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Value of Contrast-Enhanced Ultrasonography in Assessing the Vascularity of Liver Metastases

Comparison With Contrast-Enhanced Computed Tomography
Yan-Ling Zheng, MD, Xiao-Yu Yin, MD, PhD, Xiao-Yan Xie, MD, PhD, Hui-Xiong Xu, MD, PhD, Zuo-Feng Xu, MD, PhD, Guang-Jian Liu, MD, PhD, Jin-Yu Liang, MD, Ming-De Lu, MD, PhD
Objective. The purpose of this study was to compare the capability of contrast-enhanced ultrasonography (CEUS) and contrast-enhanced computed tomography (CECT) in evaluating the vascularity of liver metastases. Methods. Both CEUS and CECT examinations were performed on 70 patients with liver metastases, which were from colon carcinoma in 31, rectal carcinoma in 17, pancreatic carcinoma in 5, and others in 17. In patients with multiple lesions, the most easily observed lesion was selected as the target lesion for evaluation of vascularity. Results. Peak enhancement of the target lesion during the arterial phase was characterized as hyperenhancement, isoenhancement, hypoenhancement, and nonenhancement in 61 (87.1%), 6 (8.6%), 3 (4.3%), and 0 (0%) patients on CEUS, respectively, and in 52 (74.3%), 8 (11.4%), 8 (11.4%), and 2 (2.9%) on CECT. Contrast-enhanced ultrasonography showed more lesions with hyperenhancement than CECT (P < .01). The enhancement pattern during the arterial phase was homogeneous, inhomogeneous, and rimlike in 30 (42.9%), 16 (22.9%), and 24 (34.2%) patients on CEUS and in 13 (18.6%), 8 (11.4%), and 49 (70%) on CECT. Contrast-enhanced ultrasonography revealed more lesions with homogeneous enhancement than CECT (P < .01). Contrast-enhanced ultrasonography showed dysmorphic vessels in 33 patients (47.1%) during the arterial phase, whereas CECT showed dysmorphic vessels in 27 (38.6%; P < .01). Contrast-enhanced ultrasonography showed hypervascular lesions in 58.6% of patients, whereas CECT showed hypervascular lesions in 12.9% (P < .01). Conclusions. Contrast-enhanced ultrasonography was superior to CECT in assessing the vascularity of liver metastases. Key words: contrastenhanced computed tomography; contrast-enhanced ultrasonography; liver metastases; vascularity.
Abbreviations CECT, contrast-enhanced computed tomography; CEUS, contrast-enhanced ultrasonography; CT, computed tomography; MRI, magnetic resonance imaging; TACE, transcatheter arterial embolization Received February 24, 2010, from the Departments of Medical Ultrasonics (Y.-L.Z., X.-Y.X., H.-X.X., Z.-F.X., G.-J.L., J.-Y.L., M.-D.L.) and Hepatobiliary Surgery (X.-Y.Y., M.-D.L.), First Affiliated Hospital, and Institute of Diagnostic and Interventional Ultrasound (Y.-L.Z., X.-Y.X., H.-X.X., Z.-F.X., G.-J.L., J.-Y.L., M.-D.L.), Sun YatSen University, Guangzhou, China. Revision requested March 16, 2010. Revised manuscript accepted for publication May 17, 2010. Address correspondence to Xiao-Yu Yin, MD, PhD, Department of Hepatobiliary Surgery, First Affiliated Hospital, Sun Yat-Sen University, 510080 Guangzhou, Guangdong, China. E-mail: yinxy_pitt@yahoo.com
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ssessment of the vascularity of liver malignancies is of clinical importance because it is one of the major factors affecting therapeutic outcomes, including systemic chemotherapy and transcatheter arterial embolization (TACE). Braga et al1 used magnetic resonance imaging (MRI) to analyze the vascularity of liver metastases in 16 patients with breast cancer who underwent systemic chemotherapy and found that patients with hypervascular liver lesions were 20.5 times more likely to have disease progression than patients without hypervascular metastases. Taniai et al2 adopted contrast-enhanced computed tomography (CECT) to evaluate the vascularity of liver metastases in 45 patients with colorectal cancer who were treated with

