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DOI:10.2214/AJR.06.1060
AJR 2007; 189:W7-W12
© American Roentgen Ray Society

Clinical Observations

Enhancement Patterns of Focal Liver Masses: Discordance Between Contrast-Enhanced Sonography and Contrast-Enhanced CT and MRI

Stephanie R. Wilson1, Tae Kyoung Kim1, Hyun-Jung Jang1 and Peter N. Burns2,3

1 Department of Medical Imaging, Toronto General Hospital, 585 University Ave., Toronto, ON, Canada, M5G 2N2.
2 Department of Medical Biophysics, University of Toronto, ON, Canada.
3 Department of Imaging Research, Sunnybrook Health Sciences Centre, Toronto, ON, Canada.

Received August 14, 2006; accepted after revision December 6, 2006.

 
Supported by the Canadian Institutes of Health Research and the Terry Fox Programme of the National Cancer Institute of Canada.

Address correspondence to S. R. Wilson (stephanie.wilson{at}uhn.on.ca).

WEB

This is a Web exclusive article.


Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to investigate the origin of the infrequent discordance between the contrast enhancement patterns of liver lesions on sonography and those on CT and MRI. Forty-four discordant cases were reviewed retrospectively.

CONCLUSION. Four categories of discordance were identified, one of which is unexplained. Contrast agent diffusion caused portal venous phase discordance in malignant tumors (n = 6) whereby CT and MRI contrast material diffused through the vascular endothelium into the tumor interstitium, concealing washout. Sonographic microbubbles were purely intravascular and showed washout. Arterial phase timing discordance occurred in metastatic lesions (n = 10) with hypervascularity and rapid washout on contrast-enhanced sonography. CT arterial imaging performed later showed hypovascularity. Rapidly enhancing hemangiomas (n = 7) exhibited hypervascularity on CT when contrast-enhanced sonography also showed peripheral nodules and fast centripetal progression. Discordance caused by fat in lesions (n = 4) or liver (n = 10) reflected the inherent echogenicity of fat on sonography compared with its low attenuation on CT and low signal intensity on MRI. Infrequent cases of discordance remain unexplained. Recognition of the cause of the infrequent disagreement in enhancement patterns on contrast-enhanced sonography with those on CT and MRI improves diagnostic interpretation.

Keywords: contrast media • CT • liver disease • sonography


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Low-mechanical-index continuous real-time scanning is well established for evaluation of liver lesions with contrast-enhanced sonography. In this technique, enhancement of the lesion is compared with that of the adjacent liver parenchyma, as is done in contrast-enhanced CT and MRI. The low mechanical index minimizes microbubble loss, allowing continuous real-time imaging for several minutes. Nonlinear imaging methods suppress the tissue echo so that as the microbubbles enter the imaged region after IV injection of a small bolus, any increase in echogenicity in either the lesion or the liver is ascribed to microbubbles within the vasculature [1].

When patterns of contrast enhancement on sonography are compared with those on CT and MRI, a high level of agreement in type and pattern of enhancement is seen if the liver imaging procedures are performed in close temporal relation [2–4]. Nonetheless, occasional instances of discordance occur, and the causes of such disagreement between imaging methods have not been documented, to our knowledge. In this study, explained discordance between contrast enhancement patterns on sonography and those on CT and MRI was categorized. In rare instances, discordance remains unexplained.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
Over a 5-year period of routine contrast-enhanced sonography performed for characterization of focal liver masses, 44 nonconsecutive cases of discordance between sonograms and contrast-enhanced CT and MR images were identified as illustrative of differences in enhancement patterns. Our routine practice includes comparison of documented findings of all imaging examinations, from which these cases were selected. This retrospective study had research ethics board approval for chart review, and the requirement for informed consent was waived. Review was performed to classify discordance on the basis of physical characteristics and final diagnosis.

