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A. N. Sencha et al.
2. Nodules with a medium degree of vascularization have the same intensity of
blood ow as the thyroid parenchyma.
3. Hypovascular nodules demonstrate poor vascularization as compared with the
surrounding parenchyma.
4. Avascular nodules have no inner color spots and no peripheral rim.
Some types of vascularization are characteristic for selected lesions. For example, cysts are avascular. The hypervascular mixed type of blood ow is suspicious
for follicular lesion. However, there is no consent about the value of CDI for differential diagnosis of thyroid cancer yet. Khadra et al. [36] published the metaanalysis of 89 publications and 14 prospective studies inclusive of 4154 thyroid
nodules. They reported that utilization of vascular ow on CDI may not accurately
predict malignancy in thyroid nodules.
CDI has some disadvantages, such as distortions of the Doppler spectrum (aliasing artifact), baseline noise, and dependence on the angle of the US beam.
Power Doppler imaging (PDI) is 3–5 times more sensitive than the CDI.It demonstrates a decreased dependence on the angle between the US beam and the blood
ow and has a lower noise-to-signal ratio. It permits images of smaller vessels with
sharper contours to be obtained (Fig.1.10).
The technologies based on non-Doppler imaging of blood ow facilitate assessment of microvascularity (Fig.1.11). The presentation of these techniques is similar
to the image of contrast-enhanced ultrasound. It gives valuable information about
the distribution of small vessels (architectonics) but lacks time-related data (assessment of wash-in and washout phases of blood ow is impossible).
In pulsed-wave (PW) Doppler, a curve resulting from the Doppler shift is produced via computer processing. This permits the analysis of the velocity and spectral parameters of the blood ow as well as the calculation of some indices
(Fig.1.12).
PW Doppler is valuable for diagnosis and follow-up the patient thyroid disorders, accompanied with thyrotoxicosis. In untreated Grave’s disease, thyroidal
artery ow velocity and PSV are signicantly increased [37]. The PSV can differentiate between thyrotoxicosis owing to Grave’s disease from subacute thyroiditis
or amiodarone-induced thyrotoxicosis type 2, where the blood ow is reduced.
Joish etal. [38] suggest the following normal values in the superior thyroid artery
(STA) in euthyroid patients: the average peak systolic velocity (PSV) is
16.94±5.3cm/s; the resistance index (RI) is 0.5±0.1; and the pulsatility index (PI)
is 0.93±0.31.
PW Doppler can conrm difference in blood ow within the nodule as compared
to that in the surrounding parenchyma. Blood ow within the nodule is dened by
both its morphological structure and its size and may vary substantially, which complicates the interpretation. However, the data about the value of PW Doppler in
differentiation between benign and malignant lesions is still disputable. Some
researchers demonstrate that malignant nodules have RI (over 0.73) and PI (over
1.3) higher as compared with benign nodules [39].
1 Current State oftheProblem ofThyroid Diseases: Principles andTechnology…
a
b
21
Fig. 1.10 (a, b) Thyroid US image. Power Doppler imaging
Our own research revealed no regularity in blood ow parameters. PW Doppler
data in thyroid nodules show a wide dispersion and do not carry signicant additional information. This precludes PW Doppler from being used for the differential
diagnosis of thyroid nodules, although it may be used as an accessory feature.
Ultrasound elastography (USE) is an imaging technique based on the difference
in the elastic properties (stiffness) of normal and diseased tissues. USE is a machine
analog of palpation. Structures that are hard with palpation exhibit hard features
with elastography. Hence, it permits to detect hard tumors on soft background.
Many authors report that it helps to diagnose and differentiate cancer at early stage
and to specify its invasion [40–46].
It is available as an option for modern US scanners. The manufacturers of ultrasound equipment often use various methods of elastography with their own trademarks, for example, Natural Touch (Mindray), eSie Touch (Siemens), ElastoScan
22
A. N. Sencha et al.
a
b
Fig. 1.11 Thyroid US image. Examples of non-Doppler imaging of blood ow. (a) B-ow. (b)
Microow
(Samsung Medison), Real-Time Tissue Elastography HI-RTE (Hitachi), ElastoQ
(Toshiba), and just elastography (GE, Philips) and many others.
Ophir etal. [43] was the rst to introduce elastography for diagnostics in the
early 1990s of the twentieth century. Ultrasound elastography techniques can be
divided into two major groups, as follows:
• Strain imaging
• Shear wave imaging
Traditionally, the principle method of strain imaging is compression elastography. The technology determines tissue deformation with strain under compression
1 Current State oftheProblem ofThyroid Diseases: Principles andTechnology…
a
23
b
Fig. 1.12 (a, b) Thyroid US image. Pulsed-wave Doppler mode
and can compute relative stiffness (elasticity coefcient). Compression can be
applied articially from the outside, for example, by the hand of the examiner or
special vibrator. Alternatively, pulsation of the walls of the major vessels and heart
can be used as strain factors. The difference in tissue elasticity results in the difference in strain.
