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1 Institute of Radiology, Udine University, Via Colugna 50, 33100 Udine,
Italy.
2 Department of Radiology, Brigham and Women's Hospital, 75 Francis St., Boston
MA 02115.
Received July 5, 2002;
accepted after revision October 3, 2002.
Address correspondence to C. Del Frate.
Abstract
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SUBJECTS AND METHODS. Twenty-six consecutive patients with findings of extrahepatic primary malignancies and liver metastases suspected on transabdominal sonography were examined with both pulse inversion harmonic imaging and ferumoxides-enhanced MR imaging within a 7-day period. Pulse inversion harmonic imaging was performed before and at 20, 100, and 180 sec after a bolus injection of Levovist. MR imaging was performed before and after ferumoxides administration, using breath-hold gradient-recalled echo T1-weighted and turbo spin-echo short tau inversion recovery T2-weighted sequences. Two radiologists independently evaluated image quality, and the number, location, and diameter of lesions scanned using both techniques. Intraoperative sonography or at least 8-month follow-up confirmed the lesions depicted. Analyses included Wilcoxon's signed rank test and Interclass correlation test.
RESULTS. Levovist-enhanced pulse inversion harmonic imaging revealed 104 metastases on the first scan after contrast injection, 126 on the second scan, and 118 on the third, compared with 66 on the unenhanced scan. Pulse inversion harmonic digital sonography depicted 90% of lesions shown on ferumoxides-enhanced MR imaging (140 metastases) (p = 0.001).
CONCLUSION. Levovist-enhanced pulse inversion harmonic digital sonography is a sensitive technique for depiction of liver metastases. Pulse inversion harmonic digital sonography may have a potential role in imaging patients with possible metastatic involvement of the liver. Further studies are needed to define its place in the workup of these patients. At present, ferumoxides-enhanced MR imaging, being more sensitive, must be performed in all patients in whom pulse inversion harmonic digital sonography is not conclusive or when after pulse inversion harmonic digital sonography, patients remain eligible for surgery.
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Recently, contrast-enhanced sonography with stimulated acoustic emission has been shown to be useful in the depiction of otherwise occult liver metastases [6, 7].
Levovist ([SH U 508A] Schering, Berlin, Germany), a microbubble sonographic contrast agent approved in Italy, can produce a reliable and clinically useful systemic Doppler enhancement on sonography after IV injection. In addition to its vascular phase, Levovist is also shown to have a hepatosplenic-specific parenchymal phase after blood pool clearance. Contrast-enhanced sonography with pulse inversion harmonic digital sonography has been shown to improve the depiction of occult liver metastases [6, 7]. The sensitivity of this technique for subcentimetric lesions was reported to be higher than that of dualphase helical CT [7, 8], even though these studies are preliminary, and especially in the study by Harvey et al. [7], the CT methodology was not the optimal one. Nevertheless, on the basis of these results, this new technique may have a potential role in the depiction of liver metastases in those patients who are candidates for liver metastasectomy.
At this time, liver-specific contrast-enhanced MR imaging has been shown to be the most accurate technique in the depiction of liver metastases, and it is comparable to arterial portography CT in several reports [9, 10]. Among the several liver-specific contrast agents currently commercially available, we used ferumoxides (Ferridex, Endorem, Guerbet, France). Ferumoxides, a superparamagnetic iron oxide contrast agent, was the first liver-specific contrast agent to enter clinical trials and the first to achieve marketing approval by the United States Food and Drug Administration [11]. Several reports show the diagnostic efficacy of ferumoxides-enhanced MR imaging for the depiction of liver metastases [12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25].
The purpose of our study was to compare the sensitivity of contrast-enhanced pulse inversion harmonic digital sonography with that of unenhanced transabdominal sonography and with that of liver-specific contrast-enhanced MR imaging. In addition, pulse inversion harmonic digital sonography was performed at different scanning times after Levovist administration to define which phase offers the highest rate of lesion depiction.