Imaging Techniques
Contrast-enhanced sonography was performed with a perflutren microsphere contrast agent (Definity, Bristol-Myers Squibb). Multiple small boluses of 0.1–0.3 mL were given to a maximum dose of 10 µL/kg. Low-mechanical-index continuous real-time sonography was performed with contrast-specific nonlinear technique on Acuson Sequoia (Siemens Medical Solutions) (n = 23), HDI5000 (n = 11) and iU22 (n = 3) (Philips Medical Systems), and Aplio80 (Toshiba) (n = 7) systems. The small bolus did not enter the vein until completion of a 5-mL saline flush, which takes less than 5 seconds. Completion of the flush was recorded as time zero. Dynamic scanning focused on the lesion was performed continuously from the arterial phase wash-in of contrast material to the peak of arterial enhancement and then to 300 seconds. Portal venous images were chosen from 45 to 90 seconds, and delayed images were chosen from 90 to 300 seconds. Two consecutive 15-second cine clips at a frame rate of 10–14 Hz were recorded from wash-in to show the arterial features to the peak of enhancement.

CT scans were obtained with 4-MDCT (Light-Speed QX/I, GE Healthcare), 8-MDCT (LightSpeed Ultra, GE Healthcare), and 64-MDCT (Aquillion, Toshiba) scanners. The amount of IV iohexol (Omnipaque 300, GE Healthcare) or iodixanol (Visipaque 320, GE Healthcare) given was 2 mL/kg to a maximum of 200 mL at an injection rate of 5 mL/s. Reconstruction was performed with a standard algorithm at a slice thickness of 5 mm and 50% overlap. Our standard protocol for triphasic CT consisted of an unenhanced, arterial phase with a scanning delay of 30–40 seconds, and a portal venous phase with a scanning delay of 60–80 seconds.

MRI was performed on a 1.5-T system (Echo-speed LX, GE Healthcare) with a phased-array torso coil. The standard protocol included T2-weighted images with variable echo time, dual-echo in and out phase spoiled gradient-echo T1-weighted images, and dynamic 2D fast spoiled gradient-echo images (minimum TE, 150–200; flip angle, 80°; slice thickness, 5–8 mm; acquisition time, 24 seconds) at unenhanced, arterial (15-second delay), portal venous (50-second delay), late portal venous (85-second delay), and delayed (300-second delay) phases. Gadodiamide (Omniscan, GE Healthcare), 0.1 mmol/kg, was hand-injected IV and followed by a saline flush.

Analysis
Images were evaluated by three radiologists, and discordance was classified by consensus. The comparison was confined to visual observations regarding degree of enhancement (echogenicity on sonography, attenuation on CT, signal intensity on MRI) of the lesion relative to the liver in the arterial and portal venous phases and the behavior of this enhancement with time. Discordance was considered present if the interpretation of the enhancement of the lesions relative to the adjacent liver on contrast-enhanced sonography differed from the interpretations on contrast-enhanced CT and MR images. Each category was further analyzed in regard to observed differences in enhancement appearance, including lesion diagnosis, timing of enhancement, and information from unenhanced sonograms, CT scans, and MR images. No statistical analysis was appropriate for this subjective retrospective review.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The categories of discordance are summarized in Table 1. Three categories have proposed explanations. We could not explain a fourth category.


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  		TABLE 1: Manifestations of Discordance and Explanations with Final Pathologic Correlation

 

Contrast Agent Diffusion
In six cases, washout was seen on contrast-enhanced sonography, during which the lesion appeared hypoechoic relative to the liver in the portal venous phase, yet no similar washout was seen on contrast-enhanced CT or MRI (Figs. 1A, 1B, 1C, 1D, 1E, and 1F). In some cases, CT or MRI contrast enhancement in the lesion increased between the arterial and portal venous phases. The patients had biopsy-proven cholangiocarcinoma (n = 4) or metastasis (n = 2).


Figure 1
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  		Fig. 1A —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Axial phase sonography (A), CT (B), and MRI (C) images all show heterogeneous enhancement.

 

Figure 2
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  		Fig. 1B —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Axial phase sonography (A), CT (B), and MRI (C) images all show heterogeneous enhancement.

 

Figure 3
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  		Fig. 1C —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Axial phase sonography (A), CT (B), and MRI (C) images all show heterogeneous enhancement.

