Key words
dermatologic ultrasound - guidelines and recommendations - skin ultrasound
Introduction
Dermatologic ultrasound (DERMUS) is an application of ultrasonography (US) in the
study of the normal and diseased state of the skin and appendages (nails and hair)
[1].
As it is a growing, recently developed application, guidelines and recommendations
based on scientific evidence are not methodologically possible. However, a position
statement from a scientific society with regards to this application of US is useful
for physicians involved in dermatologic US, allowing for the foundations of present
clinical practice and evidence generation to be developed [2]
[3].
Methodological structure and classification of the consensus levels
Methodological structure and classification of the consensus levels
The executive board of the European Federation of Societies for Ultrasound in Medicine
and Biology (EFSUMB) designated a dermatologic ultrasound steering committee based
on qualifications including relevant publications, clinical experience and absence
of conflict of interest. The Policy Document Development Strategy for Clinical Practice
Guidelines, Position Statements and Technological Reviews of the EFSUMB was adhered
to throughout the process for this position statement [4].
The main topics regarding dermatologic US were selected by the steering group and
a comprehensive scientific literature search was performed to identify relevant studies.
Recommendations were elaborated by steering committee members and a consensus meeting
for expert evaluation of these recommendations was convened at the EUROSON 2019 Congress
(Granada, Spain).
A position statement was approved if > 75 % of voting members were in agreement (broad
agreement: > 75–95 % of votes, strong consensus > 95 % of the votes). For discussion
a nominal group technique was applied [4]. In the case of disagreement (≤ 50 % of the votes or less in favor) or if the rephrased
or alternative position statement again failed to gain > 75 % of votes, the position
statement was removed. A lack of consensus on this particular issue would be recorded
in the text as recommended by the EFSUMB policy document [4].
1. Technical requirements for dermatologic ultrasound
1. Technical requirements for dermatologic ultrasound
The main technological advance that has made dermatologic US possible is the introduction
of high-frequency and very high-frequency transducers with enough spatial resolution
to study the superficial structures of the skin and appendages [5]
[6].
According to the DERMUS group (an international group of experts in dermatologic ultrasound),
dermatologic US for the skin and appendages should be performed using a linear multiple
frequency 15 MHz transducer as the minimum standard [2].
Newer very high-frequency (> 20 MHz) and ultra-high-frequency transducers (30–70 MHz)
allow exploration of small adnexal structures, such as sebaceous glands and apocrine
and eccrine glands [7].
Operators performing a dermatology ultrasound study should be aware of patient history
and clinical findings. A detailed request from the referring clinician should be available
(strong agreement 9/9, 100 %).
The minimum transducer frequency for dermatologic ultrasound should be 15 MHz. Higher
transducer frequencies may provide further information that may be relevant (broad
agreement 8/9, 88.9 %).
Both gel hips and gel pads, which make it possible to separate the epidermis from
the transducer, should be used for accurate epidermal evaluation and avoidance of
superficial vascular plexus compression [8]
[9]
Also according to the DERMUS group, all US examinations should include color, power
or spectral Doppler US to ascertain the presence of a vascular anomaly, providing
fundamental information regarding inflammation and neovascularization [2]
[10].
In order to detect superficial dermal, subdermal, small vessels, the pulse repetition
frequency (PRF) should be adjusted accordingly and the gain should be adjusted to
reduce flare artifacts [11]. Proper training in color and spectral Doppler US should be included in dermatologic
US training programs [3] (see training section).
Trapezoid field-of-view (FOV) and extended FOV facilities are useful in the evaluation
of large or deep lesions. Three-dimensional reconstruction software and new non-Doppler
facilities for microvasculature assessment are useful and should be employed, if available
on the ultrasound machine [12].
Current experience regarding dermatology application of elastography is limited, and
contrast-enhanced ultrasound (CEUS) has not been deployed in dermatology US practice
[13]
[14].
Color Doppler/power Doppler and pulsed spectral Doppler (in the case of vascular anomalies)
are recommended to establish inflammatory state of skin and appendages and the presence
or neovascularization (strong agreement 9/9, 100 %).
2. Ultrasound of normal skin and appendage
2. Ultrasound of normal skin and appendage
Anatomical and histological structures of skin and appendages present differential
echogenicity that must be known as changes may indicate pathology [11]
[15].