2010 by the American Institute of Ultrasound in Medicine J Ultrasound Med 2010; 29:14031410 0278-4297/10/$3.50

Contrast-Enhanced Ultrasonography of Liver Metastasis Vascularity

TACE and found that TACE was effective in only hypervascular colorectal liver metastases. Alba et al3 used TACE as neoadjuvant treatment for 56 patients with hepatocellular carcinoma who had 131 nodules and were waiting for orthotopic liver transplantation. Subsequent pathologic examination confirmed that the antitumoral effect of TACE was more remarkable in hypervascular lesions compared with hypovascular ones. Currently, the vascularity of liver lesions is mainly assessed by CECT, MRI, and digital subtraction angiography. Of them, CECT and MRI have been most commonly used because of their noninvasiveness and convenience. However, they are not real-time imaging modalities and easily miss the early arterial phase, particularly in liver metastases in which arterial perfusion is usually shortlasting.4 Digital subtraction angiography has been used for arterial angiography and can clearly illustrate the early arterial perfusion of lesions, but it has disadvantages of invasiveness and radiation exposure. On the other hand, both CECT and digital subtraction angiography use iodinated contrast agents, which might be associated with severe adverse reactions in some patients.5 Furthermore, they are contraindicated in patients with renal insufficiency because the iodinated contrast agents are excreted by the kidney. Contrast-enhanced ultrasonography (CEUS) is a recently developed technique that can depict the blood perfusion of liver lesions in a real-time manner.4,6 Because of its advantages of noninvasiveness, real-time scanning, and safety,7 enthusiasm about CEUS for evaluating the vascularity of liver lesions has grown rapidly. The aim of this study was to compare the capability of CEUS and CECT in assessing the vascularity of liver metastases.

The diagnosis of liver metastases was established by histopathologic examination in 23 patients and 2 contrast-enhanced imaging studies (CEUS, CECT, or MRI) in 47 patients. Tumor sizes were 3.2 1.8 cm (range, 0.98.2 cm). Twenty patients had single lesions, and the remaining 50 had multiple lesions. The primary malignancies consisted of colon carcinoma in 31, rectal carcinoma in 17, pancreatic carcinoma in 5, gastric carcinoma in 3, pulmonary carcinoma in 3, esophageal adenocarcinoma in 2, gallbladder carcinoma in 2, breast carcinoma in 2, bladder carcinoma in 1, uterine cervical cancer in 1, renal carcinoma in 1, thyroid carcinoma in 1, and ileal leiomyosarcoma in 1. Informed consent was obtained from each patient. The study was approved by the Ethics Committee of the hospital. Contrast-Enhanced Ultrasonographic Technique and Image Analysis The contrast agent used for CEUS was SonoVue (Bracco SpA, Milan, Italy), a sulfur hexafluoride (SF6)-filled microbubble agent that is stabilized by phospholipids. Ultrasonographic examinations were performed with an Acuson Sequoia 512 scanner (Siemens Medical Solutions, Mountain View, CA), which incorporated Cadence contrast pulse sequencing software and a 4V1 vector transducer with a frequency range of 1 to 4 MHz. Contrast-specific contrast harmonic imaging software was installed in the system. A lowmechanical index real-time contrast-specific CEUS mode was used in the examination, and the mechanical index value indicated on the screen was between 0.1 and 0.2. First, the whole liver was thoroughly scanned using conventional gray scale ultrasonography, and the target lesion was determined. In patients with multiple lesions, the most easily observed lesion was selected as the target lesion for evaluation of vascularity. Then a bolus of 2.4 mL of SonoVue was injected via the antecubital vein, followed by 5 mL of normal saline. The contrast program was initiated at the same time. The target lesion was observed continuously during the arterial phase (830 seconds after SonoVue injection). The rest of the liver was scanned to find other lesions during the portal phase (31120 seconds) and late phase (121360 seconds).810
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Materials and Methods

