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leakage. The paranasal sinuses can also be visualized,
which makes this technique suitable even during endoscopic sinus surgery [7].
Although the indications are limited, EUS also can be
performed to visualize the external acoustic meatus using
small-diameter, radial array probes after lling the ear canal
with a saline solution. A linear array probe or a “hockey
stick” transducer can be used to examine the outer ear.
Ultrasonographic examination of the upper trachea, larynx and hypopharynx is performed during microlaryngoscopy after placing the endotracheal tube near the carina and
ooding the lumen with a saline solution to allow acoustic
coupling to the mucosa [8, 9]. Air bubbles are removed by
suction and softly tapping on the cricoid. To evaluate the
posterior larynx, the orotracheal tube is loaded up with a
laryngoscope [1]. Alternatively, a water-lled balloon can be
used around the transducer of the echoendoscope.
15.3 Sonographic Characteristics
ofParticular Structures andClinical
Applications
C. Arens and N. Davaris
a
b
15.3.1 Outer Ear andExternal Acoustic Meatus
The cartilage of the external acoustic meatus and the outer
ear appears hyperechoic, whereas most tumors display as
hypoechoic to isoechoic masses (Fig.15.1).
EUS has also been used to demonstrate middle ear
effusion, but the use of this method is limited in clinical
practice [10].
15.3.2 Nasal Cavity, Paranasal Sinuses,
andNasopharynx
Important anatomical structures such as the nasal septum,
the nasal turbinates, and the lamina papyracea can be recognized by endosonography. These structures appear as hyperechoic lines, whereas the mucosa has a homogenous
isoechoic to hypoechoic pattern. The walls of the paranasal
sinuses can also be visualized as hyperechoic lines. In cases
of extensive defects of the lamina papyracea, the periorbital
adipose tissue can be distinguished as an isoechoic to hyperechoic area (Figs.15.2 and 15.3) [7].
Submucosal glandular or nasolabial cysts appear as an
anechoic, roundish pattern. Hemangiomas and most solid
tumors appear isoechoic or hypoechoic, and EUS can help to
estimate the depth of inltration [11].
The nasopharynx is difcult to assess and displays an
irregular shape. Lymphatic tissue is mostly hyperechoic.
The surrounding bony structures lead to a complete reex-
Fig. 15.1 (a, b) Hemangioma of the outer ear duct. The tumor appears
hypoechoic to anechoic. The bony structures are hyperechoic
Fig. 15.2 Endosonography of the nasal cavity, displays the semilunar
hiatus (red arrow), the conchae (green arrows), and the nasal septum
(blue arrow)
15 Endoscopic Ultrasound
323
Fig. 15.3 A miniprobe is surrounded by hypoechoic nasal polyps
(orange arrow). The blue arrow indicates the nasal septum
Fig. 15.4 In this nasopharynx, the probe is attached to the lymphatic
tissue of the adenoids. Orange arrows mark the velum palatinum
ion and can be visualized as a sharp edge. Cystic lesions
have an anechoic appearance and can easily be detected
(Fig.15.4).
Nasopharyngeal cancer can be examined in a nasopharynx ooded with saline solution. It usually presents as an
exophytic and hypoechoic mass, that can be easily delineated
from the surrounding tissue (Fig.15.5).
15.3.3 Oral Cavity andOropharynx
The oral mucosa usually appears isoechoic with a homogenous pattern. In the buccal mucosa, a hyperechoic aspect is
attributed to the mandibular bone, whereas the sublingual
glands lead to acoustic shadowing in the oor of the mouth
[6]. Cysts and ranula can be easily visualized, appearing
anechoic with a posterior sound enhancement. Lipomas are
Fig. 15.5 Hypoechoic nasopharyngeal cancer. Artefacts are caused by
air bubbles around the probe
mostly ellipsoid in shape, appearing slightly hyperechoic
with characteristic linear echogenic striations parallel to the
skin (featherlike pattern) [12].