2.1 Ultrasound of normal skin
Ultrasound of the skin is basically a correlation of the different layers (epidermis,
dermis and subcutaneous tissue) with the acoustic interphases they produce [16].
-
The epidermis is a hyperechoic line due to its keratin content,
-
The dermis is a band inferior to the epidermal line which is less hyperechoic than
the dermis, due to the rich collagen content
-
Subcutaneous fat is a complex structure composed of hyperechoic collagen septa and
hypoechoic fatty lobules
2.2 Ultrasound of hair tracts and follicles
A hair tract (the visible part of hair) is the final keratinized product of hair follicles,
which are oblique cellular structures in the dermis [17]
[18].
-
A hair tract is a bilaminar or trilaminar lineal hyperechoic structure depending on
the presence of medulla (terminal follicles) [19]
-
Hair follicles are oblique hypoechoic structures that may vary in depth from subcutis
to upper dermis depending on the phase of growth (early anagen follicles are deeper
that superficial catagen follicles)
2.3 Ultrasound of the normal nail apparatus
The nail apparatus has a very close relationship with the distal interphalangeal joint.
Four elements must be assessed [20]
[21]
-
Nail plate: Bilaminar hyperechoic structure due to the keratin content
-
Nail bed: Between nail plate and cortex of the distal phalanx
-
Distal phalanx: Hyperechoic lineal interphase under the nailbed
-
Nail Matrix: Ill-defined hypoechoic area that surrounds the proximal nail plate area.
Systematic exploration of echogenicity of skin or appendages must be performed and
reported as changes may indicate disease (broad agreement 8/9, 88.9 %).
Special care should be taken in order to standardize examinations and to ensure that
measurements are performed at the exact same points and with the same parameters in
order to assure reproducibility of the examination (Strong agreement 9/9, 100 %).
3. Ultrasound of skin tumors
3. Ultrasound of skin tumors
Ultrasound examination of the skin is widely used for the assessment of cutaneous
tumors [22]. Even though histological examination remains the “gold standard” for the diagnosis
of oncological skin pathology [23], US can help guide preoperative diagnosis and improve both oncological and aesthetic
outcomes. Furthermore, US plays an important role not only in the therapeutic outcome
after surgical management of skin tumors, but also in the follow-up process [24].
The dermatological diagnosis of a cutaneous tumoral pathology involves clinical examination
and should be confirmed by histopathology if needed (broad agreement 7/9, 77.8 %).
Modern US technology can be successfully and effectively used in the field of skin
oncology, offering particular descriptive information which should be integrated in
the overall examination to achieve a complex evaluation of the nature of the investigated
tumor pathology. Conventional B-mode provides significant morphological data related
to the tumoral lateral and depth extension, relationship to neighboring tissues (involvement
of muscle, cartilage, bone), contour, echogenicity and echo-structure [14]
[22]. The tumor thickness (Breslow histological index) is one of the most important prognosis
factors and establishes the therapeutic strategy especially in cases of melanoma.
The evidence indicates that there is a significant correlation between the sonographic
“depth index” and the histological Breslow index [22]
[23].
The tumor thickness measurement should always be performed in the scan (longitudinal
or transverse) that presents the maximal depth, from the point just beneath the hyperechoic
band of the superficial keratin to the deepest border of the tumor invasion (broad
agreement 8/9, 88.9 %).
Doppler, contrast-enhanced ultrasound and elastography in skin tumors
A color Doppler US examination combined with spectral Doppler US can reveal macro-circulation
at the tumor bed level. The vascular features that may suggest a malignant lesion
include hypervascularization, disorganized blood flow model with peripheral or mixed
distribution, increased blood velocity and multiple vascular pedicles [23]. The lack of evidence of supply vessels in certain cases, however, reveals the limitations
of Doppler US examination, which can be overcome by CEUS, which allows for assessment
of the microcirculation. Analysis of the time-intensity curves during CEUS examination
suggests that the vascular dynamics of the tumor depend on vascular resistance, shunts,
histological type and location. The disposition of the tumor vessels, the uptake pattern
of the contrast agent, the blood flow velocity are parameters that may suggest the
malignant or benign nature of tumors. According to published data, malignant tumors
display an inhomogeneous uptake pattern on a CEUS examination with a significantly
higher value for the washout time. Compared to benign tumors, CEUS allows analysis
of tumoral vascularization from the early arterial to the late venous phase, emphasizing
maximal uptake, wash-up time, duration of passage and distribution pattern in the
area of interest [14]
[23]
[24].
