5 
Advanced Ultrasound Techniques:
Liver Elastography, Contrast-
Enhanced Ultrasonography, and
Four-Dimensional Ultrasound
MANISH DHYANI  |  JOSEPH R. GRAJO  |  XIAOZHOU MA  | 
ANTHONY E. SAMIR
Elastography
PRINCIPLE
Physicians have long used the technique of palpation in the
clinical setting. The underlying principle of palpation lies in the
ability to feel stiffer tissue in the background of softer tissue
when pressed (palpated). Ultrasound brings this concept to the
imaging platform wherein the deformation caused by a force
can be imaged, and that deformation can be quantified either
visually or quantitatively. Pathologic tissue in any organ is
usually stiffer than normal healthy tissue, and thus the technol-
ogy has a wide range of applications.
IMAGING BASED ELASTOGRAPHY TECHNIQUES
Strain Elastography
Strain elastography (also known as real-time elastography) uses
B-mode imaging as the only ultrasound technique. In this tech-
nique, the force applied over tissue is very similar to that of
palpation, wherein the ultrasound operator applies force over
the tissue of interest using the ultrasound transducer. This
applied force causes deformation of the tissue, which can be
visualized with ultrasound. Given the inherent association of
operator-dependent applied nonquantifiable force, strain elas-
tography is significantly affected by interobserver and intraob-
server variability.
Shear Wave–Based Elastography
Shear wave elastography (SWE) is a technique that uses acoustic
radiation force to induce microscopic tissue movements, pro-
ducing tissue shear waves. Depending on whether the move-
ment of the tissue itself is measured or whether the speed of the
shear waves is measured, the technique is classified either as
acoustic radiation force impulse imaging or SWE imaging.
Given that the acoustic radiation force is quantifiable and con-
stant (not observer dependent), both deformation force and
tissue deformation are known in these techniques. Quantitative
estimates of tissue stiffness, expressed as Young’s modulus or
shear wave velocity, can be obtained.
Liver Elastography
Elastography of the liver has been predominantly used for esti-
mation of liver fibrosis in the setting of diffuse liver disease and
for the noninvasive estimation of portal hypertension.
38
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DIFFUSE LIVER DISEASE
Background and Epidemiology
The prevalence of diffuse liver disease in the United States is
estimated to be as high as 14.78%.1 In 2010, cirrhosis secondary
to diffuse liver diseases resulted in an estimated 49,500 U.S.
deaths and 1.95% of all global deaths.2,3 Diffuse liver disease
has several causes, including hepatic viral disease, alcoholic
liver disease, nonalcoholic fatty liver disease, and autoimmune
hepatitis.4
Pathophysiology
Regardless of cause, chronic diffuse liver disease follows a
common pathophysiologic pathway of fibrosis to severe fibrosis
and eventually cirrhosis (Figure 5-1). The cost of managing and
treating cirrhosis is extremely high and often requires liver
transplantation.
Imaging
The goal of managing diffuse liver disease is to prevent progres-
sion to cirrhosis. Therefore, reliable liver fibrosis staging is nec-
essary to meet this goal. Unfortunately, no conventional imaging
modality (i.e., ultrasound, computed tomography [CT], or
magnetic resonance imaging [MRI]) has shown good sensitivity
or specificity for diagnosing early or severe fibrosis. Most
current imaging modalities have a high sensitivity for the diag-
nosis of cirrhosis, but this renders the goal of management
ineffective.
Liver Biopsy
Liver biopsy currently remains the gold standard for estimation
of liver fibrosis. However, liver biopsy has a number of limita-
tions: (1) invasiveness with an estimated mortality rate of up to
0.13% and a postprocedure pain rate of up to 63.9%,5-8 (2) cost,
(3) interobserver variability,9,10 and (4) sampling error (only
1/50,000th of the liver is sampled).11
HEPATITIS C
Epidemiology
Hepatitis C (HCV) is the most common hepatic viral disease
worldwide, with an estimated prevalence of 5.2 million in the
United States12 and more than 185 million worldwide.13
 5  Advanced Ultrasound Techniques: Liver Elastography, Contrast-Enhanced Ultrasonography, and Four-Dimensional Ultrasound 39

