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16
a
C. F. Dietrich et al.
• Signal separation between microbubbles and tissue, based
on the assumption that the latter behaves in a perfectly
linear fashion (i.e., the tissue responses follow the transmitted waveform exactly).
A higher MI results in a better penetration but also
increases destruction of the microbubbles. The contrast agent
dose balances the contrast enhancement intensity. In the
early phase of CEUS, it prevents over enhancement of structures with shadowing. In the contrast enhancement duration,
a sufcient contrast agent may concentrate in the late phase.
In practice, this perfectly linear model is not completely
true since the transmitted waves become distorted as they are
conducted through any medium and this produces harmonics, which are the basis for harmonic imaging widely used in
B-mode scanning. It should be pointed out that microbubble
harmonics are generated in a different way, by the fact that
the microbubbles resist compression more strongly than
expansion, so their response to a symmetrical ultrasound
pulse is asymmetrical, generating harmonics.
2.2.2 Image Depth Penetration
neareld [6]. Most importantly bubble destruction (“the
circle of disaster”) should be avoided. Regarding commonly observed artifacts we refer to the respective paragraph below [5].
2.2.3 Focus
Usually the focus should be positioned at the distal border of
the target lesion but this might vary in some scanners. For
detection, a deeper location of the focus (at least two-thirds
of the screen) is recommended (Fig.2.1).
2.2.4 Gain (Received Signal Amplication)
The gain should be usually set at or very slightly above the
noise oor so that before microbubbles arrive, the image is
dark. If the gain is set too low, sensitivity is too low and weak
microbubble signals are not detected. If the gain is set too
high signal saturation occurs possibly with acoustic shadowing (Fig.2.2).
The image depth penetration is determined by many factors
2.2.5 Background Signal (Noise)
including the manufacturer and transducer technology,
transducer frequency, acoustic power (mechanical index),
focus and other technology-dependent factors, and nally
by the patient’s condition. Limited depth penetration can be
overcome by lowering the transmit frequency with the disadvantage of lower spatial resolution, eventually resulting
in suboptimal imaging of small supercially located
lesions. Increasing the MI may improve penetration but at
the expense of microbubble destruction, especially in the
A dual-image display format is often recommended since the
nonlinear image is almost black making it difcult to focus
on the lesion of interest, which is especially necessary when
examining small and difcult to detect focal liver lesions. In
the dual-image display, a conventional B mode fundamental
image and a bubble-only contrast image are displayed sideby- side [6]. In contrast, it is also possible to overlay the contrast and B mode image, which doubles the screen size. For
b
Fig. 2.1 Focal zone set during liver contrast enhanced ultrasound
(CEUS). Normal CEUS of the liver showed an appropriately placed
focal zone at the bottom of the image (a). Poor quality CEUS of a nor-
mal liver showed focal zone set in the near eld (b), resulting in signicant loss of contrast signal in the far eld
b
a
2 Contrast Enhanced Ultrasound: How toPerform It inLiver Tumors?
c
17
Fig. 2.2 Gain adjustments during liver contrast enhanced ultrasound (CEUS). CEUS with appropriately adjusted gain demonstrates normal
enhancement of liver parenchyma (a). While too high (b) or too low (c) set of gain was not suitable for appropriate imaging
quantitative studies, the dual-image display is advantageous
2.2.7 Frame Rate
since it is important to keep the transducer at the same place
and avoid motion. It should be mentioned that the quality of
the B mode image in dual-image displays is inferior to that
obtained in non-contrast mode with the same settings [6].
For focal liver characterization with adequate visualization
and recording the frame rate should be adjusted ≥10Hz. Too
high frame rates can augment bubble destruction and too low
a frame rate does not allow real-time imaging [6] (Table2.1).
2.2.6 Dynamic Range
2.3 CEUS oftheLiver, Examination
The dynamic range is the range of signal intensities to be
displayed. It should be set to optimize the enhancement
pattern. A small dynamic range will decrease the signal levels (“grey levels”) in the image and increases visual contrast but can limit the differentiation between different
degrees of enhancement. A wide dynamic range increases
the number of “greys,” allowing for better differentiation
between different degrees of enhancement [6]. A large
dynamic range allows to improve identication of the
increased rim signal in patients with highly vascularized
metastatic lesions. A narrow dynamic range is preferred for
visualization of FLL with low perfusion. A wide dynamic
range should be used in perfusion quantication studies to
avoid signal saturation [6].
