
MRI was performed in all patients within 7 days before contrast-enhanced
sonography with a 1.5-T MR unit (Magnetom Vision Plus; Siemens Medical
Solutions) using a phased-array multicoil as a receiver coil. The MRI protocol
included axial breath-hold T2-weighted (TR/TE, infinite/90; flip angle,
150°; acquisiton time, 25 sec; slice thickness, 6 mm; interslice gap,
0.25%; matrix, 256 x 160; field of view, 350 mm), half-Fourier
single-shot turbo spin-echo (HASTE), and unenhanced and gadobenate
dimeglumine–enhanced spoiled T1-weighted (TR/TE, 170/4.6; flip angle,
80°; number of excitations, 1; acquisition time, 20 sec; slice thickness,
6 mm; interslice gap, 0.25%; matrix, 256 x 128; field of view, 350 mm)
fast low-angle shot (FLASH) sequences. A triphasic dynamic contrast-enhanced
study was obtained after the administration of an IV bolus of 0.1 mmol/kg of
gadobenate dimeglumine (MultiHance, Bracco) flushed by 20 mL of sterile saline
solution using an automatic MR-compatible injector. The scanning delay for
triphasic dynamic gradient-recalled echo imaging was 14 sec, 50 sec, and 3 min
after initiating contrast injection, representing the hepatic arterial, portal
venous, and equilibrium phases, respectively. The dynamic study was followed
by a delayed, hepatospecific phase obtained 1 hr after the injection of
contrast material, as recommended by the manufacturer. Previous studies have
shown that liver enhancement with gadobenate dimeglumine is relatively stable
during this period [10].
Image Analysis
Sonographic digital records were analyzed offline, in consensus, by two
radiologists who were both experienced in contrast sonography of the liver and
who were blinded to clinical and other imaging data.
MR images were reviewed by two gastrointestinal radiologists experienced in both liver sonography and MRI. Images were analyzed at different consensus conferences to describe size, baseline appearance, and dynamic contrast-enhancement behavior of the different lesions. Sonographic findings were eventually compared with MRI findings
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Hemangioma
Twenty-seven hemangiomas were detected in 24 patients. On baseline
sonography, all the hemangiomas were inhomogeneous with posterior acoustic
enhancement: Fifteen were hyperechoic, three hyper- and isoechoic, and nine
hypoechoic. The contrast-enhancement patterns were as follows: specific
globular enhancement (Fig. 1A)
with progressive complete (n = 12) and incomplete (n = 13)
(Fig. 1B) wash-in in 25
lesions. In the remaining two lesions, a rapid wash-in, with late washout,
characteristic of a capillary hemangioma, was observed.
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On unenhanced MRI, all the lesions were hypointense on T1-weighted and markedly hyperintense on T2-weighted images. On contrast-enhanced studies, 25 lesions showed a globular enhancement pattern during the arterial phase (Fig. 1C) with progressive centripetal filling (complete in 12 lesions and incomplete in 13 [Fig. 1D]) during the portal venous and equilibrium phases. During the 1-hr hepatobiliary phase, all lesions showed a hypointense signal compared with liver parenchyma.
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In the remaining two lesions, characterized as capillary hemangiomas, the contrast-enhancement pattern presented rapid wash-in during the arterial phase, with persistent enhancement during the portal venous and equilibrium phases. Hypointense signal compared with surrounding liver parenchyma was observed during the hepatobiliary phase. Dynamic enhancement patterns on MRI completely correlated with those on contrast-enhanced sonography.
Focal Nodular Hyperplasia
Seventeen focal nodular hyperplasias were detected in 15 asymptomatic women
with no history of chronic hepatic disease. On baseline sonography, the
lesions appeared slightly hyperechoic, with evidence of a central hypoechoic
area in seven cases. During the contrast-enhanced study, the lesions showed an
extremely rapid homogeneous contrast uptake during the arterial phase
(Fig. 2A), with mild
hyperechogenicity or isoechogenicity relative to surrounding enhanced liver
parenchyma during the portal and late phases (Figs.