Invasive carcinomas appear mostly as hypoechoic to
nearly anechoic masses. The intraoral ultrasound examination can provide precise information about the depth of inltration, the tumor extension, and the depth of the margins in
the tongue or in the mucosa of the buccal area and mouth
oor, avoiding possible artifacts caused by air bubbles or the
mandibula (Figs. 15.6, 15.7, 15.8, and 15.9) [6, 13]. The
tumor thickness can be measured. Modern ultrasound transducers can identify carcinomas with a thickness of 1mm. A
thickness less than 2mm is associated with an extension into
the lamina propria. A thickness greater than 6mm is associated with the inltration of the muscular layer [6, 14].
According to a recent meta-analysis, the sonographic intraoral examination of tumor thickness is highly accurate with
a resolution of 0.5mm [15].
15.3.4 Larynx
Ossication of the laryngeal cartilage in adults and intraluminal air usually do not allow adequate examination of the
larynx by transcervical ultrasound. On the other hand, EUS
can provide precise information about laryngeal lesions as
small as 3 mm. Adequate knowledge of the sonographic
anatomy of the larynx is a prerequisite for endolaryngeal
ultrasound examination and recognition of pathological features. Endosonographic examination of the larynx is usually
performed using a radial echoendoscope (miniprobe), similar to the examination of the trachea. Anatomical structures
such as the vocal ligament, the thyroarytenoid (vocal) muscle, the ventricular fold, the preepiglottic and paraglottic
spaces, and the epiglottis can easily be identied [4].
324
C. Arens and N. Davaris
a
a
b
b
Fig. 15.6 (a) Typical purple appearance of a hemangioma of the left
tongue. (b) Colored duplex mode during endosonography conrms a
high perfusion of the lesion
The vocal folds normally appear hypoechoic because of
the vocalis muscle and the paraglottic space, whereas the
epithelium and the vocal ligament appear hyperechoic. This
hyperechoic pattern is enhanced through signicant differences in impedance between the tissue and the intraluminal
water [1]. The ventricular folds and preepiglottic space have
a slightly denser echo than the vocal folds, possibly due to
the greater amount of tissue containing seromucous glands
and fat [1, 8]. The inner and outer perichondrium of the cricoid and thyroid cartilage appears hyperechoic. The elastic
cartilage in some areas is hypoechoic, but in adults it is
mostly isoechoic to hyperechoic because of ossication [16].
The cricoid appears as a closed ring, whereas the thyroid cartilage has a triangular shape (Figs.15.10, 15.11, and 15.12).
Tumors can usually be identied by endoscopic examination. In the EUS examination carcinomas usually appear
as hypoechoic masses, with clear margins [4]. In exophytic carcinomas or those near the anterior commissure,
it can be difcult to distinguish between an inltrative
growth pattern and lesions just touching the vocal folds.
Fig. 15.7 (a) Endoscopic picture reveals a sialolithiasis of the subman-
dibular duct. (b) Endosonography presents a complete reection of the
ultrasound beam by the stone. Orange arrows indicate distal
shadowing
EUS can be used to detect carcinomas with a minimal
extension of 3mm, but smaller tumors are hardly visible
(Fig.15.13) [1]. Identication of thyroid cartilage inltration by a carcinoma is a crucial issue and of great importance for the therapeutic procedure. It is seen as an
interruption of the inner perichondrium, which then
appears blurred and hypoechoic (Fig. 15.14). However,
precancerous lesions and microinvasive cancer can be better assessed by digital chromoendoscopy and optical
coherence tomography (SIN I-III, T1<3mm). In a prospective study, the authors were able to demonstrate that
EUS has a higher accuracy (89 vs. 77%) in comparison to
CT or MRI.Only the specicity (93 vs. 89%) and positive
predictive value (89 vs. 83%) did not present a signicant
difference between EUS and MRI [17].
The identication of small, benign lesions such as polyps
or vocal fold nodules is usually difcult with EUS alone, but
laryngeal cysts or Reinke’s edema can be identied, appearing as anechoic or hypoechoic masses with a clear border
(Fig.15.15).
EUS is also helpful for the grading of laryngeal stenoses,
before and after surgery [8].