Patients From March 2004 to September 2008, CEUS examinations were performed in 284 consecutive patients with liver metastases in our hospital. Among them, 70 patients had CECT examinations in our hospital simultaneously. Seventy patients who had both CEUS and CECT examinations were included in the study. There were 39 male and 31 female patients with a mean age SD of 56.6 12.1 years (range, 3275 years).
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The entire process was recorded and stored on the hard disk. The ultrasonographic examinations were performed by physicians with at least 4 years of experience in CEUS. Digital cine clips were analyzed offline in consensus by 2 physicians with at least 4 years of experience in CEUS. The peak enhancement level of the target lesion during the arterial phase was evaluated and classified as nonenhancement, hypoenhancement, isoenhancement, and hyperenhancement by comparison with the adjacent liver tissue.9 The enhancement pattern was categorized as homogeneous (uniform enhancement of the entire lesion), inhomogeneous (different levels of enhancement in different parts of the lesion), and rimlike (a continuous ring of enhancement seen at the periphery of the nodule). Vessels that were situated outside the lesions and showed rapid flow of microbubbles running into the lesions during the early arterial phase were defined as dysmorphic vessels. The time to the peak hyperenhancement level was analyzed on the clips. According to the peak enhancement level, enhancement pattern, and enhancement area during the arterial phase, the lesions were classified as having hypervascularity, isovascularity, and hypovascularity. Tumors meeting one of the following criteria were considered to have hypervascularity: (1) homogeneous hyperenhancement and (2) an enhancement area covering half or more of the lesion (either ringlike or inhomogeneous). Isovascularity was defined as homogeneous isoenhancement. Tumors meeting one of the following criteria were considered to have hypovascularity: (1) hypoenhancement, (2) nonenhancement, and (3) an enhancement area covering less than half of the lesion (either ringlike or inhomogeneous). Contrast-Enhanced Computed Tomographic Technique and Image Analysis The contrast agent used for CECT was Ultravist (Schering AG, Berlin, Germany), which contains iopromide. It was administered via the antecubital vein by power injection at a rate of 3 mL/s (singleslice helical computed tomography [CT]) or 4 mL/s (64-slice helical CT) at a dose of 1.5 mL/kg. Contrast-enhanced CT examinations were performed with an Xpress SX single-slice helical CT scanner (Toshiba Medical Systems Co, Ltd,
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Tokyo, Japan) or an Aquilion 64-slice helical CT scanner (Toshiba Medical Systems) within 14 days before or after the CEUS examinations. No treatment was given during the interval between the CEUS and CECT examinations. The scanning parameters were 5-mm collimation, 120 kV, and 250 mAs for single-slice helical CT and 0.5 64mm collimation, 120 kV, and 150 to 200 mAs for 64-slice helical CT. The standard dual-phase scan procedure was used. After unenhanced helical sequence scanning, the contrast agent was administered. The arterial phase sequence was obtained 25 to 30 seconds after injection, followed by a portal venous phase sequence at 50 to 60 seconds. Digital cine clips were analyzed offline in consensus by 2 physicians with at least 5 years of experience in CECT. Contrast-enhanced CT analysis was done on the same target lesions as CEUS. By comparison with the adjacent liver tissue, the peak enhancement level of the target lesion was classified as nonenhancement, hypoenhancement, isoenhancement, and hyperenhancement during the arterial phase. Similar to that for CEUS, the enhancement pattern on CECT was categorized as homogeneous, inhomogeneous, and rimlike.11 Vessels showing blood flow penetrating into the lesion during the arterial phase on CECT were considered dysmorphic vessels. The definitions of hypervascularity, isovascularity, and hypovascularity on CECT were the same as those on CEUS. Statistical Analysis The results are given as mean SD. The SPSS version 10.0 software package (SPSS Inc, Chicago, IL) was used for statistical analysis. A 2 test was used to compare the enhancement level, pattern, dysmorphic vessels, and vascularity between CEUS and CECT. The peak enhancement time was compared between the two groups using an independent Student t test. Two-tailed P < .05 was considered statistically significant.