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All patients underwent pulse inversion harmonic digital sonography and ferumoxides-enhanced liver MR imaging within a 7-day period. Inclusion criteria were age greater than 18 years; providing of informed consent; and the presence of a primary malignancy, hepatic metastases suspected on sonography, or solely hepatic metastases shown on CT. Exclusion criteria were pregnancy or breast-feeding, contraindications to MR imaging, known allergy to dextran, renal failure (creatinine level > 1.5 mg/dL), splenomegaly, and galactosemia. The histologic diagnosis of the primary malignancy was colon carcinoma (n = 12), rectal carcinoma (n = 7), breast carcinoma (n= 3), gastric adenocarcinoma (n = 2), esophageal carcinoma (n = 1), and pancreatic adenocarcinoma (n = 1). Twenty-five of 26 patients were diagnosed with liver metastases after both examinations. In one patient who underwent mastectomy 2 years before for breast cancer and who had carcinomatous mastitis on the residual breast at the time of the examination, a small liver lesion never before depicted was found. This lesion was characterized on both pulse inversion harmonic digital sonography and ferumoxides-enhanced MR imaging as a small hemangioma. Follow-up performed with both sonography and MR imaging (at 3 and 12 months) confirmed the benign nature of the lesion.
Fourteen of 25 patients were eligible for surgery after both examinations and underwent intraoperative sonography performed immediately preoperatively with a linear array, broadband 7.5- to 10-MHz transducer (AU5 ESAOTE SpA, Genova, Italy) by a surgeon qualified in sonography. After intraoperative sonography, 13 patients underwent metastasectomy, and the lesions depicted on imaging were pathologically confirmed to be metastases. In all cases, pathology was consistent with the respective known primary malignancy. In the other 12 patients, the lesions depicted were confirmed to be enlarging by at least 8-months' follow-up performed with both sonography and ferumoxides-enhanced MR imaging.
Pulse Inversion Harmonic Imaging
A commercially available scanner (HDI-5000; ATL, Bothell, WA) with a
broadband 2- to 5-MHz transducer was used. All examinations were performed by
two radiologists who were experienced in sonography and aware of the findings
obtained on transabdominal sonography but unaware of the CT findings.
A baseline transabdominal B mode sonography was initially performed to confirm the previously reported findings. Initially, a suitable acoustic window was identified to cover all the liver volume in one or two transverse scans with minimal blind areas; usually the best acoustic windows were obtained using oblique undercostal scans with the patient in a supine position, even though some patients may have required a longitudinal, axial, or lateral decubitus scan to be better examined. Then, the sonographic apparatus was set for pulse inversion harmonic digital sonography, which was performed using a CSI-3 harmonic preset, low frame rate (5 Hz), and high mechanical index (1.1–1.3). With these parameters, bubble destruction occurs, and a high-intensity transient wideband signal is produced. A bolus of 4 g of Levovist was injected at a concentration of 400 mg/mL followed by a 10-mL normal saline flush, with an injection rate of 0.5 mL/sec. One or two rapid scans covering the entire liver volume were obtained with delays of 20, 100, and 180 sec after bolus injection of Levovist. The time necessary to perform the study and to interpret the stored images was monitored.
MR Imaging
All patients underwent MR imaging of the liver within a 7-day period after
pulse inversion harmonic digital sonography. Images were obtained with a 1-T
superconductive system (Magnetom Impact; Siemens, Erlangen, Germany) using a
body coil. The examinations were performed using the following sequences:
gradient-recalled echo T1-weighted breath-hold sequence acquired in the axial
plane (TR/TE, 148.4/5.0; matrix, 80 x 256; number of excitations, 1;
rectangular field of view, 5; field of view, 8; slice thickness, 8 mm; gap,
20%; acquisition time, 14 sec). Patients were required to breath-hold after an
incomplete expiration. The entire liver was covered with two or three
breath-holds, depending on the craniocaudal extension of the liver using a
turbo spin-echo short tau inversion recovery (STIR) T2-weighted sequence
acquired in the axial plane (5100/90; inversion time, 120 msec; matrix, 196
x 256; number of excitations, 3; rectangular field of view, 6; field of
view, 8; slice thickness, 8 mm; gap, 20%; acquisition time, 5 min 43 sec).
Each patient underwent MR imaging twice, before and 60 min after ferumoxides administration. Both examinations were performed using the same protocol and both gradient-recalled echo T1-weighted and turbo spin-echo STIR T2-weighted sequences. Ferumoxides was administered to all patients at a dose of suspension of 0.075 mL/kg of body weight, corresponding to an iron concentration of 15 mmol/kg of body weight. The suspension was diluted in a 100-mL solution of 5% glucose and perfused with a slow IV infusion during 30 min.