15 Endoscopic Ultrasound
ab
c
325
Fig. 15.8 Tongue cancer. (a) Clinical image of a squamous cell carcinoma of the tongue. (b) and (c) show the tumor in two different planes. The
lesion appears irregular and hypoechoic. The inltration depth and boarding structures can easily be assessed
15.3.5 Trachea
The trachea has a horseshoe shape, which leads to its typical
appearance in EUS (Fig.15.16). The examination is usually
performed using a radial echoendoscope and starts moving
upward inferiorly and continuously, until reaching the cricoid cartilage. The elastic cartilages of the trachea can be
used as anatomical landmarks. They appear hypoechoic,
whereas the inner and outer perichondrium appears hyperechoic. The mucosa is isoechoic with a homogenous echo-
15.3.6 Hypopharynx
Examination of the hypopharynx is performed intraoperatively. The supercial mucosa appears hyperechoic, and the
muscularis layer is hypoechoic. Tumors usually can be well
visualized after endoscopic detection when the hypopharynx
is ooded with saline solution. This technique is suitable to
measure the depth of tumor inltration (Fig.15.17) [19].
In most cases, carotid arteries and possible lymph nodes
also can be identied [4].
genicity [4, 16].
Lesions in the tracheal mucosa or in the membranous por-
tion of the trachea can be identied by the examination, and
15.3.7 Proximal Esophagus
cartilage involvement can also be assessed [4]. Carcinomas
mostly appear hypoechoic, and their size and depth of inltration can be measured. Additionally, EUS can be used to
measure the degree of tracheal stenoses before and after
therapy [16].
In echoendoscopic evaluation of the esophagus, ve tissue
layers can be identied. Examination is usually performed
with a radial echoendoscope. The supercial mucosa
appears hyperechoic and the deeper mucosal layer is
326
C. Arens and N. Davaris
Fig. 15.9 (a) Clinical image of an hemangioma of the left oropharynx. (b) Endosonographic B-mode image presents a sharp delineated hypoechoic
mass. (c) Colored duplex mode demonstrated high perfusion of the lesion indicating an hemangioma
Fig. 15.10 Almost completely closed cricoid ring, with hyperechoic
cartilage
Fig. 15.11 Cricoid ring that opens anteriorly through the cricothyroid
ligament
15 Endoscopic Ultrasound
Fig. 15.12 V-shaped thyroid cartilage. The vocal folds appear
hypoechoic, whereas the elastic cone shows a hyperechoic signal
327
a
a
b
Fig. 15.13 Tumor of the left vocal fold. (a) Clinical image. (b) In
EUS, the orange arrows point at the tumor; the blue arrows indicate the
Morgagni ventricle
b
Fig. 15.14 Recurrent T4 laryngeal cancer. (a) Clinical image. (b) In
EUS, blue arrows indicate inltration of the thyroid cartilage; the
orange arrows indicate the tumor
hypoechoic. The next tissue layer is hyperechoic and corresponds to the submucosa, followed by the muscularis propria (hypoechoic) and the serosa (hyperechoic) [18].
The thyroid gland can be identied as a hyperechoic
structure on either side of the trachea, and the thymus can
sometimes be visualized distal to the thyroid. The left and
right internal jugular veins course medially to the thyroid
gland, and the left and right carotid arteries can also be visualized. Furthermore, paraesophageal and paratracheal lymph
nodes and tumors can be identied in this area (Figs.15.18
and 15.19) [18].
EUS-guided ne-needle aspiration and core biopsies can
easily be performed. The application of linear ultrasound
probes is recommended for ne-needle aspiration, as the needle remains in the imaging beam, allowing precise guidance
and placement. Core biopsies, on the other hand, are preferentially performed with radial array echoendoscopes [19].