Pathophysiology
HCV progresses insidiously and typically remains asymptom-
atic for decades, represented by the fact that that only 15% to
30% of HCV-infected patients progress to cirrhosis over a 20- to
30-year period.14-16 It has been shown that liver fibrosis of stage
F2 or greater is predictive of subsequent cirrhosis in HCV-
infected patients.17 Recent advances in therapy have been
successful in curing HCV. However, these treatments are very
expensive, with a per-patient drug expenditure of approxi-
mately $80,000.18 Treatment is therefore usually allocated to
those at risk for developing cirrhosis.
ULTRASOUND ELASTOGRAPHY
Shear wave elastographic approaches have good accuracy for
the diagnosis of F2 or greater liver fibrosis in patients with
HCV.19-21 This technique can noninvasively distinguish vary­
ing degrees of liver fibrosis that appear identical on standard
B-mode acquisition (Figures 5-2 and 5-3). SWE has also shown
high accuracy for the diagnosis of cirrhosis (F4 disease).20,21
HEPATITIS B
Epidemiology
An estimated 2 billion people worldwide are infected with hepa-
titis B (HBV).22 However, the majority of infected people clear
the virus and only a small minority remains chronically infected.
Those chronically infected can develop cirrhosis secondary to
chronic liver inflammation. This at-risk population comprises
over 350 million people globally.22
Pathophysiology
Similar to HCV, the finding of F2 or greater fibrosis on liver
biopsy carries an increased risk for subsequent cirrhosis in
patients with chronic hepatitis B.23 Therefore, the imaging diag-
nosis of early fibrosis is of paramount importance.
Imaging
Similar to HCV, conventional imaging (ultrasound, CT, MRI)
has no role in the diagnosis of early fibrosis in this cohort of
patients. Hence, elastography is a great diagnostic imaging tool
for this population.24

NONALCOHOLIC FATTY LIVER DISEASE

Epidemiology
Liver insult
Nonalcoholic fatty liver disease (NAFLD) is the most common
liver disorder, with a prevalence of 17% to 46% in the United
Cirrhosis Fibrosis States25 and a worldwide prevalence of 6% to 35%.26
Pathophysiology
Severe fibrosis NAFLD can essentially be categorized in two forms: simple
Figure 5-1  Pathophysiology of liver fibrosis. Irrespective of the cause
steatosis (~80% of cases), and (2) nonalcoholic steatohepatitis
of chronic liver disease, if left undiagnosed and hence untreated, it (NASH, 20% of cases), in which excess liver fat is associated
progresses to cirrhosis. with inflammation.26 From a clinical standpoint, it is essential

Figure 5-2  Shear wave elastogram of a 67-year-old man with chronic hepatitis C with stage F0 fibrosis on pathologic examination shows an esti-
mated liver Young’s modulus of 6.3 kPa.

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40 PART 1  Imaging Techniques

B
Figure 5-3  A, Contrast-enhanced computed tomography of a 55-year-old man with chronic hepatitis C shows no apparent abnormality in the
liver. B, Shear wave elastogram shows an estimated liver Young’s modulus of 14.3 kPa. The patient had stage F3 fibrosis on pathologic examination
from liver biopsy. B-mode appearance is identical to that in the patient with F0 fibrosis, shown in Figure 5-2.

to accurately distinguish the 20% with NASH at risk for cir-
rhosis from the 80% with simple steatosis who will not progress
and require no treatment.27
Imaging
Ultrasound.  Ultrasound has a modest sensitivity (67%) and
specificity (77%) as a screening tool for steatosis. However, it
has no role in distinguishing inflammation and fibrosis.28
Ultrasound Elastography.  In elastography, early studies have
shown promise in making this differentiation. SWE has shown
an area under the receiver operating characteristic curve (AUC)
of 0.944 in differentiating F2 or greater fibrosis.29 Similarly,
studies have shown AUCs of 0.90 to 0.97 in differentiating F3
or greater fibrosis.30,31
PORTAL HYPERTENSION

Computed Tomography and Magnetic Resonance Imaging.  Cause

CT and MRI can quantify liver fat, but conventional CT and The hallmark of cirrhosis is portal hypertension. However, the
MRI cannot distinguish simple steatosis and NASH, which cur- diagnosis is best made by measuring the hepatic venous pres-
rently requires nontargeted liver core biopsy. sure gradient (HVPG).32

