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Ultrasonography |
1 From the Department of Medical Imaging, Toronto General Hospital, 200 Elizabeth St, Toronto, Ontario, Canada M5G 2C4 (M.J.D.M., K.K., S.R.W.); and the Department of Medical Biophysics, Sunnybrook and Women’s College Health Sciences Centre, Toronto, Ontario, Canada (P.N.B.). Received December 6, 2000; revision requested January 17, 2001; revision received May 30; accepted July 5. Supported by the Terry Fox Programme of the National Cancer Institute of Canada, the Medical Research Council of Canada, and Berlex Canada. Address correspondence to S.R.W. (e-mail: stephanie.wilson@uhn.on.ca).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Contrast material–enhanced pulse inversion US was performed on 58 unknown hepatic lesions: 23 hepatocellular carcinomas, 10 focal nodular hyperplasias, 16 hemangiomas, and nine metastases. Selected images were sequentially reviewed by readers blinded to the final diagnosis. On a baseline image, they determined lesion echogenicity, and on a vascular image, the presence or absence of distinct vascularity. On an arterial phase interval-delay flash image and a postvascular image, they assessed enhancement of the lesion and liver. Responses were compared with confirmed diagnoses.
RESULTS: Focal nodular hyperplasia was characterized by detectable vascularity and positive enhancement on interval-delay and postvascular scans (sensitivity, 83% [eight of 10 lesions]; specificity, 98% [40 of 41 lesions]). Hepatocellular carcinoma also showed detectable vascularity and positive enhancement on interval-delay images but no postvascular enhancement (sensitivity, 68% [14 of 20 lesions]; specificity, 74% [23 of 31 lesions]). Vascular imaging with SH U 508A did not contribute to the diagnosis of metastasis or hemangioma. However, no or weak enhancement during the arterial phase flash without postvascular enhancement produced a sensitivity of 83% (seven of eight lesions) and sensitivity of 77% (33 of 43 lesions) for metastasis. Peripheral nodular enhancement on arterial phase flash images was highly specific (98% [37 of 38 lesions]) but not sensitive (44% [six of 13 lesions]) for hemangioma.
CONCLUSION: SH U 508A-enhanced pulse-inversion interval-delay flash and postvascular phase imaging are helpful in differential diagnosis of focal hepatic lesions.
Index terms: Angioma, gastrointestinal tract, 761.3194 • Liver, focal nodular hyperplasia, 761.3198 • Liver neoplasms, diagnosis, 761.12985, 761.12988, 761.12989 • Liver neoplasms, secondary, 761.33 • Liver neoplasms, US, 761.12985, 761.12988, 761.12989
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Pulse inversion (PI) imaging is a newer method that is highly sensitive to microbubbles (6). With this technique, two pulses are transmitted for each scanning line. The second pulse is inverted (180° out of phase) with respect to the first. Echoes from both pulses are collected by the transducer and summed. Linear reflectors, such as normal tissue, produce no net signal. However, nonlinear reflectors such as microbubbles produce echoes that are asymmetric and do not sum to zero. The result is that echoes from bubbles are detected preferentially by using the PI method, improving image contrast between tissue and microbubbles. If sound is transmitted at high intensity, as measured with the mechanical index (MI), SH U 508A bubbles are disrupted by the first pulse, increasing the difference between the two echoes and further enhancing the signal. The contrast produced with a high-MI technique is dramatic but short lived, since the microbubble agent is destroyed in the process (7).
There are three ways in which the liver can be imaged with SH U 508A and PI. Continuous real-time imaging of a hepatic lesion, immediately after the peripheral venous injection of the contrast agent, shows progressive contrast enhancement of the large and small vessels of the parenchyma and lesions. We refer to this phase as the vascular phase. During this phase, cessation of scanning for a few seconds allows bubbles to accumulate in the vasculature without disruption. Brief reinsonation at high MI destroys, often in a single frame, the bubbles that have accumulated over that period within the lesion and the surrounding liver, producing a brief "interval-delay flash." The degree of enhancement of the lesion can then be compared with that of the adjacent liver. The strength of the interval-delay flash reflects the amount of microbubble contrast material accumulated within the vascular bed during the delay, which in the arterial phase is related to the arterial vascular volume.