Results
With respect to the enhancement level of the target lesions, there were 61 patients (87.1%) with hyperenhancement, 6 (8.6%) with isoenhancement, 3 (4.3%) with hypoenhancement, and
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Table 1. Peak Enhancement Level During the Arterial Phase on CEUS and CECT
CEUS Hyper Iso CECT Hypo Non Total

Hyper Iso Hypo Non Total

49 3 0 0 52

6 2 0 0 8

6 0 2 0 8

0 1 1 0 2

61 6 3 0 70

0 (0%) with nonenhancement on CEUS and 52 (74.3%) with hyperenhancement, 8 (11.4%) with isoenhancement, 8 (11.4%) with hypoenhancement, and 2 (2.9%) with nonenhancement on CECT. Contrast-enhanced ultrasonography

showed more lesions with hyperenhancement than CECT (P < .01; Table 1). As illustrated in Figure 1, the liver metastases appeared hyperenhanced during the arterial phase on CEUS but isoenhanced on CECT. With respect to the enhancement pattern, homogeneous, inhomogeneous, and rimlike enhancement were seen in 30 (42.9%), 16 (22.9%), and 24 (34.2%) patients, respectively, on CEUS and in 13 (18.6%), 8 (11.4%), and 49 (70.0%) on CECT. CEUS revealed more lesions with homogeneous enhancement (P < .01; Table 2). As illustrated in Figures 2 and 3, the liver metastases appeared to have homogeneous hyperenhancement during the arterial phase on CEUS but rimlike enhancement on CECT.

Figure 1. Liver metastasis with a diameter of 1.9 cm from rectal carcinoma in a 47-year-old woman. A and B, Contrast-enhanced ultrasonography showed that the lesion was homogeneously hyperenhanced during the arterial phase (A, arrow) and homogeneously hypoenhanced during the portal phase (B, arrow). C and D, Contrast-enhanced CT showed that the lesion was homogeneously isoenhanced during the arterial phase (C, arrow) and homogeneously hypoenhanced during the portal phase (D, arrow).

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Table 2. Contrast Enhancement Pattern During the Arterial Phase on CEUS and CECT
CEUS Homogeneous CECT Inhomogeneous Rimlike Total

Homogeneous Inhomogeneous Rimlike Total

10 2 1 13

6 1 1 8

14 13 22 49

30 16 24 70

Contrast-enhanced ultrasonography showed dysmorphic vessels in 33 patients (47.1%), whereas CECT showed dysmorphic vessels in 27 (38.6%). Contrast-enhanced ultrasonography showed dysmorphic vessels in more patients with liver metastases than CECT (P < .01; Table 3 and Figures 3 and 4).

According to the definitions of hypervascularity, isovascularity, and hypovascularity, CEUS showed that 41 of 70 patients (58.6%) had hypervascular lesions, 4 (5.7%) had isovascular lesions, and the remaining 25 (35.7%) had hypovascular lesions. By comparison, CECT showed that only 9 patients (12.9%) had hypervascular lesions, 2

Figure 2. Liver metastasis with a diameter of 2.0 cm from rectal carcinoma in a 51-year-old man. A and B, Contrast-enhanced ultrasonography showed that the lesion was homogeneously hyperenhanced during the arterial phase (A, solid arrows), with a transient hepatic attenuation difference in the adjacent parenchyma (A, open arrow), and homogeneously hypoenhanced during the portal phase (B, arrow). C and D, Contrast-enhanced CT showed that the lesion had rimlike enhancement during the arterial phase (C, solid arrow), with an adjacent transient hepatic attenuation difference (C, open arrow), and was homogeneously hypoenhanced during the portal phase (D, arrow).