Evaluation of Images
Pulse inversion harmonic imaging.—All sonograms were stored
digitally on a magnetic optical disk and reviewed offline using specifically
designed software (HDIlab; ATL). Corresponding images from different scans
obtained before and after contrast administration were compared.
For subjective analyses, two radiologists unaware of MR imaging results, with 4 and 20 years of experience in abdominal liver sonography, evaluated the following findings independently: lesion conspicuity, by comparing fundamental B mode sonography and pulse inversion harmonic digital sonography obtained at 20, 100, 180 sec after Levovist injection (lesion conspicuity on sonography was considered excellent when lesions presented an echogenicity very different from liver parenchyma; good, when they were well visualized but the difference in echogenicity with the liver was lower; moderate, when lesions were almost isoechoic to the liver parenchyma; and poor, when they were barely visible); lesion depiction, by comparing pulse inversion harmonic digital sonography obtained before and at 20, 100, 180 sec after Levovist injection. For each scan, each reviewer considered the number, the location (according to the Couinaud segmental classification [26]), and the size of the lesions depicted. A lesion was considered real only if both observers detected it.
MR imaging.—Two radiologists, different from the ones who evaluated pulse inversion harmonic digital sonography, with 4 and 12 years of experience in liver MR imaging, reviewed the MR images using unenhanced and ferumoxides-enhanced sequences and were unaware of the results of pulse inversion harmonic digital sonography. Each radiologist considered number, location (according to the Couinaud segmental classification [26]), and size of the lesions depicted. A lesion was considered real only if both observers detected it.
Statistical Analysis
Because the Shapiro-Wilk test failed to give sufficient evidence of the
normality of the data distributions, statistical analysis was performed using
the Wilcoxon's signed rank test for paired observations, considering a
p value of 0.05 to be statistically significant. The total number of
lesions depicted with pulse inversion harmonic digital sonography was compared
with the number depicted on ferumoxides-enhanced MR imaging.
Correlation between the different reviewers was evaluated using the Interclass correlation test, and confidence intervals were calculated.
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In one patient, the only lesion depicted showed a peripheral enhancement during the first scan at 20 sec after Levovist injection and was still completely hyperechoic in comparison with the surrounding liver parenchyma during the last scan at 180 sec after Levovist injection. This typical enhancement was seen in three other lesions depicted in two different patients and allowed us to characterize the lesions as hemangiomas. In all cases, ferumoxides-enhanced MR imaging confirmed the diagnosis, and the follow-up studies confirmed the stability of these lesions.
Increased lesion conspicuity in comparison with that on the unenhanced scan was observed using pulse inversion harmonic digital sonography during all three scans obtained at 20, 100, and 180 sec after Levovist injection. The increased conspicuity was the effect of the enhancement of normal liver parenchyma. The maximal lesion conspicuity was observed during the second scan at 100 sec after Levovist injection. The lesion conspicuity appeared to be reduced during the first scan at 20 sec, when the parenchymal enhancement was greatest but heterogeneous. During the third scan, obtained at 180 sec after Levovist injection, the lesion conspicuity was reduced (Fig. 4) in comparison with that of the second scan but was still good. Nevertheless, in two patients with fatty liver, the normal liver parenchyma was bright during unenhanced sonography, with relatively hypoechoic lesions; after Levovist injection during pulse inversion harmonic digital sonography, no improvement of lesion conspicuity was shown.
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In summary, in comparison with unenhanced sonography, in only one patient (3.85%) of 26 was a decrease in conspicuity of some lesions observed (otherwise, in the same patient more lesions were revealed after Levovist injection); in two (7.69%) of 26 patients, no changes in conspicuity were observed (otherwise, the conspicuity of lesion was high already in unenhanced sonography); in two (7.69%) of 26 patients, pulse inversion harmonic digital sonography could not show any definite lesion because of the body habitus of the patients; in 21 (80.77%) of 26 patients, an increase in lesion conspicuity was observed in all contrast-enhanced scans, in particular in the scan obtained at 100 sec after Levovist injection.