SH U 508A also produces organ-specific delayed enhancement of the liver that occurs after the agent has cleared the blood pool (8). During the vascular phase, many of the circulating microbubbles appear to become trapped in or around the liver vasculature, possibly in areas of low shear stress in the hepatic vascular sinusoids. If contrast material is allowed to accumulate in these regions for about 4 minutes after injection without insonation, a high-MI sweep through the liver results in high enhancement of the parenchyma as the accumulated bubbles are disrupted. We use the designation postvascular phase imaging to describe this phenomenon. The purpose of this study was to combine postvascular and vascular phase PI imaging by using SH U 508A enhancement to differentiate focal hepatic masses.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Twenty-three hepatocellular carcinomas (HCCs) were evaluated in 20 patients, 18 men and two women, aged 32–75 years. Lesions were 1–20 cm in diameter. Pathologic confirmation was obtained in 18 patients. In the remaining two patients, a diagnosis was established with clinical and imaging parameters, including a history of chronic hepatic disease and a hypervascular mass with rapid washout in the portal venous phase at contrast material–enhanced multiphasic spiral computed tomography (CT) and dynamic magnetic resonance (MR) imaging (9).
Ten focal nodular hyperplasias (FNHs) were evaluated in 10 patients, all women aged 25–42 years. Lesions were 2–13 cm in diameter. All FNHs were diagnosed by using one or more of positive sulphur-colloid hepatic scintigraphy (eight patients), typical enhancement and signal characteristics on MR images (five patients), and/or typical appearance and enhancement patterns on triphasic CT scans (four patients). All patients were asymptomatic, had no history of chronic hepatic disease, and were not taking oral contraceptives.
Sixteen hemangiomas were evaluated in 13 patients consisting of seven women and six men, aged 33–67 years. Lesions were 1–15 cm. All hemangiomas had imaging confirmation consisting of typical enhancement characteristics (peripheral nodular enhancement at early phase imaging, which subsequently fills in at delayed imaging) at triphasic CT (12 patients) and/or dynamic gadolinium-enhanced MR imaging (four patients) and/or correlating persistent pooling of tracer with red blood cell scintigraphy (six patients).
Nine metastatic lesions were evaluated in nine patients consisting of seven women and two men, aged 49–74 years. Pathologic confirmation was obtained in all patients, revealing spread from colorectal (two patients), breast (two patients), gallbladder (two patients), pancreatic (one patient), and gastrointestinal stromal tumor (one patient). An additional patient had poorly differentiated carcinoma of unknown origin.
US Technique
Scanning was performed by a single radiologist (M.J.D.M.) using a model 5000 scanner (ATL Ultrasound, Bothell, Wash) equipped with PI imaging software. The MI was set at 0.8–1.2 for vascular phase imaging and at its maximum level (1.3) for postvascular imaging. The line density and frame rate were set to a low level (5 Hz), with no frame averaging (persistence). Scanning was performed with a C5-2 convex array probe, and images were stored on S-VHS videotape and 90-frame digital cineloops. After baseline imaging, two contrast material boluses, each of 6-mL SH U 508A at 300 mg/mL concentration, were injected into the brachial vein. Four sets of images were then obtained:
1. Baseline US included routine gray-scale evaluation of the liver. A preliminary sweep was then performed during suspended respiration, in the optimal plane for visualization of the lesion, and stored as a baseline cineloop. Machine settings such as focal zone and time-gain compensation were optimized.
2. Following the first injection, real-time scanning commenced immediately. The vascularity of the lesion was recorded continuously during the vascular phase from wash-in to the peak of arterial enhancement.
3. At the peak of enhancement from the first injection, as determined with the appearance of the blood vessels in the lesion and adjacent liver, the patient suspended respiration while the probe was held in position centered on the lesion. The freeze button was then pressed, suspending acoustic output of the probe and thus allowing bubbles to accumulate within the vascular space of the liver and lesion. After 10 seconds, scanning was resumed, the acoustic output from the probe instantly disrupting the accumulated bubbles in the lesion and liver, producing a brief interval-delay flash.
4. Postvascular phase images were obtained by giving the second injection and waiting a full 4 minutes before scanning. The lesion was then insonated at high MI as part of a continuous sweep of the liver in the same plane as the preliminary sweep.