The pre-contrast examination preparations are important,
which include the identication of the target focal liver
lesion, the identication of the best position of the patient,
and the optimal scan plane to minimize out-of-plane motion
from respiration, usually longitudinal along the axis of the
respiratory movements [6].
larger) should be inserted in the antecubital vein of left arm,
while avoiding interaction of the injector with the right-sided
examiner (Fig. 2.3). Some important inuencing factors
should be avoided, e.g., avoid the side of the breast (or axillary) surgery to minimize the risk of worsening lymphedema.
Technique
For injection of contrast agents, the cannula (20 gauge or
18
a
Table 2.1 Ultrasound contrast agents in clinical use
Brand Shell material Gas core
Denity Lipid Octauoropropane 1.1–3.3 12.0 Yes Left ventricular opacication
Optison Sonicated albumin Octauoropropane 3.0–4.5 0.5–0.8 Yes Left ventricular opacication
SonoVue
(Lumason)
Sonazoid Sucrose Peruorobutane 2.1 1.2 Yes Characterization of focal liver
Lipid Sulfur hexauoride 1.5–2.5 0.15–0.56 Yes Left ventricular opacication
Mean
diameter (μm)
Concentration as
prepared (×1 × 109)/mL
(C)FDA
approved FDA approved indications
Characterization of focal liver
lesions
lesions
C. F. Dietrich et al.
b
c
d
Fig. 2.3 Preparation for liver contrast enhanced ultrasound. Choose
the most suitable contrast agent, SonoVue (a) or Sonazoid (b). Preparing
for the contrast agents according to manual indications (c–e). The can-
nula (20 gauge or larger) should be inserted in the left arm, preferably
the antecubital vein, to avoid interaction of the injector with the rightsided examiner (f)
e
2 Contrast Enhanced Ultrasound: How toPerform It inLiver Tumors?
19
f
Fig. 2.3 (continued)
Central line and port systems can be used as long as there is
no lter requiring a high injection pressure, but be aware of
a possible shorten contrast arrival time [6]. The catheter
should be removed after the exclusion of any pseudoanaphylactic reaction. When multiple injections are anticipated, a
three-way stopcock may be valuable and facilitates sequential administration of the contrast agent and then the saline
ush, without removal of either syringe. The author almost
never uses a three-way stopcock.
The timer should be started at the time of the beginning
of the UCA injection. The application via a central venous
line with a much shorter arrival time is a good reason for
this [6].
The injection bolus for SonoVue™ is given at about
1–2ml/s to avoid high pressure with the risk of microbubble
destruction. Immediately after injecting the contrast agent, a
5–10ml saline bolus should be given to ush the line with
higher pressure >2ml/s. The contrast dose depends on the
Fig. 2.4 Doppler blooming artifact. Following contrast administration,
there is a marked increase in Doppler signal throughout the liver with
color pixels displaying well beyond the expected vessel margins, indicating blooming artifact
quality of the machine and the machine setting. It is
suggested to use lower dosages between 0.4 and 4.8ml in
small pediatric patients. Artifacts might appear in the early
Repeated injection is advised under the following circum-
stances [6]:
phases of enhancement with a too high contrast agent dose,
including acoustic shadowing, over-enhancement of small
structures, and signal saturation (Fig.2.4). Meanwhile, too
low a dose might cause the concentration of microbubbles
to be subdiagnostic in the late phase, mimicking the detection of wash-out [6].
• There are additional FLL, which require
characterization.
• The initial injection failed and did not provide the full
answer to the detection and/or characterization of a FLL
to allow for assessment of missing information.
20
C. F. Dietrich et al.
• A wash-out region may be identied on sweeps of the
liver in either the PVP or the LP to allow arterial enhancement characterization.
2.4 Improved Detection ofFocal Liver
Lesions
Conventional ultrasound is the most commonly used imaging modality for focal liver lesions, but is less sensitive in the
detection of FLL while comparing with CECT, CEMRI, or
intraoperative US. With the application of CEUS, it has dramatically increased detection rate of FLL before operation,
especially in liver metastases ≤10mm [7–18].
2.5 Characterization ofFocal Liver
Lesions
The contrast features of focal liver lesion (FLL) should be
described in terms of the enhancement degree and enhancement phase. It is important to know in advance if the liver
is normal or diseased (e.g., liver cirrhosis, brosis, or steatosis). This may affect the contrast enhancement features
of the FLL and its surrounding liver parenchyma.
Enhancement including isoenhancing, hyperenhancing,
and hypoenhancing, which refers to the progressive intensity of the signal relative in FLL to the adjacent parenchyma. “Wash-out” is dened by the reduction in
enhancement degree which follows peak enhancement.
Sustained enhancement refers to the continuation of the
iso- or hyperenhancement in the FLL relative to the adjacent parenchyma over time. Non- enhancing refers to the
complete absence of enhancement [6].