Lesion depiction.—In 14 (53.8%) of 26 patients, pulse inversion harmonic digital sonography after contrast administration depicted the same number of lesions as unenhanced sonographic imaging: one lesion in each of seven patients (one of these lesions was a hemangioma), two lesions in three patients, three lesions in two patients, and no lesions in two obese patients. The size of these lesions was between 10 and 45 mm.
In only one (3.85%) of 26 patients, pulse inversion harmonic digital sonography revealed one lesion fewer than unenhanced sonography had revealed. The scan obtained after Levovist injection was of an 8-mm isoechoic lesion with a hypoechoic border, located in segment VIII, close to the surface of the liver dome, in a blind area. Otherwise, this patient had six other metastatic lesions, and this missed lesion did not change management decisions.
In 11 (42.30%) of 26 patients, pulse inversion harmonic digital sonography after Levovist administration depicted more lesions than unenhanced sonography. Lesions shown only after Levovist injection measured from 3 to 20 mm (mean diameter, 9 mm) (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 2A, 2B, 2C, 2D, 3A, 3B, 3C, 3D).
In four patients (15.38%), pulse inversion harmonic digital sonography after contrast injection revealed one to six lesions more than unenhanced sonography (zero or two lesions) and resulted in changing the management of these patients. In the other seven patients, pulse inversion harmonic digital sonography revealed more lesions (one to 30) than unenhanced sonography (> four), but this finding did not change the management of patients because of diffuse metastatic involvement.
After pulse inversion harmonic digital sonography, 14 patients were considered eligible for surgery, whereas two patients without lesions were considered eligible for follow-up.
Considering the number of metastases depicted at pulse inversion harmonic digital sonography on each scan after Levovist administration compared with the unenhanced scan, we had an increase in metastases depiction of 57.6% in the scans at 20 sec (66–104 metastases) after Levovist injection, of 90% (66–126 lesions) in the scans at 100 sec, and of 78.8% (66–118 lesions) in the scans at 180 sec. In our experience, the greatest number of lesions was depicted during the second scan at 100 sec after Levovist injection. Four hemangiomas were depicted in all scans. The correlation between the two reviewers was excellent, with an Interclass correlation test of 0.9976 (CI, 0.9946–0.9989).
The time required to perform the study ranged from 10 to 15 min (mean time, 13 min), whereas the time spent to interpret the images ranged from 10 to 20 min (mean time, 16 min).
Pulse Inversion Harmonic Digital Sonography Versus
Ferumoxides-Enhanced MR Imaging
Ferumoxides-enhanced MR imaging revealed 144 lesions, 140 metastases, and
four hemangiomas. The correlation between the two reviewers was excellent,
with an Interclass correlation index of 0.9992 (CI, 0.9982-0.9996), higher
than that obtained for Levovist-enhanced pulse inversion harmonic digital
sonography.
All four hemangiomas were markedly hyperintense on unenhanced T2-weighted sequences, and, after ferumoxides administration, all hemangiomas showed uptake of contrast media and resulted in a marked drop in signal intensity.
Pulse inversion harmonic sonography depicted 90.27% of the lesions revealed on ferumoxides-enhanced MR imaging: four of four hemangiomas and 126 of 140 metastases. Nevertheless, a statistically significant difference (p = 0.001) was shown between the number of metastases depicted on pulse inversion harmonic digital sonography and ferumoxides-enhanced MR imaging.
In 22 (84.61%) of 26 patients, ferumoxides-enhanced MR imaging did not change the management of the patients despite revealing up to seven more lesions than pulse inversion harmonic digital sonography (Figs. 1A, 1B, 1C, 1D, 1E and 1F). In two patients (7.69%) in whom pulse inversion harmonic digital sonography showed only one lesion each, ferumoxides-enhanced MR imaging revealed three lesions in one patient and two in the second patient. In these patients, their management changed because the lesions were located in different lobes of the liver and the patients were therefore no longer considered eligible for surgery. In two other obese patients (7.69%) in whom pulse inversion harmonic digital sonography could not show any lesions, MR imaging showed four metastases, two visible only after ferumoxides administration; this finding changed the management of these patients.
After ferumoxides-enhanced MR imaging, only 14 patients were considered eligible for surgery instead of 16 identified by pulse inversion harmonic imaging.