328
C. Arens and N. Davaris
a
Fig. 15.17 Endoscopic ultrasound (EUS) examination of the right
piriform sinus with a visible hypoechoic lymph node (LK)
b
Fig. 15.15 Reinke’s edema. (a) Clinical image. (b) In EUS, blue
arrows point at a right-sided Reinke’s edema extending to the supra-
glottic area
Fig. 15.16 Typical horseshoe-shape appearance of the trachea on EUS
Fig. 15.18 Lipoma of the esophagus. Clear delineated echogenic
tumor of the tunica submucosa. Arrow indicates lamina muscularis
propria
15 Endoscopic Ultrasound
Fig. 15.19 Hypoechoic tumor (between markers) of the lamina mus-
cularis propria (arrowhead). It is most likely a leiomyoma. Differential
diagnosis should include a gastrointestinal stromal tumor (GIST)
15.4 Conclusion
Endoscopic ultrasound proves to be a reliable imaging tool
for the investigation of lesions in the head and neck region
329
and can easily be performed during microlaryngoscopy, panendoscopy or even in an ambulatory setting. It offers higher
image resolution than CT scans or MRI and allows complete
sonographic evaluation of whole organs as well as pathological conditions, especially head and neck cancer.
References
1. Arens C, Kraft M.Endoscopic ultrasound of the larynx. Curr Opin
Otolaryngol Head Neck Surg. 2016;24:128–34.
2. Mallery S. Endosonographic instrumentation. In: Shami VM,
Kahaleh M, editors. Endoscopic ultrasound. NewYork: Humana
Press; 2010. p.3–32.
3. Zech M, Scherer M, Maier H, Heppt W.Endosonographie des lar-
ynx. Eur Arch Otorhinolaryngol. 1994;251:480–1.
4. Kraft M, Mende S, Arnoux A, Arens C.Anatomical landmarks for
endosonography of the larynx. Head Neck. 2010;32:326–32.
5. Sugiura K, Iwai T, Oguri S, Tohnai I. Intraoral ultrasonography
with wrapped acoustic coupling medium. Br J Oral Maxillofac
Surg. 2017;55:202–4.
6. Shintani S, Yoshihama Y, Ueyama Y, Terakado N, Kamei S,
Fijimoto Y, et al. The usefulness of intraoral ultrasonography
in the evaluation of oral cancer. Int J Oral Maxillofac Surg.
2001;30:139–43.
7. Noda K, Tamura M, Doi K, Kubo T.Ultrasonography in a nasal
cavity lled with water during endoscopic sinus surgery. Ann Otol
Rhinol Laryngol. 2002;111:836–41.
8. Arens C, Glanz H. Endoscopic high-frequency ultrasound of the
larynx. Eur Arch Otorhinolaryngol. 1999;256:316–22.
9. Tamura E, Kitahara S, Kohno N.Clinical assessment of intralaryn-
geal ultrasonography. Laryngoscope. 2001;111:1767–70.
10. Wu CH, Hsu CJ, Hsieh FJ.Preliminary use of endoluminal ultraso-
nography in assessment of middle ear with effusion. J Ultrasound
Med. 1998;17:427–30.
11. Pruna X, Inaraja L, Gallardo E, Serra J, Casamitjana F, Serrano
A. Value of sonography in the assessment of space-occupying lesions of the anterior nasal fossa. J Clin Ultrasound.
2000;28:14–9.
12. La’porte SJ, Juttla JK, Lingam RK.Imaging the oor of the mouth
and the sublingual space. Radiographics. 2011;31:1215–30.
13. Helbig M, Flechtenmacher C, Hansmann J, Dietz A, Tasman
AJ.Intraoperative B-mode endosonography of tongue carcinoma.
Head Neck. 2001;23:233–7.
14. Angelelli G, Moschetta M, Limongelli L, Albergo A, Lacalendola
E, Brindicci F, etal. Endocavitary sonography of early oral cavity
malignant tumors. Head Neck. 2017;39:1349–56.
15. Klein Nulent TJW, Noorlag R, Van Cann EM, Pameijer FA,
Willems SM, Yesuratnam A, et al. Intraoral ultrasonography to
measure tumor thickness of oral cancer: a systematic review and
meta-analysis. Oral Oncol. 2018;77:29–36.
16. Arens C, Eistert B, Glanz H, Waas W.Endolaryngeal high- frequency
ultrasound. Eur Arch Otorhinolaryngol. 1998;255:250–5.