The timing (early versus late onset, fast versus slow),
degree (complete, incomplete), and pattern should be
described in comparison to the surrounding “normal” parenchyma. The combined evaluation of the arterial contrast
enhancement and portal venous and late wash-out of a lesion
compared to the surrounding healthy liver parenchyma allows
characterization of a FLL either as non-hepatic tissue (e.g.,
malignant, inammatory, or brotic) if wash-out is present or
as benign if iso- or hyperenhancement can be observed in
comparison to the surrounding liver parenchyma.
In addition, analyzing the arterial vessel architecture in
the early arterial wash-in phase allows further characterization, especially in benign focal liver lesions as hemangioma
with peripheral nodular contrast enhancement and centripetal ll in [19] or as focal nodular hyperplasia with typical
vascularity [20]. The vascular pattern of hepatocellular adenoma is more complex [21]. The characteristics are also
valid for pediatric patients [22, 23].
The combined evaluation of the above diagnostic features
makes it possible to characterize FLL in patients with liver
cirrhosis as typical for HCC according to the Liver Imaging
Reporting and Data System (LI-RADS) [24, 25].
2.6 Artifacts
Knowledge of the basic physical and technical principles of
ultrasound is needed to understand sonographic images and
ndings and to be able to evaluate the possibilities and limitations of the method. Conventional and CEUS imaging are
susceptible to multiple artifacts (imaging errors) since the
properties assumed to be constant, such as straight-line
sound propagation, attenuation (penetration), sound speed,
acoustic eld characteristics (the narrower the acoustic eld,
the better the suppression of side lobes not corresponding to
wanted signals), acoustic attenuation, damping (due to
reection, absorption, refraction, scatter, and interference)
(Fig. 2.5), and other factors, often deviate from the actual
properties of the sound beam. Knowledge of such artifacts
helps to avoid errors.
The visualization of the contrast agent signals is based on
an interaction between the emitted ultrasound wave and the
microbubbles, which depends on the equipment settings
(acoustic power, image rate, focal zone, etc.). Wrong equipment settings are often the reason for CEUS artifacts that can
result in uncertain diagnoses or even misdiagnoses in extreme
cases.
Perhaps the most important CEUS artifact is bubble
destruction (Fig. 2.6). The MI plays a crucial role here. It
balances the signal intensity and penetration on the one hand
and the stability of the microbubbles on the other hand. The
CEUS “circle of disaster” is characterized by the following
criteria: microbubble destruction → increase in contrast
agent dose → attenuation (shadowing) → higher mechanical
index → additional microbubble destruction. The secret is to
nd a good balance between the contrast agent dose and the
equipment- specic settings.
Pseudoenhancement arises from nonlinear artifacts
occurring in FLL that appear echogenic on conventional
B mode ultrasound and eventually deep in location
(Fig. 2.7). The presence of oscillating microbubbles in
vascularized tissue between the transducer and the object
of interest may create nonlinear echoes that can give the
appearance of enhancement of a deep lesion relative to
2 Contrast Enhanced Ultrasound: How toPerform It inLiver Tumors?
21
Fig. 2.5 Mirror Image Artifact. Contrast enhanced ultrasound (CEUS)
of the liver showed a mass in the posterior right lobe with peripheral
hyperenhancement adjacent to the inferior vena cava (IVC). A mirror
image of the lesion and IVC was opposite the interface with the diaphragm and lung base
Fig. 2.6 Near eld bubble burn-off artifact. A horizontal stripe of low signal in the near eld due to inhomogeneous microbubble destruction
(bubble burn-off)
22
C. F. Dietrich et al.
Fig. 2.7 Contrast ultrasound enhancement (CEUS) of a hepatocellular
carcinoma lesion immediately after transarterial chemotherapy and
radiofrequency ablation. CEUS prior to contrast administration showed
background tissue. This pseudoenhancement typically
occurs in the late portal venous phase and progresses over
time in distinction to real enhancement, which always initiates within the arterial phase [26]. This nonlinear propagation of the ultrasound beam increases with bubble
concentration.
