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Characterization of Focal Liver Lesions in Real Time Using Harmonic Imaging with High Mechanical Index and Contrast Agent Levovist

¹ All authors: Sardinian Mediterranean Imaging Research Group, Via Gorizia no. 11, Sassari 07100, Sardinia, Italy.

Received August 8, 2003; accepted after revision December 3, 2003.

 
Address correspondence to V. Migaleddu (vmigale{at}tin.it).

Abstract

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OBJECTIVE. The aim of this study was to characterize focal hepatic lesions using agent detection imaging and Levovist.

MATERIALS AND METHODS. Sixty-five patients (21 male and 44 female; age range, 8–82 years; mean ± standard deviation, 58.1 ± 14.5 years) were independently evaluated by two observers in a blinded manner using stored sonographic images. Seventy-five lesions were found: 15 hepatocellular carcinomas, nine focal nodular hyperplasias, two adenomas, 21 hemangiomas, 23 metastases, and five regenerative nodules. Nine patients were excluded (six because of technical failures, three with unproven diagnoses). New high-mechanical-index software was used to reveal power harmonic responses from contrast microbubble destruction. After a venous bolus injection of 4 g of Levovist at a strength of 400 mg/mL, delayed imaging was used to study lesion enhancement in the arterial, portal, and parenchymal phases. Two comparisons were made. The first was between the B-mode image and the first contrast-enhanced image after the flash. The second was between color Doppler sonograms and real-time contrast-enhanced perfusion images.

RESULTS. Contrast-enhanced images after the flash and real-time contrast-enhanced images revealed more information for the characterization of the lesion than did gray-scale and color Doppler images (p < 0.0001, Wilcoxon's signed rank test). Different types of lesions showed statistically significant differences in enhancement during each of the three vascular phases (p < 0.005, Kruskal-Wallis test). Lesions with lower contrast enhancement were metastases and regenerating nodules. Good agreement was present between the two observers; differences were not statistically significant (p > 0.05).

CONCLUSION. Agent detection imaging with Levovist increased diagnostic confidence in the characterization of focal hepatic lesions as compared with standard sonography.

Introduction

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Recent studies describe the appearance of focal liver lesions after the administration of the contrast agent SH U 508A (Levovist, Schering) using a static imaging method and a high mechanical index that results in the destruction of almost all microbubbles in the field of view [1–3]. The systems used are based on phase inversion technology that allows the cancellation of the signal from the fundamental frequency and increases the contrast signals coming from the focal lesions and surrounding tissue. With this technique, observation of static frames at different times allows evaluation of the hemodynamics of the lesion. The importance of observing the behavior of the contrast agent in the late phase has been reported [4–7]. The contrast agent used in our study, Levovist, is widely available and is composed of granules of galactose and water with a small amount (0.1%) of palmitic acid. Once prepared, the contrast agent consists of stabilized microbubbles that enhance the signals from blood for 2–5 min [8]. The objective of our study was to verify whether the use of Levovist and a new technique of high mechanical index combined with dynamic detection (agent detection imaging) improve specificity in the diagnosis of focal liver lesions and whether the results differ between two observers.

Materials and Methods

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Technology
The sonographic scanner used for our study was a Sequoia 512 Imagegate (Acuson, Siemens) with agent detection imaging software that uses a high mechanical index (typically 1.9) necessary for the destruction of the microbubbles. This software differs from that commonly used because the fundamental pulse is produced with a narrow band that allows separation in receipt, without overlapping, of the fundamental echoes from those of the harmonic signal arising from the tissue and blood flow. This arrangement results in greater contrast resolution and optimal spatial and detail resolution. Agent detection imaging is a technology that can overcome the limitations of a static examination because it allows a short time (we selected 3 sec) for contrast-enhanced real-time imaging. This software uses a high mechanical index and is therefore capable of detecting the harmonic signal arising from the destruction of the microbubbles contained in the macro- and microvessels present in the region of interest delimited by the color Doppler box. The broadband signal generated by the destruction of the microbubbles in the region-of-interest box is interpreted as a pseudo-Doppler signal tied to the loss of correlation between transmit and receive, as already shown with stimulated acoustic emission [4]. Stimulated acoustic emission is used to visualize the contrast agent. With this method, a high mechanical index is also used, and the destruction of microbubbles occurs and gives rise to high-frequency harmonic echoes with random and casual patterns. These echoes are color-coded using color Doppler velocity, unlike agent detection imaging, which codes the signal according to the intensity scale of color Doppler energy. With agent detection imaging software, a high mechanical index is activated and conventional gray-scale imaging becomes contrast-enhanced harmonic imaging. This image is characterized by an immediate flash as most of the microbubbles in the scanning plane are destroyed. This frame is the first observed, followed by the observation in real time of frames containing harmonic signals arising from the destruction of the microbubbles in the blood flow of the macro- and microvessels moving around and in the lesion studied.

