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Journal of Medicine, Radiology, Pathology & Surgery (2015), 1, 17–23
REVIEW ARTICLE
Ultrasound in maxillofacial imaging: A review
Chaya M. David, Ritu Tiwari
Department of Oral Medicine and Radiology, Dayananda Sagar College of Dental Sciences and Hospital, Shavige Malleswara Hills, Bengaluru, Karnataka, India
Keywords
Color Doppler ultrasonography, elastography,
transducer, ultrasonography
Correspondence
Dr. Chaya M. David,
Department of Oral Medicine and Radiology,
Dayananda Sagar College of Dental Sciences
and Hospital, Shavige Malleswara Hills,
Kumaraswamy Layout, Bengaluru - 560 078,
Karnataka, India.
Email: [email protected]
Abstract
The story of the application of ultrasound (US) in imaging goes back a long way in
history. It has been deemed useful in various situations and has evolved over time to
a more sophisticated and precise modality. Some of the advances are in the form of
newer and more useful equipment increasing its pertinence in dentistry and medicine.
Currently, it is being used in various head and neck pathologies owing to its non-invasive
nature and has gained wider acceptance in maxillofacial imaging. In this paper we will
take a relook of US in areas such as its history, basic principles, advances in the equipment
and wide array of applications in head and neck pathologies and also weigh its merits and
demerits in specific areas.
Received 09 May 2015;
Accepted 16 Jun 2015
doi: 10.15713/ins.jmrps.23
Introduction
Imaging forms the cornerstone of accurate diagnosis and
formulation of the treatment plan. With novel advancements in
this field, the existing modalities are successfully redefining the
rules of diagnostic imaging. Ultrasound (US) is one such modality
which has grown by leaps and bound. Strictly speaking, the term
refers to the acoustic waves which corresponds to the upper
limit of sounds audible to humans (>20 KHz). Over the past few
decades, rapid strides in technology have led to the emergence
of an array of applications in the maxillofacial area. The latest
generation of machines and different sizes of transducers suited for
head and neck region have provided enhanced spatial resolution
and excellent near field resolution.[1] There has been a great deal
of interest in the imaging of neoplasms in the thyroid, salivary
gland, the floor of mouth, tongue, and palatal tumors. It can also be
used to assess the lymph nodes, tumor thickness (TT), sialoliths
and in the examination of vessels of the neck like atherosclerotic
plaques in the carotid artery. Other important applications being
US guided fine needle aspiration biopsy, temporomandibular joint
disorders (TMDs), and masticatory muscle assessment.[2,3]
The US continues to gain popularity due to its noninvasive nature, easy availability, and relative cost effectiveness.
Furthermore, it gives “real-time” tomographic images with cross
sectional information.[4]
Despite this, US often have faced criticism due to its high
operator dependence and poor contrast. However, with the
advent of novel improved versions of equipment, color-Doppler
and three-dimensional (3D) US these limitations have been
overcome to a large extent. This article revisits the evolution
of US along with its basic principles and equipment while
highlighting the notable advances made in the technique and its
various contributions in diagnostic maxillofacial imaging.
History
The first recorded evidence referring to the use of sound
waves for the spatial orientation in bats dates back to 1794
by Lazaro Spallanzani, who discovered the phenomenon of
echo-location.[5] Not long after that, in 1877, Jacques, and
Pierre Curie described the piezoelectric and the inverse
piezoelectric effect.[5] This path-breaking discovery led to the
conceptualization of ultrasonography.