2.6.1 Long Liver Enhancement
Prolonged innocuous liver enhancement has been very rarely
observed over the past decade after the bolus injection of
microbubble contrast agents. It appears as a heterogeneous
enhancement in the liver most often observed during the performance of the CEUS examination and often around 2min
and lasting up to 5h after contrast injection on both B-mode
and contrast-specic modes (Figs. 2.8 and 2.9). It is not
destroyed by sonication at high MI. The enhanced signals
can also be observed in the portal and superior mesenteric
veins, though not in the systemic circulation. It is very simi-
the lipiodol deposition inside the lesion devoid of signal with a few
echogenic foci
Fig. 2.8 Prolonged heterogeneous liver enhancement. B mode ultrasound through the liver following contrast administration (SonoVue)
showed patchy, heterogenous areas of increased echogenicity. This
appearance may last for several hours. However, it is likely not clinically signicant and should not be confused for pathology
2 Contrast Enhanced Ultrasound: How toPerform It inLiver Tumors?
Fig. 2.9 Prolonged heterogeneous liver enhancement. B mode ultrasound through the liver following contrast administration (Sonazoid)
showed wavey, heterogenous areas of increased echogenicity. This
appearance may last for several hours. However, it is likely not clinically signicant and should not be confused for pathology
lar to US ndings of free portal venous gas that have been
observed in end-stage oncological (e.g., gastrointestinal and
urological) diseases within the last hours to days before
death, in severe enterocolitis in newborns and adults as well
as in some asymptomatic patients [27].
2.7 Safety
Ultrasound contrast agents are safe with a very rare incidence of adverse events. Laboratory checks to assess thyroid,
liver, or renal function before administration is not necessary
since there are no hepato-, cardio-, or nephrotoxic effects.
The reported incidence of severe side effects is lower than
that with current CT contrast agents and is comparable to
those with MR contrast agents [6]. It has been reported that
life-threatening anaphylactic reactions in abdominal applications had a rate of 0.001%, with no death in a series of more
than 23,000 abdominal patients [28].
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Improved Detection ofFocal Liver
Lesions withContrast Enhanced
Ultrasound
Bei-JianHuang, YiDong, andWen-PingWang
3
Abbreviations
CEUS Contrast enhanced ultrasound
CT Computed tomography
FLL Focal liver lesion
HCC Hepatocellular carcinoma
IOUS Intraoperative ultrasonography
IO-CEUS Intraoperative contrast-enhanced ultrasound
MRI Magnetic resonance image
3.1 Introduction
• Conventional ultrasound is the most frequently used
imaging modality as the rst-line imaging of abdominal
organs, including the liver, but is reported to be less sensitive than CECT, CEMRI, or intraoperative ultrasound in
the detection of focal liver lesions (FLL).
• CEUS has dramatically increased the capability of conventional ultrasound for detection of FLL, especially
those invisible on conventional ultrasound.
• CEUS has a considerably higher sensitivity of up to
80–90% in detecting liver metastases, comparable to that
of CECT and CEMRI [1].
• CEUS is of particular useful in detecting liver metastases
≤10mm.
3.2 Reasons forFocal Liver Lesions Not
Detected onCEUS
• Despite of its high detection rate and diagnostic accuracy
in FLLs, CEUS still faces the challenges in the detection
of some indistinctive lesions, especially when the diameter of lesion is less than 10mm.
• In the background of liver cirrhosis, some early or recurrent
HCCs may be isoechogenic with indistinctive margins, or
show hyperechoic similar with those of cirrhosis nodules.
• After molecular targeted therapy for colorectal liver
metastasis, some lesions’ volume may shrink and become
isoechoic. These lesions are so-called occult tumors since
they cannot be detected on CEUS or even on CECT.
• In the condition of sever fatty liver, hemotherapy-induced
steatohepatitis, hepatic sinus obstruction, liver structure
changes after repeated surgical procedures and local ablative treatment or residual or recurrent lesions located
adjacent to treatment area, FLLs might be difcult to be
detected by ultrasound.
• Specic tumor location, such as too deep or close to dia-
phragm, subcapsular tumors affected by rib occlusion or
abdominal wall reverberation, may result in difculties in
tumors detection.
3.3 Detection ofLiver Primary
Malignancies
• CEUS have improved detection and characterization of
HCC.Homogeneous hyperenhancement during the arterial phase and mild wash-out are indicative for HCC in
liver cirrhosis.
• The incident rate of recurrent HCCs ranging from 45.2%
B.-J. Huang (*) · Y. Dong · W.-P. Wang
Department of Ultrasound, Zhongshan Hospital, Fudan University,
Shanghai, China
e-mail: huang.beijian@zs-hospital.sh.cn;
dong.yi@zs-hospital.sh.cn
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021
W.-P. Wang et al. (eds.), Contrast-Enhanced Ultrasound Imaging of Hepatic Neoplasms,
https://doi.org/10.1007/978-981-16-1761-4_3
to 60.0% after HCC hepatectomy. The CEUS enhancement pattern of recurrent HCCs including hyper- or isoenhancement during arterial phase, with no wash-out in
portal or late phases (Fig.3.1).
25