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 5  Advanced Ultrasound Techniques: Liver Elastography, Contrast-Enhanced Ultrasonography, and Four-Dimensional Ultrasound 41
Pathophysiology
The onset of portal hypertension after the development of cir-
rhosis is progressive. However, depending on severity, there is
significant variation among the four stages with varying degrees
of survival. The median 1-year survival in the four stages of
cirrhosis has been reported to be 99%, 97%, 80%, and 43%,
respectively.33
Imaging
Ultrasound, Computed Tomography, and Magnetic Reso-
nance Imaging.  Conventional imaging has high sensitivity for
the detection of cirrhosis. However, there is a limited role in the
diagnosis of HVPG.
Ultrasound Elastography.  Ultrasound elastography has used
both liver and spleen stiffness as a direct assessment of portal
hypertension. Spleen stiffness measurements can be indepen-
dently used as good predictors of clinically significant portal
hypertension using elastography. For diagnosing clinically sig-
nificant portal hypertension, a liver stiffness value of 24.6 kPa
with SWE has been reported to have a sensitivity, specificity, and
accuracy of 81%, 88%, and 82%, respectively.34
Contrast-Enhanced Ultrasound
Investigations of contrast-enhanced ultrasound in the abdomen
are predominantly performed on liver, kidney, pancreas, and
spleen for screening of anatomic structures, lesion characteriza-
tion, and blood volume and perfusion evaluation.
The common enhancing patterns of focal liver lesions are
well established in contrast-enhanced ultrasound (Figure 5-4).
The typical patterns of liver lesions include (1) contrast absence
Figure 5-4  Illustrations of enhancing patterns
of focal liver lesions in contrast-enhanced Arterial phase patterns
ultrasonography.
Contrast absence
(hypoechoic/hypovascular)
Diffuse homogeneous
hyperechoic
Heterogeneous
Diffuse dotted
Diffuse heterogeneous
Rim-like
Peripheral nodular
Spoke-like
Stippled heterogeneous
(basket sign)
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(e.g., cyst or small hemangioma); (2) diffuse hyperechoic
enhancement (e.g., hepatocellular carcinoma [HCC], hyper­
vascular metastasis, and focal nodular hyperplasia [FNH])
(Figure 5-5); (3) heterogeneous enhancement (e.g., large
HCC); (4) diffuse heterogeneous enhancement (e.g., HCC,
lymphoma, metastasis); (5) rim-like enhancement (e.g., ab-
scess, metastasis, cholangiocarcinoma); (6) peripheral nodular
enhancement (e.g., hemangioma) (Figure 5-6); (7) spoke-like
enhancement (e.g., FNH); and (8) stippled heterogeneous or
“basket sign” (e.g., HCC). Malignant lesions usually manifest a
rapid washout, owing to arteriovenous shunts in the portal
venous phase, and centripetal filling is not seen.35 Benign lesions
usually manifest in an isoechoic homogeneous enhancing pat-
tern. The residual central hypoechoic area is often a specific
pattern for the diagnosis of FNH.36
Four-Dimesional Ultrasound
Technical advances in ultrasound have led to earlier diagnoses
and improved monitoring of disease progression.37 One such
advancement, three-dimensional (3D) volumetric ultrasound,
has been reported to be more efficient than 2D imaging in some
applications, such as fetal imaging38 (with no additional side
effects).39,40 4D ultrasound allows for dynamic imaging, such as
observation of fetal activity.38,41
4D ultrasound is the evolution of 3D imaging and is defined
as real-time 3D ultrasound imaging. In other words, a “time
axis” is added to 3D imaging to make the 3D image animated
or updated in real time, providing a “live show” in a 3D view of
the target.39,42 Depending on different settings, 4D ultrasound
can be used to show surface anatomy, such as the fetal face and
gallbladder polyps (Figures 5-7 and 5-8).
Illustration Portal/Late phase patterns Illustration
Contrast absence
(hypoechoic/hypovascular)
Diffuse homogeneous
hyperechoic
Heterogeneous
Residual central hypoechoic area
42 PART 1  Imaging Techniques

C C

A B

C D
Figure 5-5  Images from a 66-year-old man with cirrhosis show a hypoechoic mass (arrows) in the transverse plane of ultrasound and computed
tomography (CT) images. A, Image captured at 14 seconds after the administration of an ultrasound contrast agent represents the diffuse hetero-
geneous contrast enhancement (arrow) in the early arterial phase. B, Image captured at 47 seconds represents the microbubble washout (arrow)
quickly beginning in the portal venous phase. C, Image captured at 78 seconds demonstrates the full washout of microbubbles (arrow) in the
hypoechoic mass. D, Corresponding contrast-enhanced CT image demonstrates the early arterial phase contrast enhancement (arrow). This lesion
was histopathologically proved to be hepatocellular carcinoma.

A B

C D
Figure 5-6  Images from a 59-year-old man show a large hypoechoic mass (arrows) in the sagittal plane during contrast-enhanced ultrasonography
that was incidentally discovered in segment 7 of the liver. A, Image captured at 23 seconds after the administration of an ultrasound contrast agent
represents a typical peripheral nodular contrast enhancement pattern in the early arterial phase. B, Image captured at 47 seconds shows the micro-
bubbles gradually centripetally filling in during the portal venous phase. C, Image captured at 161 seconds demonstrates the microbubbles to finally
fill out the hypoechoic mass, which appears as homogeneous hyperechoic enhancement. The enhancing patterns demonstrate the lesion was a
typical hemangioma. D, Corresponding contrast-enhanced magnetic resonance image in the portal venous phase confirmed the lesion was a
hemangioma.

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 5  Advanced Ultrasound Techniques: Liver Elastography, Contrast-Enhanced Ultrasonography, and Four-Dimensional Ultrasound 43

Figure 5-7  Multiplanar four-dimensional image of an early pregnancy. This image illustrates the typical layout in a 3D/4D display. The upper left,
upper right, and lower left images are usually the transverse, sagittal, and coronal planes of the region of interest (ROI); the green cross (X) and
dashed line (—-) represent the central point and line of the ROI of each plane, which can be adjusted by the operator. The lower right image is the
reconstructed 3D/4D image corresponding to the ROIs selected in the prior three planes. (Courtesy LOGIQlibrary, GE Healthcare.)

Figure 5-8  Single reconstructed three-dimensional image of the gallbladder. A polyp (arrow) in the anterior wall of the gallbladder neck is well
shown using opacity mode. (Courtesy LOGIQlibrary, GE Healthcare.)

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44 PART 1  Imaging Techniques
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