Strain elastography is also a useful examination in the diagnosis of skin cancer.
The qualitative elastography appearance is significantly associated with semi-quantitative
elastography (strain ratio) measurements. Any type of elastography provides information
about tissue stiffness. According to the literature, malignant tumors display a high
or medium increase in stiffness. The stiffness positively correlates with the thickness
of the tumors. The role of elastography in skin tumors has not been subject to active
research. As malignant tumors are stiffer than benign ones, elastography added to
B-mode and color Doppler US examination has the potential to improve the accuracy
of traditional clinical diagnosis [25]
[26].
The use of dermatologic ultrasound as an examination for palpable skin tumors is recommended,
since it offers valuable information regarding tumoral extension, vascularization,
delimitation and degree of compressibility for optimized treatment (broad agreement
7/9, 77.8 %).
3.1 Ultrasonographic aspects of non-melanoma and melanoma skin cancer
Basal cell carcinoma
Basal cell carcinoma (BCC) displays US features such as the presence of hyperechoic
‘dots’ or punctiform hyperechoic areas within the lesion (which correspond to calcium
deposits, keratinized cells or prominent basal cell aggregates), anechoic or hyperechoic
areas (suggestive for cysts, mucin deposits), the presence of two or more vascular
pedicles [23]. The blood flow is more prominent at the inferior aspect of the lesion. Tumor margins
are difficult to assess in cases of morpheaform and infiltrative BCC, although in
most cases BCCs tend to have well-defined borders [28]
[29]. The presence of cutaneous elastosis can on occasion make the exact measurement
of the lesion difficult [24]. Furthermore, the hyperechoic ‘dots’ within the tumor, determined by the presence
of keratin or basal cell nests, can be of use in differentiating a basal cell carcinoma
from melanoma and even different histologic varieties of BCC [29]
[30].
Squamous cell carcinoma
Squamous cell carcinoma (SCC) can present perpendicular shadows determined by superficial
scales or crusts. Hyperkeratosis and the presence of abundant inflammatory infiltrate
may lead to an overestimation of tumor size [22]. SCCs frequently invade deeper structures. Due to the risk of the development of
metastasis, loco-regional lymph nodes should also be evaluated [31]. Regarding the microcirculation pattern, SCCs usually present with two or more vascular
pedicles and have a mixed or peripheral intratumoral circulatory pattern [23]
[24].
Melanoma
Malignant melanoma (MM) usually presents as homogeneous or inhomogeneous, hypoechoic,
with an irregular contour, intense chaotic vascularization (mostly arterial vessels)
[32], two or more vascular pedicles, increased echogenicity of the underlying subcutaneous
tissue, increased or moderate stiffness on elastography [33]. When a melanoma is suspected, it is important to check for satellite lesions, in-transit
lesions and lymph node metastasis [33]
[34].
Other skin malignancies
Skin lymphoma, angiosarcoma, Kaposi sarcoma, adnexal carcinoma and other non-melanoma
skin cancer (NMSC) can also be assessed using US [35]
[36]
[37]. Cutaneous lymphoma may appear either as a nodular or diffuse mass. The nodular
mass appears solid hypoechoic and is poorly defined. The diffuse form appears as a
hyperechoic, poorly defined area with increased thickness of the subepithelial layers.
The thickness or degree of infiltration of cutaneous lymphoma can also be assessed
by US [37]. Moreover, the changes in skin infiltration following therapy can be evaluated by
B-mode US examination and elastography. An angiosarcoma can also have a characteristic
malignant appearance on US examination, appearing as a hypoechoic, poorly defined
lesion with intense vascularization that infiltrates deeper structures [38]. Kaposi sarcoma is seen as a hypoechoic, intensely vascularized plaque or nodule
[35].
As the biology, growth rate and metastasis risk of malignant skin tumors are diverse,
sonographic follow-up should be done according to the normally accepted clinical practice
for skin cancer.