Videotapes and cineloops were reviewed, and four still images were selected by the sonographer for each lesion at baseline and in the three phases of SH U 508A enhancement. These four images were shown independently to three readers (including K.K.), all experienced sonographers with knowledge of the principles of US contrast material enhancement. Readers were blinded to patient identity, final diagnosis, and results of other imaging tests. For each image, they answered the specific questions summarized in Table 1. From the baseline image, the reviewers determined the echogenicity of the lesion compared with that of normal liver. Questions relating to image sets 2–4 were then answered sequentially, with continuous access to the baseline image. The reviewers could not, however, change preceding responses. For the vascular image, obtained with continuous imaging after bolus injection, they graded their ability to identify distinct lesional vascularity. For the interval-delay flash and the postvascular image, they assessed the intensity and distribution of enhancement of the lesion compared with that of the adjacent liver. For lesions enhancing on images 3 and 4, the reviewers described the pattern of enhancement, as shown in Table 1. The reviews were performed independently and the mean of the graded responses calculated for each question or combination of questions. Agreement between readers was assessed with the multirater 
statistic, which was calculated for the 58 responses to each question by the three readers. Responses from the reviewers were then compared with the confirmed diagnoses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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statistic for the level of agreement between readers for each question is shown in Table 1).
Baseline Imaging
Fifteen lesions were isoechoic to the adjacent liver, 24 were less echogenic, five were hyperechoic, and 14 were mixed in echogenicity.
Vascular Imaging
In 39 (67%) of the 58 lesions, vessels with distribution and number that were identified could be estimated by the reviewers. In the remaining 19 (33%) lesions, the reviewers could not determine the presence of vascular structures within the lesion. In the 39 lesions in which vascularity could be assessed, a stellate pattern was identified in six. Vascularity was diffuse in six, patchy in 20, and had a marginal pattern in seven others. A dominant tortuous feeding vessel was seen in two lesions.
Comparison with the final diagnosis showed that in the highly vascular lesions, FNHs (Fig 1) and HCCs (Fig 2), 26 (78%) of 33 lesions had detectable vascularity. Furthermore, three (50%) of six lesions with a stellate vascular pattern (Fig 1) had a final diagnosis of FNH. Six (38%) of 16 hemangiomas showed marginal vascularity (Fig 3). Both lesions with a tortuous feeding artery were FNHs.
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Comparison of the final diagnoses with the interval-delay flash images showed that in nine (90%) of 10 FNHs (Fig 1) and 16 (70%) of 23 HCCs (Fig 2), the reviewers reported enhancement of the lesion equal to or greater than the intensity of the adjacent enhancing liver. A nonenhancing scar was seen in two lesions: one FNH (Fig 4) and one HCC (Fig 5). A pattern of peripheral nodular enhancement was seen by the reviewers in seven of 16 hemangiomas (Fig 3). No other lesion showed a pattern interpreted as peripheral nodular enhancement. Three of 16 hemangiomas showed no enhancement on the interval-delay flash images (Fig 6). Metastases showed no enhancement (five [56%] of nine lesions) or weak enhancement of intensity less than that of the liver (four [46%] of nine lesions) on the interval-delay flash images (Fig 7). A rindlike pattern of enhancement also was seen (Fig 8).
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By using the combined results of the image review, criteria for the interpretation of SH U 508A–enhanced US images in three phases are proposed and summarized in Table 2. This shows, for example, that if lesion enhancement in all three phases indicates a diagnosis of FNH, the sensitivity and specificity in this study would have been 83% and 98%, respectively. Similarly, a lesion that enhanced with vascular imaging and in the arterial phase interval-delay flash but not in the postvascular phase indicated HCC with a sensitivity of 68% and a specificity of 74%. Continuous vascular imaging with SH U 508A made no contribution to the diagnosis of metastasis or hemangioma, but the arterial phase interval-delay flash did. In particular, peripheral nodular enhancement was specific (98%) but not sensitive (44%) to hemangioma. No or weak enhancement on the arterial phase interval-delay flash image and no postvascular enhancement indicated metastasis (sensitivity, 83%; specificity, 77%).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The optimal method for vascular contrast imaging includes selection of the lowest possible MI so that bubble destruction is minimized. This allows for visualization of blood flow in tiny vessels and vessels with a slow flow velocity, as long as the continuous insonation does not destroy the bubbles. Contrast agents containing perfluorocarbon gas lend themselves optimally to this approach because the higher-density gas creates a more stable bubble. An air-based contrast agent such as SH U 508A, on the other hand, is known to have a weak harmonic response when insonated with an ultrasound beam at low MI (11). Destruction of the bubble is therefore required for its detection, rendering it a less suitable agent for continuous imaging. SH U 508A does, however, render major vessels, such as the fast-flowing hepatic arteries, visible on the PI image because they have a sufficient flow velocity to refill their volume with new bubbles between frames. We therefore asked the readers whether they could see distinct vascularity with sufficient confidence to describe its pattern. Our study showed inconsistent and generally less helpful information from the vascular image interpretation. Only in FNHs and some HCCs (26 of 33 lesions) was distinct lesional vascularity seen. Because HCCs and FNHs are recognized hypervascular lesions, we believe that SH U 508A depicts arterial flow in them only because the flow velocities are sufficiently high. Our own experience has shown that SH U 508A is not as good for the vascular assessment of focal hepatic masses as are the perfluorocarbon contrast agents (7).