Methodology
The contrast agent used was Levovist in doses of 4 g administered as a bolus injection (in 2–3 sec) in a concentration of 400 mg/mL.

First, we performed conventional or tissue harmonic imaging of the lesion and color Doppler evaluation of its vascularity. To study a single lesion, images were acquired at various time intervals of 10–15 sec, 20–30 sec, and 1, 2, 3, 4, 5, and 6 min after injection. Using these time intervals, the arterial, portal, and parenchymal enhancement phases were visualized.

When agent detection imaging is activated, destruction of microbubbles occurs, resulting in an instantaneous flash contrast image. This step was followed by real-time observation of the macro- and microvessels for a minimum of 3 sec.

Patients
A total of 74 patients were examined, and of these, 65 were included in our study (21 male and 44 female; age range, 8–82 years; average age ± standard deviation [SD], 58.1 ± 14.5 years). Nine patients (12%) were excluded, six because their images were technically insufficient and three because the diagnosis could not be confirmed. Technical failures in the six patients who were excluded occurred only at the start of the study and reflect our learning curve. The most common causes of failure were poor cooperation from the patient or deep lesions. To eliminate unsuccessful examinations, we used an intercostal approach that reduced the distance between the transducer and the lesion and eliminated the deep respiration necessary for subcostal examinations. Our findings were hemangiomas (n = 21); adenomas (n = 2); focal nodular hyperplasias (n = 9); hepatocellular carcinomas (n = 15); regenerating nodules (n = 5); and metastases (n = 23) from colon (n = 10), breast (n = 9), bladder (n = 1), neuroendocrine (n = 2), and prostate (n = 1) cancer.

The diagnosis was confirmed on CT for the hemangiomas (except in one patient with a histologic diagnosis after laparoscopic nodulectomy of a suspected hepatocellular carcinoma in chronic liver disease); CT and percutaneous biopsy confirmed the diagnoses of the adenomas, focal nodular hyperplasias, hepatocellular carcinomas, and regenerating nodules. Two cases of colon metastases were confirmed with biopsy during surgery on the primary tumor. In one patient with hepatocellular carcinoma, CT was not performed because of the patient's intolerance for iodine contrast media; the diagnosis was confirmed only with percutaneous biopsy.

Image Analysis
Sonograms were evaluated by two double-blinded observers without knowledge of the final diagnosis or the evaluation of the other observer.

We compared the baseline gray-scale image with the contrast-enhanced images. The first image was obtained 10–15 sec after the contrast injection, which resulted in a flash contrast image of the arterial phase. The second image was obtained 20–30 sec after injection, resulting in a flash contrast image of the portal phase. The next images were obtained at 1, 2, 3, 4, 5, and 6 min in the same manner to show the contrast enhancement in the early and late parenchymal phases.

The flash score consisted of the absence or presence of enhancement in the lesion compared with the surrounding parenchyma. Lack of enhancement, enhancement at the rim, homogeneity of the enhancement, and whether enhancement was less than, equal to, or greater than that of the surrounding parenchyma were also evaluated. Enhancement and homogeneity were assigned a numeric score from 0 to 4.5.

The vascular score consisted of comparison of baseline color Doppler images with those obtained in real time using contrast-enhanced harmonic imaging in the arterial, portal, and late phases. This set of data was subdivided into mild, medium, or high enhancement and regular or irregular appearance of the macro- and microvessels in and around the lesion. These evaluations were given a numeric score from 0 to 3.5 (Table 1).

The data were analyzed using Wilcoxon's signed rank test and the Kruskal-Wallis test [9, 10].