Ultrasound is useful for dermatological tumor follow-up. The frequency and length
of follow-up are based on each tumor type (broad agreement 8/9, 88.9 %).
4. Inflammatory skin diseases
4. Inflammatory skin diseases
Although inflammation of the skin and appendages can usually be accessed by clinical
visual inspection or palpation, some deep processes are difficult to evaluate as they
involve deeper cutaneous structures such as deep dermis and subcutaneous tissue [1]
[8]
[39]. Moreover, skin sclerosing diseases (i. e., morphea, scleroderma, chronic graft
versus host disease) have episodes of inflammatory change, which are difficult to
evaluate, and will require a different therapeutic approach [40]. Therefore, the role of US in these clinical scenarios is to add useful information
to the clinical visual exploration for more accurate patient assessment and staging
[41].
4.1 General inflammatory ultrasound signs in skin diseases
Although there is an immense variety of inflammatory diseases of the skin and appendages,
common shared US findings in inflammatory skin disorders include [39]:
-
Hypoechogenic areas in the subepidermal portion of the dermis
-
Increased local blood flow demonstrated by color Doppler US
-
Hypoechogenic septa and hyperechoic fatty lobules when the subcutaneous tissue is
affected
These features help to determine the level and extent of the changes in inflammatory
disorders of the skin, hair, and nails [41].
With inflammatory diseases of the skin and appendages, the level and extent of inflammation
should be assessed and reported as it may influence treatment (broad agreement 8/9,
88.9 %).
4.2 Skin ultrasound in infectious diseases
Ultrasound can be used to assess the extent of plantar warts and to monitor treatment
response in human papillomavirus infections [42]. Ultrasound assessment of abscesses has also become widespread in emergency departments
in the United States. Ultrasound evaluation in the pediatric emergency department
can alter the treatment strategy (drainage vs. no drainage) in15 % of cases evaluated
by physical examination alone [43]. An additional advantage of US in the diagnosis of abscesses is that it can be performed
with minimal point-of-care training [44].
Ultrasound is useful in evaluating and detecting subclinical subcutaneous abscesses
in the emergency department. Ultrasound equipment and trained personnel are recommended
for this kind of evaluation (broad agreement 7/9, 77.8 %).
Psoriasis
Ultrasound characteristics of psoriasis include epidermal and dermal thickening and
subepidermal hypoechoic areas with increased blood flow on color Doppler US. These
US findings, and in particular, dermal thickness, have been found to be correlated
with disease severity measured using the Psoriasis Area Severity Index and other scales
assessing the severity or extent of disease [45]
[46]. In a multicenter study by the Spanish Rheumatology Society, high-frequency US evaluation
showed a reduction in plaque thickness and Doppler signal intensity in the dermis
of patients treated with infliximab [47]. Psoriatic nails appear thicker and irregular mainly on the ventral aspect of the
nail plate in comparison with healthy nails or nails affected by other diseases (atopic
dermatitis, mycoses) [48]
[49]. Nail disease in psoriasis has been correlated with the presence of enthesopathy
and psoriatic arthritis, even in the absence of clinical signs. Therefore, with clinically
inconclusive signs of a psoriatic onychopathy, US may add useful information [50]
[51]
[52].
In patients with suspected psoriatic arthritis, US findings of psoriatic onychopathy
can support the diagnosis of psoriasis (strong agreement 9/9, 100 %).
Hidradenitis suppurativa
Hidradenitis suppurativa is a predominantly dermal and subcutaneous inflammation that
can be assessed in detail by US. Comparing epidermal and dermal thickness in patients
with hidradenitis and healthy controls, Wortsman et al. found that areas of the body
affected by hidradenitis exhibited an increased dermal-epidermal thickness, areas
of lower echogenicity, formed by pseudo-cysts, fistulous tracts and fluid collections
that allowed US diagnosis of hidradenitis suppurativa [53]
[54].
In a multicenter study ultrasound better assessed hidradenitis suppurativa patients
than clinical inspection alone, resulting in upstaging of most patients as a consequence
of the identification of occult and deep fistulous tracts, previously considered to
be part of an inflammatory nodule [55].
Ultrasound is recommended for supporting diagnosis, staging and treatment monitoring
in hidradenitis suppurativa treatment (strong agreement 9/9, 100 %).