Ian Donald introduced the US in diagnostic medicine in 1956,
when he used one-dimensional Amplitude mode (A-mode)
to measure the fetal head. The commercial use of US devices
began in 1963 when “brightness mode” (B-mode) devices were
constructed.[6] In 1955, Satomura and Nimura were credited for
Doppler effect based visualization of blood circulation. What
Journal of Medicine, Radiology, Pathology & Surgery ● Vol. 1:4 ● Jul-Aug 201517
David and Tiwari
followed was the “Sonic Boom” of the 1970s, when the “gray
scale” was introduced that lead to the introduction of US scanners
that generated the real time images. The first use of diagnostic
US in dentistry appears to have been by Baum et al. in 1963, to
image the internal structures of teeth using 15 MHz wave.[7] The
clinical applications in dentistry were studied actively afterward,
the most noteworthy being the work of Palou et al. (1987) in the
measurement of periodontal bone morphology.[8]
The late 1990s to early 2000 saw an expanded the research
focusing on the dental hard tissues and soft tissues. Hinders and
co-workers (1998) developed the US periodontal probe at NASA
Langley Research Center.[6] Culjat et al. (2003) used pulsed US
imaging to determine the enamel thickness.[9] Current research
endeavors at expanding the usage of US in maxillofacial region,
some of them directed in detection of caries, dental cracks and
fractures, soft tissue lesions, periapical lesions, maxillofacial
fractures, muscle thickness, and implant dentistry.[10]
Basic Principles and Equipments in US
Ultrasonography is founded on the principle of conversion of
electric energy to mechanical energy and viz.[11]
The US is a longitudinal pressure wave made of areas of
compression and rarefaction. When transmitted through a
medium, it causes the molecules to oscillate in the course of
wave propagation.[12] Simplest manner of depicting a US beam
is in the form of a parallel bundle for a certain distance beyond
which it disperses. This parallel component is referred to as the
Fresnel zone (near-field) and diverging portion is called the
Fraunhofer zone (far-field) [Figure 1]. Pressure amplitude varies
greatly in the Fresnel zone, and it decreases at a steady rate with
the increasing distance from the transducer in the Fraunhofer
zone.[11] The High-frequency US has a long Fresnal zone and
a greater depth resolution, although the tissue absorption also
increases.[13]
US pulse comprises a collection of frequencies called the
bandwidth (5-20 MHz). Higher is the fundamental frequency,
better is said to be the spatial resolution. As the wave passes
through the tissues, it speeds up during the compression
phase and slows in rarefaction phase. This produces distortion
and creates the harmonic frequencies. Harmonics are those
frequencies which are the multiples of fundamental frequency.
Echoes from the patient being a mirror image of the pulse, also
have the same distortion and harmonic frequencies.[14]
The Diagnostic US utilizes a transducer for conversion
of energy, built on the phenomenon of piezoelectricity. The
piezoelectric effect is a reversible process in which crystals (lead
zirconium titanate) exhibiting the direct effect and the reverse
effect that is, the generation of electrical charge from an applied
mechanical force and vice versa. When an external electric
impulse is sent to these crystals, their dipoles align themselves
in accordance with the electric field leading to a change in
the thickness of the crystal. This begins a series of vibrations
that produce the sound waves which are transmitted into the
tissues.[2]
18
Ultrasound in maxillofacial imaging
Figure 1: Ultrasound beam showing Fresnel and Fraunhofer zone
The transducer functions as both “transmitter” and “receiver”
and obtains the beam reflected from the tissues.[12,15] It detects
and amplifies the weak signals and compresses the wide range of
amplitudes into a range that can be displayed on the screen.[14]
Each transducer is focused at a particular depth.[11] The echoes
so established collectively form an image that can be visualized
and documented.[12,15] The image displayed comprises of a
wide gray scale depending on the echogenicity of the tissue
imaged. Echogenicity is the ability of a surface to return a signal.
Structures are said to be hyperechoic, when they are brighter
than their surroundings, hypoechoic structures are less bright
and appear gray, anechoic structures are black as they do not
produce any signal, whereas, isoechoic have the same echoes as
the surroundings.[14] Several different transducers are available in
clinical practice depending on the area being imaged. Commonly
used ones are linear probes (bandwidth 3-12 MHz) for small
parts, curvilinear or convex probes (1-5 MHz) for obstetrics
and abdominal usage and sector or phased-array (3.5-5 MHz)
for echocardiography and gynecological uses [Figure 2].
Certain new and more specialized variants are also available
now such as the intracavity probes (transesophageal, transrectal,
transvaginal), biplane probe, and intravascular probes.[11,14]
Different imaging mode displays are available in US
A-mode displays the amplitude of the reflected sound. It is used
for measuring the boundaries of tissues of different acoustic
properties.[3]
B-mode produces different echogenicity and shows the
texture and tissue borders as black and white images.[6] As US
wave passes through tissues of different acoustic impedance,
some are reflected back, and some penetrate deeper. The echo
signals so received from many coplanar pulses generate an
image.[4] Owing to the wide gray scale used, even very small
differences in echogenicity can be visualized.