2B and
2C). A central scar was evident
on the portal and late phases in seven cases. A specific diagnostic clue in
the characterization of focal nodular hyperplasia was the evidence of
revascularization during the portal and late phases after microbubble
disruption as a result of the flash scanning application.
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On unenhanced MRI, all the lesions were isointense on T1-weighted images and iso- to slightly hyperintense on T2-weighted images. MR images showed homogeneous contrast enhancement during the arterial phase (Fig. 2D), with isointensity during the portal (Fig. 2E) and equilibrium phases. During the 1-hr hepatobiliary phase, all lesions showed isointense to slightly hyperintense signal compared with liver parenchyma (Fig. 2F). A central scar (hyperintense on both the T2-weighted images and on the portal and late phases of contrast-enhanced T1-weighted images) was observed in five cases.
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Adenoma
Four adenomas were evaluated in four women with histories of chronic use of
oral contraceptives. All four lesions appeared as rounded, iso- to hyperechoic
lesions. All lesions were characterized by early homogeneous contrast
enhancement during the arterial phase
(Fig. 3A), with subsequent
rapid washout during the portal phase
(Fig. 3B). On unenhanced
examination, the lesions were hypointense on T1-weighted images and slightly
hyperintense on T2-weighted images. MR images showed homogeneous and intense
contrast enhancement during the arterial phase
(Fig. 3C), with rapid washout
during the portal venous and equilibrium phases
(Fig. 3D) and no evidence of
either a central scar or a pseudocapsule. During the 1-hr hepatobiliary phase,
all lesions showed a hypointense signal compared with liver parenchyma.
Dynamic MRI findings correlated well with contrast-enhanced sonographic
features in all patients (Fig.
3E).
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As shown in our study, contrast-enhanced sonography is useful in providing specific contrast-enhancement patterns during real-time evaluation of liver lesions, without any risk of missing the optimal phase of observation. This is equivalent to MRI, but at a lower cost and with better patient compliance.
Regarding hemangiomas, a typical feature is evidence of globular enhancement, with progressive in-filling, which was observed in 25 of our patients. This is particularly useful in the presence of atypical hemangiomas, which appear on baseline examinations as hypo- or hysoechoic (having the same echogenicity as the surrounding liver parenchyma, commonly with a thin hypoechoic peripheral rim) lesions, as seen in our study in nine patients. However, when a different contrast behavior during the arterial phase was observed, the detection of late washout led to the diagnosis of capillary hemangioma [12].
Focal nodular hyperplasias showed an early strong and homogeneous enhancement during the arterial phase. During the portal phase, the lesions appeared mildly hyperechoic over the normal parenchyma because of their portal supply, whereas the lesions appeared hysoechoic (having the same enhancement as the surrounding enhanced liver parenchyma in the late phase) during the late phase. Key points in the characterization of focal nodular hyperplasias are early and homogeneous enhancement during the arterial phase, presence of portal supply, evidence of a hypoechoic scar, and lack of a pseudocapsule. These features are helpful in differentiating focal nodular hyperplasia from hepatocellular carcinoma and adenoma.
The association of a history of chronic use of oral contraceptives with the presence of a rounded and well-marginated lesion showing early homogeneous enhancement during the arterial phase and rapid washout during the portal phase may lead to the diagnosis of adenoma. An important point in differentiating adenoma from focal nodular hyperplasia is the absence of portal supply. A clue to discriminate hepatocellular carcinoma from adenoma is the slow and more heterogeneous arterial enhancement and the frequent presence of a pseudocapsule. All contrast-enhanced sonographic findings correlated well with those of MRI.
As shown in our study, contrast-enhanced sonography with SonoVue is a useful tool in the characterization of focal liver lesions. This technique is characterized by high cost-effectiveness, high patient compliance, and high accuracy in providing specific contrast-enhancement patterns that are roughly comparable to those obtained on MRI. Although our study population was limited, especially regarding the few cases of adenomas and the absence of regenerative nodules, our results show that in the workup (follow-up and diagnosis) of patients with benign focal liver lesions, sonography should be performed with second-generation contrast agents and new technologies such as Contrast Tuned Imaging.
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