From sonar to ultrasound examination of the skin - development and characterization of the method

The development of aesthetic medicine and cosmetolo - gy procedures has resulted in an increase in the number of complications and adverse events. Specialists performing ex - ertions in this area more and more often raise the necessi - ty of better and more reliable skin diagnostics at the highest available level, which contributes to the safety of treatments as well as reduces the number of complications. A diagnos - tic method that allows objective and non-invasively images of individual layers of the skin is high-frequency ultrasound. The aim of the study was to present the current scope of knowledge on ultrasound examination of the skin based on the available literature. Subsequently, the development of the method, the physical basis for the formation of the ultra - sound image, the types of apparatus and probes used in skin examinations, the ultrasound image of the skin, and the pa - rameters that can be assessed are discussed. As the analysis of the literature and the authors' own ex - perience showed, high-frequency ultrasound examinations in the field of aesthetic medicine and cosmetology may find a wider application.


INTRODUCTION
In recent years, very dynamic development of aesthetic medicine and cosmetology have been observed.The value of this market is constantly growing.In 2018 it was valued at 52.5 billion USD, and in 2021 at 99.1 billion USD.In the following years, a steady increase of 14.5% per year is forecast [1].Along with the growing value of this market, the number of performed procedures is rising, and as a consequence, the number of postoperative complications observed is also increasing.
Currently, in most cosmetology and aesthetic medicine clinics, skin diagnostics, and thus treatment planning, is based mainly on visual assessment of the skin and palpation.Devices for measuring skin hydration, lubrication, or elasticity are relatively rarely used, although they are also subjective methods, requiring the maintenance of repeatable test conditions [2,3].Besides, they are limited only to the surface of the skin.Ultrasonography (USG) allows visualizing the skin in a non-invasive, safe way.At the same time, it is an objective method that can be used for diagnostic purposes, during procedures, as well as in the long-term assessment of the effectiveness of conducted therapies [4,5].The interest in skin ultrasonography and its use in cosmetology, aesthetic medicine, and dermatology is constantly growing, but many specialists still do not know its full possibilities and applications.

DEVELOPMENT OF SKIN ULTRASONOGRAPHY
The origins of ultrasonography can be traced back to the construction of sonar, which took place at the beginning of the 20th century.One of the first to use ultrasound in medicine was the neurologist and psychiatrist Karl T. Dussik, who evaluated brain tumours (Fig. 1) [6].
In the following years, much better devices were constructed, and ultrasound examinations became popular in many fields of medicine.During this period, attempts were also made to perform ultrasound imaging of the largest organ of the human body, which is the skin.Unfortunately, many of these trials ended in failure, because the devices equipped with heads with too low frequency were used and it was not possible to obtain an image of the skin [8].It became possible only after the introduction of heads with higher frequencies -above 10 MHz.The first article on ultrasound imaging of the skin was published in 1979, and the authors, Aleksander and Miller, attempted to assess skin thickness using a 15 MHz transducer [9].In the following years, new devices appeared that used heads with frequencies of 20-25 MHz [9].In the late 1990s, Yano and his co-workers developed an ultrasound scanner equipped with a 40 MHz transducer [11].At the turn of the 1980s and 1990s, research work was carried out mainly in Germany, Denmark, and Italy and focused on the assessment of healthy skin as well as skin affected by diseases (e.g.scleroderma) and the assessment of skin tumours.Pioneering studies on ultrasound imaging of melanoma were also conducted [12].
In Poland, work in this field began in the 1990s, the research was conducted mainly in the following centers: Warsaw, Wrocław, and Katowice.Probably the first Polish article on skin ultrasonography was published in 1995 by Pierzchała and Rubisz-Brzezińska [13].A significant contribution to the development of Polish ultrasound research was made by the work carried out at the Ultrasound Department of the Institute of Fundamental Technological Research (IPPT) of the Polish Academy of Sciences (PAN) under the supervision of prof.Andrzej Nowicki, who together with his team developed the first Polish apparatus for skin testing.Research conducted with this device resulted in the first Polish article published in a foreign journal in 2000 [14].In the 21st century, with the dynamic development of technology, cameras became more and more available, and thus the number of reports in this field increased.Over the last 20 years, Polish researchers have published works on the use of ultrasonography in dermatology [15][16][17] (monitoring the treatment of scleroderma, atopic dermatitis, psoriasis, basal cell carcinoma, cavernous angiomas in children, seborrheic warts) as well as in aesthetic medicine and cosmetology [18,19].
Currently, in Poland and around the world, research on skin ultrasonography is underway in many centers, which is confirmed by the number of published reports.According to the data obtained from the PubMed database, after entering Fig. 1 The first attempts at ultrasound imaging of brain tumours were undertaken by Karl T. Dussik Source: [7].
the search term "skin high-frequency ultrasound", the number of scientific papers is constantly increasing.In 1978, two articles were published, in 2000 -14, in 2010 -53, and in 2021 -166 (Fig. 2).
The subject of these studies gathers around two axes: dermatology and broadly understood aesthetic medicine and cosmetology.The expansion of this field is also manifested in the development of equipment that can be used in research.The number of devices for skin testing available on the market is constantly growing.The first ultrasound device for skin examination was produced in Poland 10 years ago.Manufacturers are continuously improving devices, introducing new solutions that increase diagnostic capabilities.
Considering the dynamic development of skin ultrasonography in recent years, it can be assumed that this method has a chance to become more popular.