Motion mode, it is a two-dimensional image that allows
recording the motion. It has a high temporal resolution and is
valuable in the accurate evaluation of rapid movements example
in the heart.[4]
Doppler mode this mode is based on the “Doppler effect”
which is defined as “the observed changes in the frequency
Journal of Medicine, Radiology, Pathology & Surgery ● Vol. 1:4 ● Jul-Aug 2015
Ultrasound in maxillofacial imaging
David and Tiwari
Figure 2: Different types of transducers
of transmitted waves when relative motion exists between
the source of the wave and an observer.”[16] This enables the
examination of blood flow in vessels on the basis of backscatter
from erythrocytes.
Color Doppler
It depicts vascular flow in terms of the direction of blood flow and
its mean velocity in the area of concern. Based on the Doppler
shift, it uses color coding to delineate the feeder vessels, namely
red color for arteries and blue for veins. The arterial or venous
nature is defined with a spectral wave pattern that is plotted with
time on the X-axis and Doppler frequency on the Y-axis. It is
especially of use in vascular tumors and vascular malformations.
Other techniques in use are continuous wave Doppler, pulsed
wave Doppler, Doppler duplex, and power Doppler.[17]
Technical Advances in US Equipment
Transducer technology and array designs are constantly
improving.[12] Developments include portable scanners, highfrequency scanners (above 20 MHz), and miniature pocketsize scanners (8.9 cm display and 3.0 MHz phased array for
color Doppler imaging).[18] Broadband transducers with new
piezoelectric materials are available. The Focused US is being
used to overcome the rapid decrease in exposure within the
sonication path. Focusing overcomes the attenuation loss and
concentrates energy deep in the body with little effect on tissues.
The US is focused by radiators, lenses, or reflectors.[12]
Current B-mode US includes special imaging modes such
as tissue harmonic imaging and spatial compound imaging
(multibeam imaging). In modern units, a second harmonic
component is also employed, frequency of which is twice that of
initiating signal. This results in the reduction of artifacts in the
tissues. Spatial compound imaging is the means of electronically
routing parallel US beams to image the same area several times.
The echoes are then compounded into a single image. This
produces reduced “noise” as well as improved contrast and
margins.[4]
Enhanced image resolution has been attained through the
use of contrast-enhanced US using micro bubbles. It has also
increased the sensitivity of US in tumor detection and most of
the functions performed currently by computed tomography
(CT)/magnetic resonance imaging (MRI) can be allocated to
US as well.[18,19]
Variations of US principle have been implicated in
several specifically designed techniques. One among these is,
transcranial Doppler that uses a low-frequency (≤2 MHz) sector
or curved linear array transducer probe, for dynamic monitoring
of intracerebral blood flow velocity and vessel pulsatility.
Its varied applications in vascular pathologies include the
quantification of right to left shunts, subarachnoid hemorrhage,
intra- and extra-cranial arterial stenosis, micro embolism and in
raised intracranial pressure.[20,21]
3D US is another technical advancement that was proposed
and patented first in 1987.[22] It involves the transmission of sound
waves at different angles and reconstruction of the returning echoes
using the complex software to obtain a 3D volume data.[22] Fourdimensional (4D) US is further modified the version of 3D US, in
which the fourth dimension of time is added. That is, the images are
produced in “real time” thus avoiding the time lag observed with the
computer-based reconstructions as is the case with 3D US.[22] 3D/4D
US is principally used in obstetrics for fetal anomaly detection,
echocardiography for congenital heart defects and neurology to
assess the brain development.[22] However, other gynecological and
cardiac applications are also receiving the attention of late.
US elastography is a technique for evaluating the elastic
properties of soft tissues, quantitatively or qualitatively based
on the elastic modulus of tissues. Two types developed are
“shear wave based” and “real-time tissue elastography,” which
are used for the measurement of liver stiffness. It has found that
the application in masticatory muscle assessment in patients
with TMDs or submucous fibrosis and to differentiate between
the benign and malignant tumors in the thyroid, as well. Realtime tissue elastography that uses a grayscale US machine has
also been developed by incorporating elastography into the
conventional US scanner.[23] Elastography, although still partly
under research, has shown the promising results.