17. Kraft M, Bruns N, Hügens-Penzel M, Arens C.Clinical value of
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18. Cooper ST, Sanders MK.Radial endoscopic ultrasound. In: Shami
VM, Kahaleh M, editors. Endoscopic ultrasound. New York:
Humana Press; 2010. p.63–90.
19. Arens C, Weigt J, Schumacher J, Kraft M.Ultrasound of the lar-
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2011;59(2):145–54.
Contrast-Enhanced Ultrasonography: Clinical Applications
JulianKüstermeyer
16
16.1 Introduction
Contrast-enhanced ultrasound (CEUS) is an emerging
diagnostic technique. It was rst described in the 1990s as
a combination of using a contrast agent with established
ultrasound techniques. It allows analysis of perfusion patterns in greater detail than conventional sonographic
modalities. Today, a number of contrast agents with different properties are available for a variety of indications.
Since the technique’s beginnings two decades ago, contrast
agents have steadily improved. Besides its diagnostic features, therapeutic options are given by using targeted contrast agents, which release specic drugs locally.
Meanwhile, cardiac, vascular, and abdominal examinations
with CEUS have become accurate tools in clinical routines,
especially in Europe and Asia [1]. For some years now,
CEUS applications have also become more and more valuable in the eld of head and neck sonography, even though
international guidelines initially were only available for
CEUS in the liver. A consensus initiative of the World
Federation for Ultrasound in Medicine and Biology
(WFUMB) and the European Federation of Societies for
Ultrasound in Medicine and Biology (EFSUMB) rst published recommendations for these guidelines in 2012 [2].
Currently there are no internationally approved guidelines
regarding the use of CEUS for extrahepatic applications,
except the European guidelines from 2012 [3]. They include
recommendations and indications for CEUS applications in
the head and neck: assessment of the carotid artery or neck
Electronic Supplementary Material The online version of this chapter (https://doi.org/10.1007/978-3-030-12641-4_16) contains supplementary material, which is available to authorized users.
J. Küstermeyer (*)
Department of Otorhinolaryngology, Head and Neck Surgery,
KRH Nordstadt Clinic–Academic Hospital, Hannover, Germany
e-mail: julian.kuestermeyer@krh.eu
abscesses, monitoring of tumor therapy, and follow-up of
ap transplants, lymph nodes, and the salivary glands [4].
In summary, the application of CEUS in the head and
neck to date has meant off-label use in many diseases, but the
European guidelines explicitly recommend its use for some
particular indications in the head and neck. Many studies
report an improvement of diagnostic accuracy by using
CEUS in the head and neck, and there appear to be a variety
of promising applications for future clinical routines.
16.2 Basics andTechnical Remarks
Contrast agents used for CEUS consist of microbubbles with
diameters of about 3μm, which is comparable to the scale of
erythrocytes. Most of these commercially available microbubble contrast agents comprise a core of gas coated with
lipid or protein layers. Earlier generations of microbubbles
consisted of an air-lled core, which was not as durable as
the current gas-lled bubbles. Their physicochemical properties prevent them from leaking from intact blood vessels
into the surrounding tissues and circulating freely inside the
systemic vasculature. Unlike contrast agents used for CT or
MRI, microbubbles do not diffuse through the endothelium
of blood vessels. Therefore, the microbubbles also help to
detect the perfusion of very small vessels. Other conventional ultrasound modalities, such as color-coded duplex
sonography, allow solely the detection of vascularization,
whereas CEUS allows detection of perfusion. Also, ultrasound contrast agents are used extravascularly in body cavities; for example, they can be used to detect sialolithiasis in
the salivary ducts.
Microbubbles are prepared by shaking a dry mixture with
a saline solution. The application is mostly intravenous, in a
dosage of about 1–5 mL through a venous catheter.
Afterwards, the bubbles can be detected for about 5minutes
until they disrupt and are metabolized, primarily by the lung
and (to a smaller degree) by the liver.