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(2.9%) had isovascular lesions, and 59 (84.3%) had hypovascular lesions (P < .01). In 9 hypervascular lesions on CECT, 7 (77.8%) of them were shown to be hypervascular on CEUS, and the remaining 2 (22.2%) were isovascular. In 59 hypovascular lesions on CECT, 32 (54.2%) were shown to be hypervascular on CEUS. On the other hand, 32 of 41 hypervascular lesions (78.0%) on CEUS were shown to be hypovascular on CECT. These findings illustrate that CEUS was more sensitive than CECT for detecting the vascularity of liver metastases. Of the 32 lesions that were hypervascular on CEUS but hypovascular on CECT, the time to peak hyperenhancement on CEUS ranged from 9 to 19 seconds (mean, 15.8 2.5 seconds) after injection of the contrast agent. In 7 lesions that

were hypervascular on both CEUS and CECT, the time to peak hyperenhancement on CEUS ranged from 18 to 30 seconds (23.1 4.2 seconds; P < .01), suggesting that when the time to peak enhancement of a lesion was too short, CECT was likely to underassess its vascularity.

Discussion
The vascularity status of liver metastases is one of the major factors influencing therapeutic outcomes. Braga et al1 treated 16 patients with liver metastases from breast cancer using systemic chemotherapy and found that patients with hypervascular liver lesions assessed by MRI were 20.5 times more likely to have tumor progression compared with those without hyper-

Figure 3. Multiple liver metastases from colon carcinoma in a 47-year-old man. AC, Contrast-enhanced ultrasonography showed that the target lesion with a diameter of 1.7 cm had dysmorphic vessels during the early arterial phase (A, arrows) and was homogeneously hyperenhanced during the arterial phase (B, arrows) and homogeneously hypoenhanced during the portal phase (C, arrow). D, Contrast-enhanced CT also showed that the target lesion had dysmorphic vessels (arrow), but it had rimlike isoenhancement.

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Table 3. Dysmorphic Vessels of Metastatic Lesions Detected on CEUS and CECT

CEUS Present CECT Absent Total

Present Absent Total

19 8 27

14 29 43

33 37 70

vascular metastases. Another study treated 45 patients with liver metastases from colorectal carcinoma using TACE and showed that it was effective in only hypervascular lesions assessed by CECT.2 Hence, accurate assessment of the vascularity status of liver metastases is of clinical importance. On the basis of CECT and MRI, liver metastases have predominantly been thought to be hypovascular.12 Recently, Murphy-Lavallee et al13 used CEUS to evaluate the vascularity of liver metastases and found that 88% of them were hypervascular during the early arterial phase. However, there is still a lack of studies comparing CEUS and CECT/MRI for assessing the vascularity of liver metastases. In this study, we compared CEUS and CECT for evaluating the vascularity of liver metastases in 70 patients. Contrast-enhanced ultrasonography showed that 43% of the metastatic lesions had homogeneous enhancement, 47% had dysmorphic vessels, and 58.6% were hypervascular. On the contrary, CECT showed homogeneous

enhancement in only 19% and dysmorphic vessels in 39%, and only 12.9% of them were hypervascular. In the 59 hypovascular lesions on CECT, 54.2% of them were shown to be hypervascular on CEUS. On the other hand, 78% of hypervascular lesions on CEUS were shown to be hypovascular on CECT. Among 3 patients with liver metastases from breast and thyroid cancers that were classic potentially hypervascular, CECT showed hypervascular liver lesions in only 2 (1 in breast cancer and 1 in thyroid cancer), whereas CEUS revealed hypervascular lesions in all 3 (data not shown). These results suggest that CEUS is more sensitive and accurate than CECT for depicting the vascularity of liver metastases. These findings might be attributed to the following reasons. First, CEUS is a real-time dynamic scanning modality and can continuously assess the vascularity of a lesion immediately after injection of a contrast agent.14,15 The dose of SonoVue used in CEUS was only 2.4 mL and was administered by bolus injection. Contrast-enhanced ultrasonography would not miss any time of enhancement during the whole arterial phase and hence could accurately assess the vascularity of a lesion. On the contrary, CECT is an instant scanning modality and can assess the vascularity of a lesion only at a certain point in time during the arterial phase. Because the dose of Ultravist used in CECT was 1.5 mL/kg (60100 mL in total) and was administered by power injection at a rate of 3 mL/s (single-slice

Figure 4. Multiple liver metastases from colon carcinoma in a 70-year-old woman. A, In the live compare mode showing CEUS on the left and the baseline image on the right, CEUS showed dysmorphic vessels around the target lesion with a diameter of 7.2 cm (arrow). B, Contrast-enhanced CT showed no dysmorphic vessels around the lesion (arrows).