Intraoperative Sonography and Follow-Up
Fourteen of 25 patients were eligible for surgery after both imaging
modalities and underwent intraoperative sonography before surgery. Findings of
intraoperative sonography confirmed the lesions depicted on imaging in 13
patients who underwent surgery with pathologic confirmation. In one patient,
intraoperative sonography confirmed the three lesions depicted on imaging but
visualized two small (3- and 4-mm) additional metastases (false-negative
finding on imaging) on the surface of the liver; the patient was then no
longer eligible for surgery. In the other 11 patients, the follow-up
(8–16 months) performed using both sonography and ferumoxides-enhanced
MR imaging in every patient confirmed the enlargement of the lesions initially
depicted by both imaging modalities.
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Pulse inversion harmonic digital sonography, a recently introduced digital sonographic technique, has been shown to improve the depiction of liver metastases. After administration of a microbubble contrast agent, microbubbles accumulate in the normal liver and spleen parenchyma within a few minutes, and being stationary in this phase, they cannot be depicted by conventional Doppler sonography [6, 28]. When properly insonated, microbubbles interact with the ultrasound beam in different ways. At low acoustic powers, they reflect sonographic echoes; at increasing powers or mechanical index, microbubbles display nonlinear scattering properties, producing harmonic components. At higher powers, bubble destruction occurs [29]. Parenchymal tissues, such as the liver, generate few harmonic components. The analysis of the harmonic components of the sonographic signal after Levovist administration using the high mechanical index of the ultrasound beam permits the signal-to-noise ratio between the tissues to increase where the microbubbles have accumulated and also in the areas where they are not present. Pulse inversion harmonic digital sonography is a relatively new imaging technique coupled with sonographic contrast administration that relies on nonlinear bubble behavior to increase image contrast. Two trains of out-of-phase pulses are sent, and the returning echoes are summed. Linear scatters, such as those produced by parenchymal tissues, respond equally to both pulses. Because the two trains of waves are out of phase, the returning waves are equal in shape and opposite, and their addition results in a cancellation. On the contrary, microbubbles produce different responses to the two pulse trains, and their addition results in a strong residual signal [8].
The exact site of the normal liver parenchyma where microbubbles accumulate (sinusoids or reticuloendothelial cells) is not yet known, but microbubbles are not present in primary liver malignancies and, in particular, in liver metastases [7]. Liver malignancies appear as hypoechoic lesions surrounded by normal liver parenchyma, which becomes more echogenic as a result of the accumulation of microbubbles [7].
Previous studies indicate that pulse inversion harmonic digital sonography seems to be superior to dual-phase helical CT in the depiction of subcentimetric liver metastases [6, 7, 8], even though these studies are preliminary with sometimes suboptimal CT methodology. On the basis of these preliminary studies, contrast-enhanced pulse inversion harmonic digital sonography has the potential to become the principal examination for the depiction of liver metastases in those patients for whom the routine helical CT excluded other metastatic sites and who are therefore candidates for metastasectomy.
The sensitivity of pulse inversion harmonic digital sonography, however, has never been compared with that of liver-specific contrast-enhanced MR imaging, currently considered the most sensitive and noninvasive imaging modality to depict liver metastases, superior to CT, and comparable to CT arterial portography [9, 10]. We investigated the capability of pulse inversion harmonic digital sonography to depict liver metastases in comparison with transabdominal gray-scale sonography and ferumoxides-enhanced MR imaging.
Pulse inversion harmonic digital sonography was performed before and at 20, 100, and 180 sec after Levovist injection. Increased lesion conspicuity in comparison with unenhanced sonography was observed on pulse inversion harmonic digital sonography on all three scans obtained after Levovist administration, as a result of the normal liver parenchyma enhancement. The maximal lesion conspicuity observed during the second scan at 100 sec after Levovist injection confirmed several reports that indicated that the liver-specific phase of Levovist was observed 2–5 min from the beginning of injection [30, 31]. The lesion conspicuity appeared to be reduced during the first scan at 20 sec, in which the parenchymal enhancement was maximal but heterogeneous, probably because in this phase the microbubbles are still arriving through the vessels and accumulating in the normal liver parenchyma. In this phase, the presence of microbubbles inside the vessels, imaged in the axial plane, also mimics the presence of round hyperechoic lesions with hypoechoic borders, interpretable as potential metastases. This pitfall, however, can easily be avoided by comparing, as we did, the scans obtained after Levovist injection with the unenhanced scan. During the third scan, obtained at 180 sec after Levovist injection, the lesion conspicuity is reduced in comparison with the second scan but still good. Most lesions were depicted during the second scan at 100 sec after Levovist injection, with an increase in depiction of 90% (66–126 lesions) in comparison with unenhanced sonography.