Results

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Tables 2 and 3 give the flash and vascular scores, respectively, of the two observers. Those results show that the scores of the two observers for the three phases and for all the lesions together are significantly greater than 0 (p < 0.0001). The analyses of the two observers were evaluated separately; the differences between them were negligible and were never statistically significant (p > 0.05, Wilcoxon's signed rank test). In the arterial phase of the hepatocellular carcinomas, early enhancement was registered with respect to the surrounding parenchyma in 13 (86.7%) of 15 cases. Larger lesions were associated with more heterogeneous enhancement. In the late parenchymal phase, washout of contrast material from in the lesion compared with the surrounding parenchyma was noted in 12 (80%) of 15 cases. In all cases, irregular microvessels were identified in the lesion during observation in real time (Fig. 1A, 1B, 1C, 1D). In two cases, no early enhancement in the arterial phase was observed in hypovascular hepatocellular carcinomas; just one or more irregular microvessels in the lesions were observed in real time. The adenomas and focal nodular hyperplasias all showed enhancement of the lesions in the arterial phase. The washout of contrast material in the parenchymal phase was poorly defined or absent. The characteristic presence of vascular enhancement in the center of the nodule (the "central spider" sign) was identified on real time in focal nodular hyperplasias (Fig. 2A, 2B, 2C, 2D). Rim enhancement at the periphery in the arterial phase (18/21; 85.7%) and progressive lobular enhancement in the centripetal direction in successive phases (19/21; 90.5%) were identified in the hemangiomas (Fig. 3A, 3B, 3C, 3D). An early hypervascular pattern was observed in two high-flow hemangiomas. Modest heterogeneous enhancement in the arterial phase was confirmed in some metastases, and a characteristic lack of enhancement was visualized in the late parenchymal phase (23/23; 100%) (Fig. 4A, 4B, 4C, 4D). Regenerating nodules showed little enhancement in the three phases and nonvascularization during real-time observation (Fig. 5A, 5B, 5C, 5D). The flash and vascular scores for the different lesions revealed statistically significantly different enhancement in each of the three phases (p > 0.005, Kruskal-Wallis test). Compared with conventional imaging and color Doppler imaging, metastases and regenerating nodules generally showed less information obtained from contrast-enhanced imaging, particularly with real-time observation.

View larger version (149K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —67-year-old man with cirrhosis and hepatocellular carcinoma. Arterial phase flash sonogram shows early enhancement of lesion.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —67-year-old man with cirrhosis and hepatocellular carcinoma. Portal phase flash sonogram shows increased enhancement in comparison with surrounding parenchyma.

View larger version (177K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —67-year-old man with cirrhosis and hepatocellular carcinoma. Parenchymal phase flash sonogram shows early washout of contrast material in lesion in comparison with surrounding parenchyma.

View larger version (147K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —67-year-old man with cirrhosis and hepatocellular carcinoma. Sonogram obtained during real-time vascular evaluation in arterial phase shows arterial segmental branch (arrow) from which irregular microvessels arise.

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —9-year-old girl with focal nodular hyperplasia. Arterial phase flash sonogram shows early enhancement of lesion.

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —9-year-old girl with focal nodular hyperplasia. Portal phase flash sonogram shows enhancement of lesion similar to surrounding parenchyma.

View larger version (146K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —9-year-old girl with focal nodular hyperplasia. Parenchymal phase flash sonogram shows no apparent washout.

View larger version (123K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —9-year-old girl with focal nodular hyperplasia. Sonogram obtained during real-time vascular evaluation shows "central spider" sign.

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —28-year-old woman with hemangioma. Arterial phase flash sonogram shows rim enhancement.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —28-year-old woman with hemangioma. Portal phase flash sonogram shows progressive lobular enhancement in centripetal direction.

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —28-year-old woman with hemangioma. Parenchymal phase flash sonogram shows almost complete fill-in.

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D. —28-year-old woman with hemangioma. Sonogram obtained during real-time vascular evaluation shows microvessels in peripheral zone (arrow).

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —63-year-old man with metastatic liver disease. Arterial phase flash sonogram shows inhomogeneous and low enhancement of lesion.

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —63-year-old man with metastatic liver disease. Portal phase flash sonogram shows slightly less enhancement.

View larger version (156K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —63-year-old man with metastatic liver disease. Parenchymal phase flash sonogram shows complete lack of enhancement.

View larger version (149K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —63-year-old man with metastatic liver disease. Sonogram obtained during real-time vascular evaluation shows poor vasculature of lesions.

View larger version (162K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —65-year-old man with cirrhosis and regenerating nodule. Arterial phase flash sonogram shows no enhancement of lesion.

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —65-year-old man with cirrhosis and regenerating nodule. Portal phase flash sonogram shows homogeneous enhancement in comparison with surrounding parenchyma.