 

Figure 4
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  		Fig. 1D —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Portal venous phase imaging is discordant, with sonography (D) showing washout but CT (E) and MRI (F) both showing increased lesional enhancement. Biopsy confirmed malignant cholangiohepatoma. It is hypothesized that portal phase enhancement in CT (E) and MRI (F) indicates contrast material in tumor interstitium.

 

Figure 5
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  		Fig. 1E —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Portal venous phase imaging is discordant, with sonography (D) showing washout but CT (E) and MRI (F) both showing increased lesional enhancement. Biopsy confirmed malignant cholangiohepatoma. It is hypothesized that portal phase enhancement in CT (E) and MRI (F) indicates contrast material in tumor interstitium.

 

Figure 6
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  		Fig. 1F —29-year-old man with lipase deficiency exhibiting portal venous phase discordance due to diffusion of contrast agent. Portal venous phase imaging is discordant, with sonography (D) showing washout but CT (E) and MRI (F) both showing increased lesional enhancement. Biopsy confirmed malignant cholangiohepatoma. It is hypothesized that portal phase enhancement in CT (E) and MRI (F) indicates contrast material in tumor interstitium.

 
Timing
Two variations of discordance were due to timing. In the first type (n = 10), a mass was seen as hypervascular in the arterial phase of contrast-enhanced sonography but hypovascular on contrast-enhanced CT or MRI. In the portal venous phase of all three techniques, these lesions exhibited washout. All lesions in this category had a final diagnosis of metastasis, which exhibited rapid arterial enhancement and rapid washout on contrast-enhanced sonography (Figs. 2A, 2B, and 2C). The peak enhancement of metastatic lesions occurred much earlier than the typical arterial phase of contrast-enhanced CT and MRI. This peak enhancement was detected only with real-time contrast-enhanced sonography, as shown in the quantitative measurement of echo level in relation to time (Fig. 2D). All three techniques, however, would show a hypovascular mass were they acquired at the same point in the arterial phase.


Figure 7
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  		Fig. 2A —46-year-old woman with metastatic colon cancer exhibiting discordance due to timing of imaging. Axial contrast-enhanced sonograms obtained 10 (A) and 18 (B) seconds after initiation of contrast injection show initial hypervascularity (A) followed by rapid washout as contrast enhancement of liver parenchyma progressively increases.

 

Figure 8
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  		Fig. 2B —46-year-old woman with metastatic colon cancer exhibiting discordance due to timing of imaging. Axial contrast-enhanced sonograms obtained 10 (A) and 18 (B) seconds after initiation of contrast injection show initial hypervascularity (A) followed by rapid washout as contrast enhancement of liver parenchyma progressively increases.

 

Figure 9
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  		Fig. 2C —46-year-old woman with metastatic colon cancer exhibiting discordance due to timing of imaging. Arterial phase axial CT scan shows same metastasis as hypovascular mass. CT scan is timed to miss transient hypervascularity in early arterial phase.

 

Figure 10
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  		Fig. 2D —46-year-old woman with metastatic colon cancer exhibiting discordance due to timing of imaging. Graph shows quantitative measurement of enhancement from contrast-enhanced sonogram. Metastatic lesion fills rapidly to peak and washes out within 5 seconds of initiation of arterial enhancement in hepatic parenchyma. Lesion becomes enhanced at lower level than liver for rest of arterial phase. Typical timing for arterial phase contrast-enhanced CT image is indicated.

 

The second variation of timing discordance (n = 7) showed arterial phase peripheral nodular enhancement with rapid centripetal progression on contrast-enhanced sonography but uniform arterial phase hypervascularity on contrast-enhanced CT or MRI (Figs. 3A, 3B, 3C, and 3D). All lesions were rapidly enhancing hemangiomas. Analysis of the timing of the arterial phase of contrast-enhanced sonography showed that enhancement of the lesions was similar to their appearance on CT if only a single frame of contrast-enhanced sonography was included that was acquired at the time of the CT arterial phase image.


Figure 11
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  		Fig. 3A —34-year-old man with asymptomatic rapidly enhancing hemangioma exhibiting discordance due to differences in timing. Contrast-enhanced sonography was performed after outside CT, which suggested focal nodular hyperplasia. Sequential contrast-enhanced sonographic frames at 6 seconds (A), 9 seconds (B), and 17 seconds (C) in arterial phase show marginal enhancement, peripheral nodular enhancement, and centripetal progression of enhancement sustained for remainder of period of observation to 300 seconds.