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helical CT) or 4 mL/s (64-slice helical CT), CECT started to scan after completion of contrast agent injection3,16 and usually missed the early arterial phase (1525 seconds). If the peak enhancement of a lesion falls in this period, CECT is likely to underestimate its vascularity. In our study, of the 32 lesions that were hypervascular on CEUS but hypovascular on CECT, the time to peak hyperenhancement was between 9 and 19 seconds (15.8 2.5 seconds) after injection of the contrast agent. In the 7 lesions that were hypervascular on both CEUS and CECT, the time to peak hyperenhancement was between 18 and 30 seconds (23.1 4.2 seconds). This indicated that when the time to peak enhancement of a lesion was too short, CECT was likely to underassess its vascularity. In summary, our results show that CEUS tends to be superior to CECT in assessing the vascularity of liver metastases. More accurate assessment of the vascularity of liver metastases by CEUS can help select candidates who would gain potential benefits from treatment and predict prognosis. For example, for liver metastases from colorectal carcinoma, TACE is indicated for patients with hypervascular lesions because it is effective for only hypervascular lesions and not hypovascular lesions. Contrast-enhanced CT may neglect some patients who are potential candidates for TACE because it underestimates the vascularity of liver lesions. Comparatively, CEUS can identify more patients suitable for TACE by showing more hypervascular lesions. Admittedly, a largescale clinical trial is still needed to assess the clinical importance of CEUS in assessing the vascularity of liver metastases.

4.

Krix M, Kiessling F, Essig M, et al. Low mechanical index contrast-enhanced ultrasound better reflects high arterial perfusion of liver metastases than arterial phase computed tomography. Invest Radiol 2004; 39:216222. Singh J, Daftary A. Iodinated contrast media and their adverse reactions. J Nucl Med Technol 2008; 36:6974. Bhayana D, Kim TK, Jang HJ, Burns PN, Wilson SR. Hypervascular liver masses on contrast-enhanced ultrasound: the importance of washout. AJR Am J Roentgenol 2010; 194:977983. Schneider M. SonoVue, a new ultrasound contrast agent. Eur Radiol 1999; 9(suppl 3):S347S348. Quaia E, Calliada F, Bertolotto M, et al. Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: diagnostic performance and confidence. Radiology 2004; 232:420430. Albrecht T, Blomley M, Bolondi L, et al; EFSUMB Study Group. Guidelines for the use of contrast agents in ultrasound: January 2004. Ultraschall Med 2004; 25:249256. Xu HX, Liu GJ, Lu MD, et al. Characterization of focal liver lesions using contrast-enhanced sonography with a low mechanical index mode and a sulfur hexafluoride-filled microbubble contrast agent. J Clin Ultrasound 2006; 34: 261272. Nino-Murcia M, Olcott EW, Jeffrey RB Jr, Lamm RL, Beaulieu CF, Jain KA. Focal liver lesions: pattern-based classification scheme for enhancement at arterial phase CT. Radiology 2000; 215:746751. Kanematsu M, Kondo H, Goshima S, et al. Imaging liver metastases: review and update. Eur J Radiol 2006; 58:217 228. Murphy-Lavallee J, Jang HJ, Kim TK, Burns PN, Wilson SR. Are metastases really hypovascular in the arterial phase? The perspective based on contrast-enhanced ultrasonography. J Ultrasound Med 2007; 26:15451556. Dietrich CF. Characterisation of focal liver lesions with contrast enhanced ultrasonography. Eur J Radiol 2004; 51(suppl):S9S17. von Herbay A, Vogt C, Willers R, Hussinger D. Real-time imaging with the sonographic contrast agent SonoVue: differentiation between benign and malignant hepatic lesions. J Ultrasound Med 2004; 23:15571568. Park Y, Choi D, Lim HK, et al. Growth rate of new hepatocellular carcinoma after percutaneous radiofrequency ablation: evaluation with multiphase CT. AJR Am J Roentgenol 2008; 191:215220.

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