When carrying out compression USE, the ultrasound probe is positioned perpendicular to the skin over the thyroid gland and the lesion. Additional external pressure with the probe is rhythmically applied one to two times per second to the entire
surface with displacement of 1–5mm. Total compression usually lasts for 2–5 s
until several static images with minor noise and artifacts are displayed. To improve
24
A. N. Sencha et al.
a
b
Fig. 1.13 (a, b) Thyroid US image. USE. Different color of the nodules reects different
stiffness
interobserver reliability and effectively control the degree of compression, the scanner displays a special reference icon (in the shape of a circle, spring, scale, index,
etc.). As a result, a color “compressive” image superimposed over greyscale image
is displayed on the screen. Certain color map is used to code tissue stiffness
(Fig.1.13). Hard structures are usually colored with dark or blue. Soft areas are usually marked with light or red. Intermediate colors are applied, respectively. Scanners
usually offer several color maps, such as “blue-green-red,” shades of gray, or customized maps with shades of red or other colors. Abnormal tissues often have their
own strain characteristics. Hard lesions are suspicious for malignancy.
1 Current State oftheProblem ofThyroid Diseases: Principles andTechnology…
25
The following elastographic features of thyroid lesions are necessary to
assess [44]:
• Presence and intensity of the color pattern in the structure of the lesion
• Type of color (hard, soft, mixed)
• Homogeneous/heterogeneous
• Size of colored area in comparison with the size of grayscale size of the lesion
• Differentiation of colored zone from the surrounding tissues
Itoh etal. [47], Rago etal. [48], and Zubarev etal. [46] specify a ve-point scale
of elasticity score with USE.A score of 1 corresponded to even elasticity of the
entire lesion (i.e., the entire lesion was evenly shaded in green). A score of 2 indicated elasticity in large part of the nodule, with some areas of no strain (i.e., the
hypoechoic lesion had a mosaic pattern of green and blue). A score of 3 indicated
elasticity only at the peripheral part of the lesion (i.e., the peripheral part of lesion
was green, and the central part was blue). A score of 4 indicated no elasticity in the
entire hypoechoic lesion (i.e., the entire lesion was blue, but its surrounding area
was not included). A score of 5 indicated no elasticity in the entire lesion and in the
surrounding area (i.e., both the entire hypoechoic lesion and its surrounding area
were blue). The higher score corresponded to the increased risk of malignancy
Compression USE is relatively simple to perform, but it is not easily reproducible. Uniform compression of the whole thyroid gland is impossible due to short
probe aperture. Neck structure, especially the trachea, prevents from compression
of both lobes together. Compression of individual parts (one lobe or isthmus) that
contain lesions is much easier and efcient. Park etal. [49] demonstrated very high
interobserver variability with free hand compression USE.
The data on the diagnostic value of USE in thyroid lesions are contradictory. The
sensitivity ranges from 73% to 100% with specicity of 60–95% [12, 44, 50–53].
USE permits assessment of only the lesions that were detected with conventional
ultrasound. It cannot be used as a screening method. USE supplies additional data
that is sometimes crucial for the indication of FNAB.Garra (2011) reported that
biopsy could be avoided in approximately 15% of lesions that would ordinarily be
biopsied without increasing the rate of missed cancers. According to Sencha etal.
[55], USE decreases the number of FNAB by 6.9%, thereby reducing the risk of
complications and the level of patient’s stress associated with invasive procedure.
Quantitative (digital) data are more objective for assessment of tissue elasticity.
These methods utilize shear wave technology and are often named elastometry. As
opposed to manual compression elastography, they induce tissue strain with a standardized machine-generated impulse. It could be a mechanical impulse for transient
elastography (which is generally used for liver stiffness assessment) or ultrasound
impulse of high energy. They are signicantly less operator-dependent.
The technology of share-wave elastography is based on the fact that the shear
wave velocity depends on tissue strain. The harder the tissue (which is common
for malignant tumors), the higher the shear wave velocity. Measurement of shear
26
A. N. Sencha et al.
a
b
Fig. 1.14 Elastometry. Echograms. (a) Shear wave elastography of the thyroid gland. Measuring
the Young’s modulus in the thyroid parenchyma. (b) Virtual Touch Tissue Quantication.
Measurement of shear wave velocity in a thyroid lesion
wave velocity permits assessment of tissue rigidity. Higher velocity corresponds
to harder tissue.
There are the following true quantitative indicators of rigidity/elasticity of tissues (Fig.1.14):
• Young’s modulus (measured in kPa)
• Shear wave velocity (m/s)
There are also several indexes that are based on two above-listed indicators.
However, some elasticity indices, such as strain ratio, are semiquantitative since
1 Current State oftheProblem ofThyroid Diseases: Principles andTechnology…
27
they are calculated on the basis of qualitative data. Heterogeneous soft tissues can
have complex pattern of shear wave propagation due to reections from the boundaries of structures with different acoustic impedance resulting in data distortion.