 

Figure 12
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  		Fig. 3B —34-year-old man with asymptomatic rapidly enhancing hemangioma exhibiting discordance due to differences in timing. Contrast-enhanced sonography was performed after outside CT, which suggested focal nodular hyperplasia. Sequential contrast-enhanced sonographic frames at 6 seconds (A), 9 seconds (B), and 17 seconds (C) in arterial phase show marginal enhancement, peripheral nodular enhancement, and centripetal progression of enhancement sustained for remainder of period of observation to 300 seconds.

 

Figure 13
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  		Fig. 3C —34-year-old man with asymptomatic rapidly enhancing hemangioma exhibiting discordance due to differences in timing. Contrast-enhanced sonography was performed after outside CT, which suggested focal nodular hyperplasia. Sequential contrast-enhanced sonographic frames at 6 seconds (A), 9 seconds (B), and 17 seconds (C) in arterial phase show marginal enhancement, peripheral nodular enhancement, and centripetal progression of enhancement sustained for remainder of period of observation to 300 seconds.

 

Figure 14
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  		Fig. 3D —34-year-old man with asymptomatic rapidly enhancing hemangioma exhibiting discordance due to differences in timing. Contrast-enhanced sonography was performed after outside CT, which suggested focal nodular hyperplasia. Axial arterial phase CT image obtained 35 seconds after contrast administration shows uniformly enhanced mass. Diagnostic considerations include hemangioma and focal nodular hyperplasia. Mass exhibited sustained enhancement in portal venous phase on both sonogram and CT scan.

 
Discordance Due to Fat
Discordance occurred in cases with a large deposit of fat. The results depended on whether the fat was in the lesion or in the liver parenchyma. In the four cases in which a lesion contained fat (one lipoma, one angiomyolipoma, and two adenomas), contrast-enhanced sonography showed greater relative enhancement of the lesion through all phases of enhancement. This finding was discordant with the contrast enhancement on CT and MRI, both of which showed less relative enhancement of the mass compared with the liver. In Figures 4A, 4B, 4C, 4D, 4E, and 4F, the baseline and contrast-enhanced images show a hyperechogenic mass from which it is impossible to determine the degree of vascularity of the lesion. The unenhanced CT scan shows a mass with less attenuation than the adjacent liver tissue, which continues to be evident after injection of the contrast agent. Similarly, highly echogenic fatty livers on baseline sonograms (n = 10) showed apparent brightness or echogenicity throughout sonographic contrast enhancement. This finding was discordant with the CT and MRI findings, which showed the liver as having less attenuation or signal intensity than the expected norm.


Figure 15
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  		Fig. 4A —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Baseline sonogram shows highly echogenic mass in posterior aspect of right lobe of liver. Profound echogenicity and disruption of diaphragmatic echo distal to mass raise possibility of fat-containing mass.

 

Figure 16
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  		Fig. 4B —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Arterial phase sonogram at peak of enhancement shows hypervascularity in lesion.

 

Figure 17
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  		Fig. 4C —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Portal venous phase image shows echogenic mass. Liver has become enhanced. Without quantification, it is impossible to determine whether mass has washed out.

 

Figure 18
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  		Fig. 4D —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Unenhanced axial CT image corresponding to A shows low-attenuation (–41 H) mass consistent with presence of fat.

 

Figure 19
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  		Fig. 4E —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Arterial phase CT image shows vascularity related to mass. Degree of hypervascularity was more evident on contrast-enhanced sonogram.

 

Figure 20
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  		Fig. 4F —68-year-old woman with asymptomatic biopsy-proven hepatic angiomyolipoma exhibiting discordance due to lesional fat. Portal venous phase CT image shows similar difficulty to contrast-enhanced sonogram in determining washout.