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5C. —65-year-old man with cirrhosis and regenerating nodule. Parenchymal phase flash sonogram shows no evident washout.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5D. —65-year-old man with cirrhosis and regenerating nodule. Sonogram obtained during real-time vascular evaluation shows no apparent vessels in lesion.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The mechanical index is related to the acoustic pressure of the ultrasound beam on the insonated structures and is a measure of the beam's power. The mechanical index is the ratio between the negative pressure at the focal point and the central frequency of the transducer. An ultrasound beam with a mechanical index of less than 0.2 produces nonlinear harmonic echoes from the resonance of the microbubbles; a mechanical index greater than 1.0 produces destruction of the microbubbles.

Contrast-enhanced harmonic imaging with systems using a high mechanical index requires an imaging delay to allow reperfusion of the lesion and the surrounding parenchyma after the destruction of the microbubbles; therefore, using a system with a high mechanical index requires a longer learning period than a system using a low mechanical index. In our experience, agent detection imaging with real-time observation of contrast enhancement in the macro- and microvessels reduces the learning curve.

Agent detection imaging uses both fundamental echoes and contrast-enhanced harmonic echoes in the formation of the image. Unlike the low mechanical index technique in which the fundamental gray-scale image is absent, agent detection imaging software offers the possibility of visualizing the fundamental gray-scale image, the contrast-enhanced harmonic image by itself, or both together. At the start of the examination, an optimal baseline gray-scale image can be obtained so that the lesion is perpendicular to the ultrasound beam and in the center of the box in which the contrast-enhanced harmonic image is formed.

Visualization of contrast enhancement in the intrahepatic macro- and microvessels permits the determination of the arterial and the portal contributions to a lesion, which allows one to modify the time intervals of the examination according to the vascular pattern of the lesion. For example, because of the hyperkinetic circulation of cirrhosis in hepatocellular carcinoma, it is necessary to obtain the first scan at 10–15 sec. In focal nodular hyperplasias and adenomas, it is best to choose scanning intervals to study the arterial and early portal phases. Hemangiomas and metastases require particular attention in the portal and the early and late parenchymal phases. The quantity and the concentration of the contrast agent we used (4 g and 400 mg/mL) were sufficient to obtain information from both the early and the late phases ( 6 min).

Our results show that the information acquired with contrast imaging both in the flash phase and during real-time vascular observation is clearly superior to that obtained with conventional sonography and color Doppler sonography. The observation in real time of the peri- and intralesional vessels seen after the first flash of microbubble destruction added diagnostically important information such as the regularity or irregularity of the vasculature. Other static contrast-enhanced imaging technologies that use a high mechanical index and intermittent scanning, such as pulse inversion, flash echo, and combined contrast chain, do not reveal the same clear information that is possible with real-time scanning. In our experience, real-time contrast-enhanced imaging technologies that use a low mechanical index, such as coherent contrast-enhanced imaging, contrast-tuned imaging, and helical biphasic or triphasic CT, also do not readily show these findings.

Image interpretation (from contrast-enhanced CT experience) is simple, sufficiently objective, and not operator-dependent, as seen by the results of our two observers.

In the characterization of focal liver lesions, this method can improve diagnostic specificity because of observing different contrast enhancement for different disorders. These statistically significant results are achieved both by evaluating the contrast-enhanced flash images and through real-time evaluation.

The contrast-enhanced examination was less useful than conventional and color Doppler sonography in regenerating nodules and metastases. For the latter, the characteristic appearance is the lack of enhancement in the parenchymal phase. Clinical and laboratory evaluations are important in chronic liver disease because hypovascular hepatocellular carcinomas can be confused with regenerating nodules. When lesions are found that do not enhance in the arterial phase and that present internal irregular small vessels at real-time evaluation, sonographically guided biopsy is recommended. In our experience, hepatocellular carcinomas were found in two cases with this contrast pattern.

The central spider sign visualized in real time in the nodules of focal nodular hyperplasia strongly suggests the diagnosis. Arterial and venous vessels can be visualized in the center of high-flow hemangiomas. Rim enhancement visualized in the arterial phase can help in the diagnosis of high-flow hemangiomas.

In conclusion, agent detection imaging with Levovist achieves a high specificity in the diagnosis of focal liver lesions. Such imaging may reduce the need for more costly and invasive examinations such as CT, MRI, and biopsy.

Acknowledgments
 
We thank Matteo Bottai of the Consiglio Nazionale delle Ricerche in Pisa, Italy, for providing the statistical analysis.

References

Top Abstract Introduction Materials and Methods Results Discussion References

 

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Migaleddu, V. Articles by Vincentelli, I. Search for Related Content PubMed PubMed Citation Articles by Migaleddu, V. Articles by Vincentelli, I. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?