Collagenosis
Scleroderma is the collagenosis disease most widely studied by US, as treatment varies
according to the stage of disease (inflammatory or sclerotic). In a study of 104 morphea
plaques in 59 patients, Wortsman et al. [56] showed that US had a sensitivity of 100 % and a specificity of 98.4 % for differentiating
between the inflammatory and the sclerotic phases. In the same study, US detected
subclinical inflammation in five patients with Parry-Romberg syndrome. Attempts have
been made to standardize these results to create semi-quantitative scales to assess
the effectiveness of treatments [57]. With respect to scleroderma ulcers, inflammation and superinfection can also be
assessed by US as increased vascularization is evidenced on color Doppler US [58]. Calcinosis associated with scleroderma and dermatomyositis can also be detected
and evaluated by US [58]
[59]. Recently shear wave elastography evaluation of scleroderma patients has been confirmed
to be useful for the evaluation of generalized scleroderma patients [60].
Ultrasound is recommended for supporting diagnosis, activity assessment and follow-up
in scleroderma/morphea patients (broad agreement 8/9, 88.9 %).
5. Aesthetic dermatologic ultrasound
5. Aesthetic dermatologic ultrasound
The number of aesthetic procedures has been increasing explosively worldwide over
the last decade, and most of these techniques are performed blindly, sometimes in
different institutions and by operators with variable levels of training from medical
and non-medical backgrounds. Moreover, patients may forget or be unaware of the type
of treatment that they received [61]
[62]. Thus, anatomical information can be challenging to obtain, but is critical for
management and outcome in aesthetic medicine, where good results are the goal, and
scars and complications are unwanted. The use of US is expanding in aesthetic medicine
since US can provide relevant information that includes data on facial anatomical
variants, the type, location and extent of common cosmetic fillers, the identification
of implants, the complications of lipolytic procedures, and the possibility of percutaneous
US guidance for the procedure [62]
[63].
5.1 Main indications for ultrasound in aesthetic medicine
1– Assessment of photoaging
Ultrasound can detect and measure signs of photoaging caused by prolonged exposure
to the sun through the observation of the subepidermal low echogenic band (SLEB) which
is produced by the deposit of glycosaminoglycans in the papillary dermis (upper dermis)
[64].
Ultrasound is recommended as a valuable tool to detect and quantify photoaging (broad
agreement 8/9, 88.9 %).
2– Recognition of relevant anatomical data
Anatomical variants in vessels, muscles or glands, measurement of the thickness of
skin layers and the assessment of blood flow in complications are relevant for planning
or managing cosmetic techniques and complications. Moreover, the face, the most common
corporal region for cosmetic procedures, presents a complex anatomical structure where
the skin layers are thinner in comparison to other body regions, and any abnormality
is highly visible [65]
[66].
Ultrasound is recommended as a valuable tool for evaluating facial anatomical structures
in subjects before and after aesthetic procedures (broad agreement 7/9, 77.8 %).
3– Management of cosmetic fillers
Ultrasound allows for the detection and identification of common cosmetic fillers
as well as the assessment of their location and extent and potential complications.
These fillers include deposits such as hyaluronic acid, polymethylmethacrylate, silicone
(pure or oily forms), calcium hydroxyapatite, polyacrylamide, and polycaprolactone
that are approved by the Food and Drug Administration (FDA) and European Union Medical
Agencies as well as those that are not approved. Percutaneous US guidance of the injection
of hyaluronidase has also been reported in the management of hyaluronic acid complications
[67]
[68]
[69].
4– Detecting implants and their complications
Ultrasound can support the detection of organic and synthetic implants and their complications.
Examples of organic implants are fat, cartilage and bone grafts. Examples of synthetic
implants are pure silicone, polyethylene, and polydioxanone (e. g. tensor threads).
Complications of implants include an excessively superficial location, extrusion,
chronic inflammatory and fibrotic reactions as well as rupture [62]
[65]
[69]
[70]
[71].
Ultrasound is recommended as a valuable tool to detect and identify common types of
cosmetic fillers and organic or synthetic implants and is recommended in the management
of their complications (strong agreement 9/9, 100 %).