Recent digital communications in medicine specifications
have enabled full integration of US with picture archiving and
communications system thus, regulating the storage and transfer
of images.[19] With the innovative newer technologies set to
revolutionize the US practice, it has been ensured that US is
encompassed by the mainstream dentistry.
Applications of US in Maxillofacial Imaging
Imaging of structures in head and neck can be performed with
exquisite details using US.
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David and Tiwari
Ultrasound in maxillofacial imaging
Swellings of head and neck region US can be used in
establishing the differential diagnosis of cystic or solid masses
of the neck, cervical lymphadenopathy. It serves to differentiate
benign from malignant masses and intra glandular and extra
glandular anomalies of the salivary glands.
Inflammatory swellings
Siegert et al. (1987) had initially classified the US appearances
of inflammatory swellings into five types edema, infiltrate, preabscess, echo-poor abscess, and echo-free abscess.[24,25]
Cystic swellings
Cysts appear as an anechoic area due to its fluid/air filled nature.
Since liquids are homogeneous, and there are no structures to
produce internal echoes, there is little or no attenuation of sound,
which creates enhanced transmission of sound at the distal aspect
of cysticmass. If the cyst becomes infected, then the content of
thelesion can produce some echoes leading to a hypoechoic area.
For example, branchial cyst and sebaceous cyst classically appear
as well defined, homogenous, anechoic, and hypoechoic areas
respectively with posterior acoustic enhancement.[15,26]
Benign neoplasms
Pleomorphic adenoma appears as rounded, circumscribed
and hypoechoic with distal acoustic enhancement. Lipomas
are seen as oval or elliptical masses with regular margins and
a typical striped or feathered internal echotexture [Figure 3].
Hemangioma appears as multiple hypoechoic areas with some
amount of vascularity on Doppler study.[15,26]
Malignant neoplasms
The US features depend on the grade of the tumor. Low-grade
malignant neoplasms appear similar to pleomorphic adenoma
and larger lesions present with apparent malignant features such
as irregular, poorly defined margins, and heterogeneous internal
structure.[15,26]
A study conducted by Shankar et al. established the reliability
and diagnostic efficiency of US in head and neck swellings.[26] The
sensitivity and specificity of US in inflammatory swellings was
found to be 96.5% and for cystic swellings, swellings of muscular
origin, lymphadenopathies, it was 100%. In addition, sensitivity and
specificity for benign and malignant neoplasms were 92.86% and
100% respectively.[26] Specific appearances were noted for different
swellings. An abscess appears as an ill-defined hypoechoic area.
Submandibular sialadenitis was seen as duct dilation proximal to
an obstruction. Acute parotitis was seen as an enlarged hypoechoic
gland with coarsening of gland texture and chronic parotitis
presented as a coarse, reticulated pattern with multiple, rounded,
hypoechoic foci seen within the gland parenchyma.[15,26,27]
Oral submucous fibrosis (OSMF)
US can be used to demonstrate the number, length and thickness
of the fibrotic band.[28] OSMF shows the increased hyperechoic
20
Figure 3: Ultrasonographic image of a lipoma in the right cheek
overlying the mandible seen as a focal area in the subcutaneous soft
tissue plane with echotexture similar to subcutaneous fat
areas representing the fibrous bands or diffuse fibrosis.[3] Color
Doppler and spectral Doppler shows the decreased vascularity and
peak systolic velocity in the lesional area.[28] Masticatory muscle
hypertrophy is also seen in OSMF patients who can be assessed with
US. Chakarvarty et al. measured the thickness of masseter muscle
by ultrasonography (5-11 mHz) and found it to be increased in
OSMF as compared to a control group. Also, the thickness was
more during contraction as compared to relaxation in both OSMF
patients and normal individuals.[29] Krithika et al. characterized
the US features of the buccal mucosa in the patients with OSMF
and observed that the submucosa which appeared hypoechoic
in the control group had a significantly increased echogenicity in
the case group. Hence concluding that the increased submucosal
echogenicity and reduced echo differentiation was present in
submucosa and muscle layer in OSMF cases.[30]
Salivary gland ultrasonography (SGUS)
Various parameters that can be studied using US includes salivary
gland volume, the degree of homogeneity (homogeneous, nonhomogeneous), and echogenicity (isoechoic or hypoechoic).