 
Unexplained Discordance
Unexplained discordance was seen in four benign lesions: two cases of focal nodular hyperplasia and two cases of adenoma. Washout was seen on either contrast-enhanced sonography or contrast-enhanced CT without similar washout with the other technique. In each diagnosis, one lesion exhibited washout on contrast-enhanced sonography but not on contrast-enhanced CT. The other exhibited washout on contrast-enhanced CT but not on contrast-enhanced sonography. In an additional three hepatomas, washout was visualized on CT, and either delayed or no washout was present on contrast-enhanced sonography. Discordance in all of these examples was unexplained.


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Strong agreement has been shown between contrast-enhanced sonography and contrast-enhanced CT both for liver mass diagnosis and for observed patterns of enhancement [2–4]. Although relatively rarely encountered, cases of discordance between contrast enhancement of liver lesions on sonography and contrast enhancement on CT and MRI have not been explained in a systematic way. We propose explanations for the categories observed in this study.

Contrast Agent Diffusion
Microbubbles for sonography are purely intravascular [1]. Regardless of when the liver and liver lesion are visualized, the microbubble signal is a reflection of the relative volume of blood within the field of view. Small-molecule contrast agents for CT and MRI, in comparison, diffuse through the vascular endothelium into the tumor interstitium, beginning the so-called interstitial phase [5, 6]. This difference in contrast agent behavior may always be present but can be particularly evident in malignant lesions. The vascular endothelium of angiogenic tumors is well known to be hyperpermeable [7], allowing CT and MRI contrast agents to diffuse more rapidly into the tumor interstitium so that washout is masked by interstitial contrast medium in the portal venous phase. Washout of contrast medium in the portal venous phase of contrast-enhanced sonography has a high correlation with the presence of malignant lesions [8, 9]. In benign lesions, this difference in contrast agent diffusion is rarely the source of discordance.

Timing
The explanation for discordance in the arterial phase relates to the differing mechanisms and speeds of image acquisition with the three techniques. On sonography of the liver, a single plane is continuously acquired at approximately 10–20 images per second, making sonography a real-time dynamic study. Differences in enhancement are recorded regardless of the rate at which they occur. In the arterial phase of helical CT and volumetric MRI acquisition, a single slice shows the lesion. Analysis of our cases of metastases showed that at the time at which the contrast-enhanced CT arterial phase images were acquired, contrast-enhanced sonography also showed a mass with less enhancement than the adjacent liver. The peak of arterial enhancement, however, had already passed. Contrast-enhanced sonography shows that metastatic lesions typically exhibit a very early and narrow time window of arterial hypervascularity with very rapid washout. This window often closes 20–30 seconds into the arterial phase [10]. Arterial phase images on CT or MRI, by comparison, are snapshots in time, often recorded when the contrast agent has already washed out of a metastatic deposit, thereby showing a hypovascular mass relative to the liver. Were the CT scan to be obtained precisely at the peak of the arterial phase within the lesion, no such discordance would be seen. These timing differences are infrequently encountered in malignant lesions other than metastatic lesions.

Discordance Due to Fat
Fat presents a particular challenge to contrast-enhanced sonography because contrast-specific imaging methods designed to suppress tissue echo may fail in the presence of echogenic fat. On sonography, fat tends to increase the echogenicity of masses containing fat and of liver affected by steatosis [11]. A highly echogenic mass on baseline sonography can be incompletely suppressed at the initiation of the injection sequence when low-mechanical-index contrast-specific imaging is selected. The enhancement caused by the contrast agent is added to the baseline echogenicity and can produce an erroneous interpretation of the degree of enhancement of either the liver or the lesion. Thus contrast-enhanced sonography can show a higher relative echo level of the lesion through all phases of enhancement. This phenomenon makes sonography discordant with CT and MRI, both of which may depict a lower signal intensity from the mass compared with liver tissue. Discordance due to fat, therefore, is evident in all phases of enhancement and on baseline unenhanced scans.

The mechanism by which fatty liver causes difficulty for contrast-specific sonography arises partly because of reliance on the second harmonic component of the microbubble echo. Pulse inversion imaging, the most popular method currently used, is sensitive to the second harmonic from both bubbles and tissue. The tissue harmonic has its origin in nonlinear propagation of the sound and is more apparent at high transmittal amplitudes. The bubble harmonic, on the other hand, comes from nonlinear oscillation of bubbles and is strong at very low transmittal amplitudes (mechanical index). Thus for low-mechanical-index pulse-inversion imaging of normal tissue, both the fundamental and the second harmonic from the background tissue are generally suppressed, and the bubbles give a strong echo.