5– Detection of complications of lipolytic procedures
The goal of these procedures is to decrease the amount of hypodermal fatty tissue
using techniques that generate inflammation and liquefaction of the fat. These procedures
include radiofrequency, mesotherapy or cryolipolysis. Ultrasound can provide anatomical
information for planning these techniques, detect the extent and location of the inflammatory
changes and may serve as a monitoring technique for the assessment of the outcomes
or the management of potential complications [62]
[72].
Ultrasound is a valuable tool to support planning and detection of anatomical changes,
assessment of outcomes and management of complications of lipolytic procedures (strong
agreement 9/9, 100 %).
6– Detection of complications of surgical aesthetic procedures
Ultrasound can detect complications of cosmetic or plastic surgery procedures, such
as dermal and hypodermal edema, lymphedema, seromas, hematomas, abscesses, fistulous
tracts, fat necrosis, granulomas and loose sutures [62]
[65].
Ultrasound is recommended for the evaluation of plastic surgery procedures and their
complications (broad agreement 7/9, 77.8 %).
7– Percutaneous ultrasound guidance of non-surgical and surgical aesthetic procedures
Percutaneous ultrasound guidance of aesthetic or plastic surgery procedures can improve
the precision of injections, drainage procedures and corrections and decrease potential
adverse reactions or complications due to injury to neighboring structures [73]
[74].
Percutaneous ultrasound guidance of non-surgical and surgical aesthetic procedures
is recommended as it increases precision and decreases the potential for unwanted
effects or neighboring injuries (strong agreement 9/9, 100 %).
6. Professional requirements, reports and training and accreditation in dermatologic
ultrasound
6. Professional requirements, reports and training and accreditation in dermatologic
ultrasound
6.1 Standard professional practical issues
Operators should be trained in US imaging and have knowledge of dermatologic pathologies
to be able to better perform and interpret examinations [1]
[2]
[3]. Regarding the certification required to perform dermatologic US, a physician (not
a sonographer) should be the person in charge of performing examinations. The main
reason for this statement is that the clinical dermatologic diagnosis must be determined
by the operator and that is not within the scope of non-physician operators [2]. Regarding the number of examinations performed during training and competence maintenance,
the DERMUS guidelines, based on expert opinion, suggest a minimum of 30 supervised
examinations for assessing competence and a minimum of 300 examinations per year for
competence maintenance [3].
Dermatological US should be performed by an adequately trained physician with knowledge
of both clinical and sonographic dermatology (strong agreement 9/9, 100 %).
6.2 Dermatologic ultrasound examination reporting
A written report of the findings has to be produced following dermatological US. A
standardized report of the US examination is recommended and images should be kept
together with the report, ideally on a computer-based picture archiving system (PACS)
and electronic patient notes (EPR). Documentation of the exact anatomical position
of US findings, for example using anatomical position markers or text within the images
describing the location of the finding, is also recommended. Dermatologic US examinations
should be correlated with the clinical and histologic results [2]
[75]. Coordinated interdisciplinary collaboration among the physicians involved in dermatological
diagnosis and treatment, i. e., radiologist, dermatologist, plastic surgeon, and pathologist,
is desirable.
A written report must be provided after a dermatologic US examination. High quality
images should be recorded, stored and made available for follow-up examinations (broad
agreement 8/9, 88.9 %)
6.3 Dermatologic ultrasound education
Theoretical and practical educational courses are needed to improve the performance
and interpretation of dermatological US [3]. Two different course models should be organized to provide a minimum of two levels
of complexity: basic and advanced. Educational course length should be a minimum of
two days: theory (one day) and practical training (one day). One experienced instructor
per five participants is recommended for the practical part of the course [3]
[76]
[77]. Educational courses should include US-guided interventions (biopsies, injections,
ablations) of dermatological lesions. Courses should be accredited by EFSUMB or any
other national ultrasound society that is part of EFSUMB or a dermatological scientific
society.
Basic courses on dermatologic US should be both theoretical and practical with a minimum
of two days of training. Clinical images should be available for training since clinical-sonographic
correlation is key in this application (broad agreement 8/9, 88.9 %).
Ongoing practice is encouraged in order to maintain skills and competence. Ultrasound
information should be integrated with clinical and histopathological data (strong
agreement 9/9, 100 %).