A structurally normal salivary gland has a medium gray scale
homogeneous echo pattern and the level of echogenicity is
higher than that of the surrounding muscles [Figure 4a and b].
SGUS studies can be used to differentiate the inflammatory,
cystic or neoplastic swellings of salivary glands.[25] Salivary gland
obstruction presenting with the pain and swelling is found to
be commonly associated with sialoliths or strictures. Sialoliths
within the gland parenchyma or the duct appear as intense
hyperechoic foci with distal acoustic shadowing, except for small
stones (<2 mm) that present sans a shadow. The duct proximal
to the stone sometimes shows the visible dilatation, and even
radiolucent lith can be visualized using US.[24,27] Obstruction
in the absence of sialolithiasis can be attributed to the ductal
strictures which can be seen in US as hypoechoic ducts with
tapering along with an enlarged gland.[26]
Journal of Medicine, Radiology, Pathology & Surgery ● Vol. 1:4 ● Jul-Aug 2015
Ultrasound in maxillofacial imaging
a
David and Tiwari
b
Figure 4: (a) Ultrasonographic image of a normal right parotid
gland which appears homogenous with increased echogencity
compared to nearby muscles, (b) oval shaped intraparotid lymph
node seen in the parenchyma of parotid with a hyperehoic hilum
SGUS also has been used for diagnosing primary Sjogren’s
syndrome (SS). Cornec et al. studied the echo structure of
the parotid and submandibular glands bilaterally and graded
it from 0 to 4. The gland size was measured, and blood flow to
the parotid gland was calculated using Doppler study. Based on
their findings, they concluded that the addition of SGUS to the
American-European Consensus Group classification criteria for
SS increased the sensitivity to 87.0%.[31]
a
b
Figure 5: (a) Ultrasonographic image of normal right cervical
lymph nodes showing hypoechoic areas of lymphoid tissue,
(b) Color Doppler image of normal right cervical nodes showing
the low flow hilar vascularity pattern
displaced. In open mouth position, normalcy is defined by
intermediate zone located between the condyle and the articular
eminence.[34,36] Razek et al. (2015) assessed the pattern of
articular disc displacement in patients with internal derangement
using US and concluded that the diagnostic efficacy of US for
anterior displacement has sensitivity of 79.3%, specificity of
72.7%.[37]
Cervical lymph node assessment
Other applications of US
Pre-operative US imaging plays an important role in delineating
the surgical treatment plan in malignancies. Normally, the
lymph node appears as a homogeneous hypoechoic area with a
thin cortex and shows hilar vascularity or largely avascular areas
in color Doppler mode [Figure 5a and b].[32,33] Reactive lymph
nodes are hypoechoic with or without the presence of echogenic
hilus whereas neoplastic nodes have indefinite internal or hilar
echoes.[24]
In a study by Hwang and Orloff, the sensitivity and specificity
of US in predicting papillary thyroid carcinoma metastasis in the
central neck was estimated to be 30.0% and 86.8%, respectively
and in the lateral neck 93.8% and 80.0%, respectively.[32] Another
study by Kagawa et al. quantitatively evaluated the relationship
between vascularity within the lymph nodes and lymph node
size on Doppler US images of patients with oral cancer. They
conclude that an increase in vascularity was a characteristic
Doppler US finding in small metastatic lymph nodes, and as the
size increased, blood flow signals got scattered and the scattering
index increased.[33]
Periapical and intraosseous lesions, maxillofacial trauma,
detection of foreign bodies, US guided fine needle biopsy,
submandibular gland injection of botulinum toxin for
hypersalivation in cerebral palsy and in basket retrieval of salivary
stones.[11]
US has gained an importance for squamous cell carcinoma
(SCC) involving the base of the tongue which is difficult to assess
clinically. US based measurement of TT can guide the surgical
resection by giving an indication of grade of malignancy.[38] A
study by Yesuratnam et al. investigated the correlation between
TT of SCC of the tongue, obtained by USG and MRI with the
histological specimens. They concluded that a high correlation
existed thus establishing the utility of US to ascertain preoperative TT.[38] Also, US-based quantitative assessment of
tongue shape and movements has been used in phonological
research to aid the speech therapy in compromised patients.[39]
Color Doppler US has also gained popularity in the diagnosis
of vascular anomalies of head and neck by obviating the need for
biopsies and decreasing the associated risks. It can be used in
imaging of vascular tumors such as hemangiomas, lymphangiomas
or slow-flow and high-flow vascular malformations.[17] A common
color Doppler presentation of arteriovenous malformation of the
tongue is described as a hypoechoic area with lobulated margins
with the depiction of feeder vessels as well.[17] The US here serves
not only as a diagnostic procedure but provides the treatment
guidance as well.