Fatty tissue has acoustic properties different from those of normal tissue. Fat is highly echogenic and substantially increases nonlinear propagation at the same amplitude compared with normal tissue [12]. Thus pulse inversion scanning at a low mechanical index, which can suppress the parenchymal echo from a normal liver, may not do so for a fatty liver, which produces a strong tissue harmonic. This phenomenon causes the contrast-enhanced examination to fail, because bubble-to-tissue contrast is fatally decreased. Therefore, if the findings on gray-scale sonography before contrast administration suggest the liver is fatty and large, it might be preferable to perform contrast-enhanced MRI, which is highly sensitive to the presence of fat and has higher diagnostic specificity than sonography [13]. CT, although sensitive to the presence of fat, suffers from obscuration of small metastatic lesions and other hypodense masses because the attenuation of surrounding liver may be similar to that of the metastatic deposit. Developments in contrast-specific sonography that decrease sensitivity to the tissue harmonic [14] may effectively suppress fat.

Some instances of discordance between contrast-enhanced sonography and contrast-enhanced CT and MRI remain unexplained. These cases are predominantly related to washout on one technique without comparable washout on the other technique. Blood volume and other liver hemodynamic factors, such as shunting, may contribute. Additional research is needed to investigate these cases of discordance. There also exists variation between lesions with the same histologic diagnosis on all techniques—the so-called atypical case.

Conclusion
Infrequent discordance between the contrast enhancement patterns of sonography and those of CT and MRI occur in at least three patterns that can be explained on the basis of physical principles of contrast imaging. Knowledge of these appearances and the explanations should decrease errors in interpretation and improve management without performance of unnecessary biopsies. The real-time capability of contrast-enhanced sonography and the intravascular properties of sonographic contrast agents are the strengths of contrast-enhanced sonography. Fat poses challenges to imaging and interpretation with all techniques. In rare cases, discordance of contrast enhancement in the portal venous phase of all techniques remains unexplained.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Burns PN. Contrast ultrasound technology. In: Solbiati L, Martegani A, Leen E, Correas JM, Burns PN, Becker D, eds. Contrast-enhanced ultrasound of liver diseases. Milan, Italy: Springer,2002 : 1-19
  2. Passamonti M, Vercelli A, Azzaretti A, Rodolico G, Calliada F. Characterization of focal liver lesions with a new ultrasound contrast agent using continuous low acoustic power imaging: comparison with contrast enhanced spiral CT. Radiol Med (Torino) 2005;109 : 358-369[Medline]
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  5. Donahue KM, Burstein D, Manning WJ, Gray ML. Studies of Gd-DTPA relaxivity and proton exchange rates in tissue. Magn Reson Med 1994; 32:66 -76[Medline]
  6. Gardeur D, Lautrou J, Millard JC, Berger N, Metzger J. Pharmacokinetics of contrast media: experimental results in dog and man with CT implications. J Comput Assist Tomogr1980; 4:178 -185[Medline]
  7. Jain RK. Vascular and interstitial physiology of tumours: role in cancer detection and treatment. In: Bicknell R, Lewis CE, Ferrara N, eds. Tumour angiogenesis. Oxford, UK: Oxford University Press, 1997: 45-59
  8. Blomley MJ, Sidhu PS, Cosgrove DO, et al. Do different types of liver lesions differ in their uptake of the microbubble contrast agent SH U 508A in the late liver phase? early experience. Radiology 2001; 3:661 -667
  9. Wilson SR, Burns PN. An algorithm for the diagnosis of focal liver masses using microbubble contrast-enhanced pulse-inversion sonography. AJR 2006; 186:1401 -1412[Abstract/Free Full Text]
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  11. Behan M, Kazam E. The echographic characteristics of fatty tissues and tumors. Radiology 1978;1 : 143-151
  12. Hamilton MF, Blackstock DT. Nonlinear acoustics. San Diego, CA: Academic Press,1998
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