© Springer Nature Switzerland AG 2019
H. J. Welkoborsky, P. Jecker (eds.), Ultrasonography of the Head and Neck, https://doi.org/10.1007/978-3-030-12641-4_16
331
332
10
Received frequency (MHz)
Microbubble signal generation
Signal (dB)
J. Küstermeyer
Unrelated to CEUS, the effective pressure to which a tissue is exposed can be calculated as the mechanical index
(MI)—a unitless number in which higher values mean
increased pressure. In most areas worldwide, manufacturers
need to equip ultrasound scanners with an indication of the
mechanical index in order to control it and avoid adverse
effects like cavitation. The US Food and Drug Administration
(FDA), for example, stipulates that diagnostic ultrasound
scanners work with a maximum MI of 1.9 [5]. CEUS is often
performed at low mechanical indices, which are dened as
less than 0.3 [6]. Low mechanical indices are suitable to
induce oscillations of the microbubbles without disrupting
them, whereas high mechanical indices will lead to bursting
of microbubbles.
Ultrasound transducers emit acoustic pressure, changing from positive to negative like a sinusoidal function.
Microbubble contrast agents scatter ultrasound according
to the applied amplitude of pressure, measured as the
mechanical index, and show vibrations. These properties
make these agents signicantly more reective than physiological tissue, and so they enhance both B-mode images
and ow-mediated Doppler signals [7]. Microbubbles
change their conguration between compression and
expansion, according to the sinusoidal pressure applied. In
contrast to normal tissue, which shows a linear behavior to
pressure, microbubbles present different kinetics. They
respond asymmetrically, with a more extensive changing
of radius during the negative- pressure phase than in the
positive-pressure phase [8, 9]. Because of this property,
microbubbles begin to show nonlinear characteristics like
harmonic oscillations—or overtones, when the exposed
mechanical force exceeds a specic limit (Fig.16.1). By
reaching a certain amount of acoustic pressure, the bubbles
nally begin to disrupt. These contexts are crucial for
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understanding most of the current CEUS techniques.
Modern ultrasound scanners use these physical effects to
cancel the linear signals from tissue and detect the nonlinear responses from the microbubbles.
There are two different methods for utilizing these
characteristics. First is harmonic imaging, which lters the
harmonic oscillations, preferably at double the transmitted
frequency. Second is pulse-inversion imaging, which uses
the nonlinear kinetics of the microbubbles. When two
pulses are sent rapidly to tissue, the second pulse mirrors
the rst pulse, according to a sinusoidal function.
Therefore, the sum of both pulses is zero. Since microbubbles respond with an asymmetrical echo, the rst echo
does not mirror the second (Fig.16.2). This technical issue
allows separation of tissue signals from microbubble signals [8–11]. Pulse-inversion imaging enables higher image
resolutions and a greater bandwidth of the transducer than
with harmonic imaging [12].
16.2.1 Safety Considerations
Extensive use of ultrasound contrast agents over the years
has proven them to be very safe. Reports of side effects and
severe adverse reactions are rare. The composition of the
gas-lled bubbles causes a gentle metabolism. Microbubbles
are not nephrotoxic and do not interact with the thyroid
gland, so preliminary blood screening tests are not necessary. The incidence of hypersensitivity and anaphylactoid
reactions is far lower than for contrast agents used for CT
scans. The rate of adverse effects is described as 0.0098%
for SonoVue®, which is the most widely used agent [13].
Microbubbles should not be used for diagnosis in patients
with severe coronary artery disease and pulmonary hypertension, and patients who have experienced unstable ischemic
heart disease in the prior 7 days should be excluded.
Pregnancy is a contraindication for using ultrasound contrast
agents, as is breastfeeding in some regions.
Although the application of microbubbles in the pediatric
context is not ofcially approved, it is widely accepted [14].
For some indications, it even allows for reduced exposure to
ionizing radiation.
Facilities for shock management and resuscitation
should be available during the use of ultrasound contrast
agents [15, 16].
16.2.2 Regulatory Status
Fig. 16.1 Microbubbles’ response is dependent on the received ultra-
sound frequency with a peak at 4MHz and a second peak (equal to
harmonic overtones) at double the frequency
Different ultrasound contrast agents are marketed worldwide
with varying congurations and approved indications
(Table16.1). Approval status differs across various regions