The interval-delay flash and the postvascular scans, by comparison, are not dependent on continuous response of the bubbles to ultrasound. Rather, bubble disruption associated with a high-MI technique produces a bright signal in proportion to the microbubble distribution. Our study findings suggest that this enhancement is easily seen and detected, even on a single still image in vascular and postvascular phases of enhancement. The distribution of the microbubbles in these two phases is distinctly different, with the bubbles in the vascular bed in the interval-delay flash and persistent in the hepatic parenchyma on the postvascular images. By comparing the enhancement or brightness of a focal lesion in the interval-delay flash to that of the surrounding hepatic parenchyma, a simple relative assessment of their vascular volumes can be made. In our study, this interval-delay flash was highly discriminatory, showing detectable enhancement equal to or in excess of that in the adjacent normal liver in nine of 10 FNHs and 16 of 23 HCCs. Furthermore, peripheral nodular enhancement of greater intensity than that of the liver was observed by all readers in eight lesions, seven of which turned out to be hemangiomas.
The brightness of the enhancement in the interval-delay flash depends on the number of microbubbles accumulated during the delay. However, the flash that follows the brief interval delay used in this study reflects only the arterial phase of filling, since portal blood containing bubbles arrives later. We recognize that hemangiomas, for example, have a high vascular volume, but most show only minor filling in the brief delay. HCCs and FNHs, by comparison, have many arterial vessels and show substantial and rapid accumulation of contrast material during the delay.
The half-life of SH U 508A within the vascular system after injection is only 2.0–3.0 minutes. After this time, gas diffuses through the bubble shell and dissolves in the blood, effectively disappearing. There is a well-documented organ-specific phenomenon, however: SH U 508A persists in the liver after the vascular phase, which reflects an interaction between the microbubbles and the hepatic tissue–they either adhere to the hepatic vasculature or are taken into the reticuloendothelial cells. A continuous sweep through the liver with a high MI causes disruption of all the bubbles accumulated in the hepatic parenchyma, producing a bright signal corresponding to the bubble distribution. This accumulation of contrast material requires normal hepatic parenchymal architecture and would explain our finding that HCCs, hemangiomas, and metastases do not accumulate contrast agent in the postvascular phase, whereas FNHs do (Fig 1). Furthermore, because many HCCs and metastases are hypoechoic on the baseline scan and do not enhance in the postvascular phase, the greatly increased enhancement of the liver leads to increased conspicuity of the lesions.
Although FNHs and HCCs showed consistent results in all three phases of imaging, the hemangiomas and metastases did not. Seven (44%) of 16 hemangiomas did not show any vascularity, and six (38%) showed vascularity that was sparse and marginal. Marginal vascularity in the vascular phase, with a tendency for pooling or clumping of the contrast-enhanced vessels, was suggestive of hemangioma (Fig 3). The vascular pools were frequently asymmetric, often seen to one edge or margin of the lesion. In two small hemangiomas less than 1.5 cm in diameter, there was a pattern of marginal vascularity in the vascular phase and a pattern of diffuse and homogeneous enhancement in the interval-delay flash, making differentiation from HCC difficult.
Peripheral nodular enhancement on the arterial phase interval-delay flash was seen in seven (44%) of 16 of the hemangiomas and was the most specific sign for this lesion in our study. However, peripheral nodular enhancement in hemangioma would also be expected to show centripetal progression over time. The results of a recent report by Kim et al (12) show that increasing the length of the interval delay showed this progression of the enhancement toward the lesion center.