Shear wave elastometry has different trade names in US scanners of different
manufacturers, such as VTTQ (Virtual Touch Tissue Quantication), Siemens;
Natural Touch, Mindray; TE (Transient Elastography), Echosens; ElastQ and
ElastPQ, Philips; SWE (Shear Wave Elastography), SuperSonic Imagine; etc. The
technology of shear wave elastography was rst implemented in FibroScan system
for liver examination. Several studies on assessment of the thyroid gland with shear
wave elastography were conducted [42, 56–62]. Shear wave elastography provides
a
b
Fig. 1.15 (a, b) Measurement of the strain ratio. Echograms
28
A. N. Sencha et al.
more reliable data as compared with compression USE.It is less dependent on operator’s experience and exhibits smaller interobserver variability [42, 63].
Denition of Young’s modulus facilitates ultrasound differentiation of thyroid
cancer [40]. The technique of the study is easy and fast to perform.
Stiffness (Young’s modulus) of thyroid lesions over 50kPa is usually suspicious
for malignancy. According to Sebag etal. [61], Magri etal. [64], Ivanishina [40],
and Mitkov etal. [18], the Young’s modulus (stiffness) exhibits the following values: in AITD 5–69kPa, in benign thyroid lesions 30–50 kPa, and in malignant
tumors 15–150kPa. The sensitivity of shear wave elastography in differential diagnosis of thyroid cancer is 85–100% with specicity of 78–94% [40, 42, 44, 58, 61].
The elasticity of thyroid lesion is usually compared with surrounding normal
thyroid tissue or other structures and is presented with strain ratio index. Strain
ratio, which is calculated as the ratio of Young’s modulus (or shear swave velocity)
in the lesion and the reference tissue, is a real quantitative parameter. In some cases,
the scanner has the software to make similar calculation based on compression USE
without measurement of specic digital values for every target area. In spite of the
numerical expression, it is semiquantitative in these cases (Fig.1.15). Malignant
thyroid lesions in our own study demonstrated the average strain ratio of 3.4±0.84.
According to Sencha etal. [44] and Ivanishina [40], the sensitivity of shear wave
elastography in the diagnosis of thyroid cancer is 78–86% with specicity of 82–90%.
USE is a relatively new modality. Prospects for its practical use are not quite
clear yet. Nevertheless, it supplies important additional data for assessment the
character of tissue changes and is expected to facilitate detection of early cancer and
differential diagnosis of thyroid lesions [40–42, 45, 50, 55].
Contrast-enhanced ultrasound (CEUS) is the technology that uses intravenously
administered contrast agents for the assessment of vascularity. Its sensitivity is
higher than the sensitivity of CDI and PDI [65–70].
The rst reports on the use of contrast agents for diagnostic ultrasound were
published in 1969 [71]. The rst contrast-enhanced ultrasound studies of the thyroid
gland with attempts to differentiate carcinomas, benign nodules, and follicular ade-
®
nomas utilized Levovist
contrast medium [72]. The second-generation contrast
agent SonoVue® (Lumason® for USA) (Bracco Swiss SA, Switzerland) is one popular ultrasound contrast medium approved for the use in many countries including
Europe (EMA) and USA (FDA). It is proven safe and well tolerated.
CEUS in diagnosis of thyroid diseases is briey discussed in available literature.
Data on its diagnostic value is controversial. Recent studies demonstrated statistically signicant differences in qualitative and quantitative characteristics of contrast
enhancement of benign and malignant thyroid lesions [65, 68, 70, 73, 74].
The technique of CEUS is identical for different organs and is well described for liver
study. Contrast agent is a suspension of sulfur hexauoride microbubbles surrounded by
a phospholipid shell. Since microbubbles are very fragile and easily destroyed with conventional US, CEUS requires special “contrast” option of ultrasound scanner that works
with low mechanical index. The medium is administered as an intravenous bolus injection (Fig.1.16a). It quickly arrives to the thyroid gland with intensive contrasting and
rapidly washes out. In the “contrast” mode, the screens are usually divided into two parts
1 Current State oftheProblem ofThyroid Diseases: Principles andTechnology…
29
that show real-time grayscale image and contrast image (sepia colored). Video (cineloop)
recording and time registration should start simultaneously with introduction of contrast
agent and last not less than 180s. It permits the analysis of the cine in all phases (arterial,
venous, and delayed) after the end of the procedure.
®
SonoVue
is an intravascular contrast agent and circulates only within vessel
lumen. It permits precise assessment of thyroid vascularity. Thyroid CEUS is characterized with some important qualitative criteria, such as intensity of blood supply,
distribution of vessels, and dynamics of wash-in and washout. High vascularity of
the thyroid parenchyma with dense rate of microvessels results in its strong overall
a
b
Fig. 1.16 Thyroid CEUS with 2.4ml of SonoVue®. (a) Photo of the position of the patient and
medical staff. (b) Arterial phase of contrast enhancement of a thyroid lesion. Sonogram. (c) Timeintensity curve of contrast enhancement. (d) Numerical data on contrast enhancement dynamics