In our early experience, we realized that in some selected cases, pulse inversion harmonic digital sonography could not increase the conspicuity of the lesions, such as in fatty livers in which the diffuse hyperechogenicity of the liver parenchyma offered an optimal contrast with the metastatic lesions on unenhanced sonography. In these patients, the administration of Levovist did not increase the conspicuity of the lesions because there was no increase in hyperechogenicity of the surrounding parenchyma, which is hyperechoic because of the presence of fat. Moreover, in the less frequent cases in which the metastases appeared hyperechoic with a thin hypoechoic rim and an optimal contrast with the surrounding liver parenchyma on unenhanced sonography, after Levovist injection the parenchyma surrounding the lesions became hyperechoic, reducing the conspicuity of the metastases.
In our study, in 14 (53.8%) of 26 patients, there was complete agreement between unenhanced sonography and pulse inversion harmonic digital sonography after contrast media administration. Pulse inversion harmonic digital sonography revealed more lesions than unenhanced sonography in 11 (42.3%) of 26 patients; in four of them, pulse inversion harmonic digital sonography changed the therapeutic approach. In only one (3.85%) of 26 patients, pulse inversion harmonic digital sonography revealed one lesion fewer than unenhanced sonography; however, this finding did not change the management of the patient. Despite the fact that pulse inversion harmonic digital sonography has some disadvantages compared with gray-scale sonography, such as lack of different possible approaches or views and the presence of artifacts due to heterogeneous bubble collapse, it is, however, much more sensitive in the depiction of liver metastases.
In our series, pulse inversion harmonic digital sonography depicted 90% (126 vs 140) of the metastases revealed on ferumoxides-enhanced MR imaging, showing a high sensitivity. However, a statistically significant difference (p = 0.001) was still shown between the number of lesions revealed on pulse inversion harmonic digital sonography and ferumoxides-MR imaging, showing once more the superiority of the latter technique. On the other hand, contrast-enhanced pulse inversion harmonic digital sonography is less time-consuming than ferumoxide-enhanced MR imaging, requiring on average 14 min instead of 80 min.
In 22 (84.61%) of 26 patients, ferumoxides-enhanced MR imaging did not change the management of the patients even if it depicted more lesions than pulse inversion harmonic digital sonography. In only four (15.38%) of 26 patients, ferumoxides-enhanced MR imaging changed the therapeutic approach compared with contrast-enhanced pulse inversion harmonic digital sonography, and two were obese patients in whom both standard transabdominal sonography and pulse inversion harmonic imaging could not show any definite lesions.
The present study has several limitations. The first limitation is the small number of patients, and the second one is the lack of state-of-the-art MR imaging equipment. In fact, the use of a body coil with a slice thickness of 8 mm and 20% overlap may affect the depiction of small metastases, decreasing the sensitivity of ferumoxides-enhanced MR imaging compared with pulse inversion harmonic digital sonography.
In conclusion, these preliminary data show that pulse inversion harmonic digital sonography is a sensitive technique in the depiction of liver metastases and may have a potential role in the examination of patients with metastatic involvement of the liver (when helical CT previously excluded other extrahepatic metastases). To define the place of pulse inversion harmonic digital sonography in the workup of metastatic liver disease requires multiple studies with more patients, comparing this technique with multidetector CT and MR imaging. In particular, the use of state-of-the-art MR imaging equipment with a phased array coil and thinner slice thickness for both T1- and T2-weighted sequences should be considered.
However, at the present time, pulse inversion harmonic imaging may not substitute for ferumoxides-enhanced MR imaging in the depiction of liver metastases. In fact, in our preliminary experience, ferumoxides-enhanced MR imaging may change change the management and therapeutic approach in many patients, in particular in patients in whom pulse inversion harmonic digital sonography is not conclusive or when after pulse inversion harmonic digital sonography, the patients remain eligible for surgery.
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