Metastases did not show uniformity of response in the vascular phase of imaging, presumably reflecting the different vascularity of the primary lesions. In five of nine lesions, we were unable to depict vascularity in the lesions. The remaining four lesions showed peripheral vascularity. However, a combination of information from the interval-delay flash and the postvascular scans showed that 83% were nonenhancing or showed diffuse weak enhancement on the interval-delay flash and were nonenhancing, with increased conspicuity on the postvascular delayed scans (Fig 7, Table 2).
The timing of the three imaging sequences is important to avoid overlap of contrast agent effects. Because adherence of the contrast agent in the hepatic parenchyma begins during the first circulation through the organ, there is some persistence involved, even in an early interval-delay sequence. We minimize this by performing interval delay right at the peak of arterial enhancement. In a similar way, we attempt to perform postvascular scanning when there is no residual contrast agent within the blood pool. Therefore, we perform postvascular scanning after an interval delay of 4.0–4.5 minutes after the completion of the bolus injection. In theory, all agent should have cleared from the blood pool by this point. Finally, the results of our study were limited by the use of a single still image for the image review. The real-time nature of a US examination allows for a better appreciation of dynamic changes, such as blood flow, and often a still image fails to capture all of the subtle findings.
Our reviewers were not asked to predict the diagnosis of the lesions studied, since the criteria proposed in Table 2 had not yet been formulated. In this study we sought to determine if simple assessments in four phases could enable differentiation of focal hepatic lesions with SH U 508A enhancement and PI imaging. Although vascular assessments were successful in a majority of hypervascular lesions as seen on the CT and MR images, vascular assessment with SH U 508A was unpredictable, difficult to perform, and nondiscriminatory. It also produced the lowest agreement between the reviewers (Table 1).
By combining the information obtained with the arterial phase interval-delay flash and the postvascular delayed scans, however, we found useful discriminatory features (Table 2). Only FNHs showed positive enhancement with both of these imaging sequences. HCCs, by comparison, enhanced on the interval-delay flash, whereas the postvascular delayed scans showed a nonenhancing lesion. No enhancement, or weak enhancement, in the interval-delay flash, with no enhancement on the postvascular delayed images, was found in 19 patients, including all eight patients with metastases who underwent successful postvascular scanning (Table 2). Metastases, like HCCs, were nonenhancing on the postvascular delayed images. Hemangiomas did not have a consistent appearance in either the vascular or postvascular phase. However, peripheral nodular enhancement in the interval-delay flash was highly specific (98%) for this diagnosis.
Results of this study show that simple assessments of SH U 508A–enhanced PI imaging provide valuable information about lesion vascularity and enhancement, which contribute positively to the characterization of a hepatic lesion with US. Future work should apply the criteria of Table 2 for the prospective evaluation of consecutive lesions in a clinical population. This will enable the diagnostic efficacy of the technique to be determined. Future readers, unlike those in the present study, should have the ability to apply these criteria together and to real-time, rather than still, US images. At the same time, ongoing technical developments to enhance sensitivity to the weak nonlinear echoes from microbubbles (13) and newer perfluorocarbon contrast agents that perform well in vascular- and liver-specific phases (14) offer hope that these preliminary results will improve in the future.
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FOOTNOTES |
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Abbreviations: FNH = focal nodular hyperplasia, HCC = hepatocellular carcinoma, MI = mechanical index, PI = pulse inversion
Author contributions: Guarantors of integrity of entire study, M.J.D.M., P.N.B., S.R.W.; study concepts and design, M.J.D.M., S.R.W.; literature research, M.J.D.M.; clinical studies, M.J.D.M., S.R.W.; data acquisition, M.J.D.M., S.R.W.; data analysis/interpretation, P.N.B., S.R.W.; statistical analysis, P.N.B.; manuscript preparation, M.J.D.M., P.N.B., S.R.W.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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V. Migaleddu, G. Virgilio, D. Turilli, M. Conti, G. Campisi, N. Canu, D. Sirigu, and I. Vincentelli Characterization of Focal Liver Lesions in Real Time Using Harmonic Imaging with High Mechanical Index and Contrast Agent Levovist Am. J. Roentgenol., June 1, 2004; 182(6): 1505 - 1512. [Abstract] |