TMDs
High-resolution ultrasonography that shows “real-time” images
of the articular disc during the mouth opening has been used
in the evaluation of TMDs. US image of the disc is of a thin
homogenous, hypo/isoechoic band whereas mandibular condyle
and the articular eminence are appreciated as hyperdense
lines.[34,35]
In closed mouth position, an intermediate zone of the disc
rests between the anterosuperior aspect of the condyle and the
posteroinferior aspect of the articular eminence. When located
anterior to this position, the disc is regarded as anteriorly
Merits and Demerits of US
US is a dynamic technique and useful in the evaluation of soft
tissue structures. Most importantly, it is non-invasive, doesn’t
Journal of Medicine, Radiology, Pathology & Surgery ● Vol. 1:4 ● Jul-Aug 201521
David and Tiwari
Ultrasound in maxillofacial imaging
Table 1: Comparison between CT, MRI and USG
Imaging modality
CT
Advantages
Superior geometric resolution 3D imaging
provides cross‑sectional information, critical
structures can be visualized accurately
Limitations
Streak artifacts in axial and coronal sections thus
reformatted thin‑slice axial CT preferred, motion
artifacts, high cost and radiation dose, limited access
Effective dose (mSv)
2 mSv for head CT
MRI
Excellent evaluation of soft tissues helps
recognize and differentiate critical anatomical
structures, e.g.: Neurovascular bundle from
adjacent trabecular bone
Bony detail cannot be appreciated, magnetic field
strength >3 Tesla causes heating of tissues and noise
(>100 db) ferromagnetic alloys produce image
deformations, geometric distortion
No radiation
exposure
Ultrasonography
Useful for evaluation of soft tissues, real‑time
images, non‑ionizing radiation, non‑invasive
and painless with good patient compliance easy
availably, less expensive, artifacts are uncommon
Operator dependent compromised quality of image
owing to insufficient contrast and resolution
No radiation
exposure
CT: Computed tomography, MRI: Magnetic resonance imaging
use radiation and provides real-time images. Hence, the patient
compliance is excellent. There are fewer occurrences of artifacts
and since the influx of state-of-the-art technologies, the design of
the US has improved manifold. US is now available in a compact
form for clinical use.
The flip side of the coin being, US is still highly operator
dependent and hinges a great deal on the experience and
knowledge of the operator. Since, specific, reproducible scan
planes aren’t available for US, the images are difficult to orient
and interpret. The images also suffer from anatomic noise
accompanying the inherent noise due to the signal returned
to the transducer which makes interpretation of the static and
dynamic images challenging.[11]
The features and utility of US are comparable with that of
other modalities such as CT and MRI (Table 1).[11,15,39]
Conclusion
In the past few years, US have expanded its horizons in
maxillofacial imaging. The sensitivity and specificity of US have
been proved to an acceptable degree in different situations
thus, reinstating the position of US as the imaging modality of
choice in a number of clinically perplexing entities. Although,
the concomitant limitations did exist with US, they have been
largely overcoming with the modifications in the apparatus and
machine. US are a continuously progressing technology, and
further research should be focused on its clinical applications in
the dentomaxillofacial region.
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How to cite this article: David CM, Tiwari R. Ultrasound
in maxillofacial imaging: A review. J Med Radiol Pathol Surg
2015;1:17-23.
Journal of Medicine, Radiology, Pathology & Surgery ● Vol. 1:4 ● Jul-Aug 201523