ULTRASONOGRAPH OPERATION -PHYSICAL BASIS
Ultrasound is used to visualize the tissues and organs of the human body.These are mechanical waves with a frequency greater than 20,000 Hz, and therefore are inaudible to humans, because the human ear perceives sounds in the range of 20-20,000 Hz.In typical medical diagnostics, for imaging abdominal organs, or in gynecology, waves in the range of 2,000,000-15,000,000 vibrations per second (2-15 MHz) are used, while in ophthalmology and skin diagnostics waves are used with higher vibration ranges reaching even 80-100 MHz [20,21].Ultrasonic waves have a number of specific properties, and the characteristic feature is the ability to propagate only in material media.If the ultrasonic wave reaches the boundary of two media with diff erent acoustic impedance, in which the acoustic impedance is a standard of the resistance of the center to the ultrasonic wave propagating in it, its energy will be divided.Some will be refl ected, refracted, absorbed, attenuated, and some will pass to the next medium.How much of the wave will be, for example, dispersed, refl ected, or absorbed, depends on the type of medium through which the wave passes.At the boundary formed by a solid-gas or liquidgas, the acoustic waves will not penetrate deeply but will be completely refl ected.Moreover, there is the phenomenon of wave refl ection, also called echo, arising at the border of two media with diff erent acoustic properties, which is the most important, because the measurement of the refl ected echo is the basis of imaging.
It should also be remembered that the depth to which the ultrasonic wave can penetrate is limited.In ultrasound examinations of the skin, it is crucial to determine the relationship between the frequency of ultrasonic waves and their attenuation in tissues.With the increase in the frequency of the ultrasonic wave, their attenuation is greater, which in turn translates into the depth of their penetration, and decreases with the increase in frequency.Therefore, it is necessary to use high frequencies in skin examinations, because only then is it possible to assess the skin.This principle results in the fact that in the examination of the abdominal cavity, the organs of which are located deep, we use transducers with a frequency of 3.5 MHz, and in the examination of superficial skin, transducers with a frequency of about 20 MHz to 100 MHz.
The ultrasound apparatus consists of a head, also called a probe, a computer with a monitor on which the image of the selected tissue or organ is visible.The most important element of each device is the ultrasound head, in which there are piezoelectric transducers, thanks to which the heads are both emitters and receivers of ultrasonic waves.According to the piezoelectric phenomenon discovered in 1880 by Pierre Curie, when an alternating electric field is applied, the transducer begins to emit acoustic waves of a certain frequency.These waves penetrate the tissues, are dispersed and absorbed, and reflecting from various centers, they generate the so-called echo.The echo, after passing through the head, reaches the transducer, causing electric charges to appear on its surface.They are then analyzed, processed, and converted into an image visible on the screen using algorithms.The information returned in the form of an echo to the head can be obtained in several presentations.In most medical and skin research, the B presentation is used, the name of which is derived from the English word brightness.In presentation B, the ultrasound echo is converted into glowing points (spots) on the screen of the ultrasound machine.In the ultrasound image, the picture of the acoustic properties is reproduced using a grayscale in its various shades -from black in the absence of an echo to white in the case of a very large echo.Typically, ultrasound machines use a 256-degree grayscale [20,21].
When discussing the basics of ultrasound, Doppler ultrasound cannot be omitted.Although it is mainly used in the diagnosis of circulatory diseases, there are more and more studies showing the usefulness of this method in skin examinations [22].In the Doppler examination, changes in the frequency of ultrasonic waves reflected from moving blood cells are analyzed, thanks to which it is possible to determine the speed and direction (to/ from the transducer) of blood flow [20,21].

APPARATUS AND HEADS USED IN SKIN USG EXAMINATIONS
For the examination of the largest organ of the human body, which is the skin, we use two types of ultrasound devices in practice: classic devices common in medical examinations. of the abdominal cavity or in gynecology, and high-frequency devices intended for a skin examination.The basic criteria for the division into classic and high-frequency devices for skin examination are frequency and type of transducer which will be discussed in the article.
Regardless of the type of device used, according to the guidelines of the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB), the minimum frequency of the transducer for skin examination should be 15 MHz -examination using high frequencies.Transducers with a frequency > 20 MHz are called very high-frequency transducers, while 30-70 MHz are classified as ultra-high frequency transducers, which enable the examination of small structures, and appendages, such as sebaceous glands [23].
If an examination is performed with a classic apparatus, then it is necessary to use an electronic linear transducer with a frequency of about 15 MHz, built of crystals (Fig. 3), although much better images are obtained using transducers with a frequency of about 20 MHz.Currently, many manufacturers of ultrasound scanners offer linear transducers with frequencies of 18 MHz and even 22 MHz.The best images of the skin are obtained on high-end ultrasound scanners, which have many options to improve imaging.The disadvantage of classic cameras, however, is their high price and their large size.In the last few years, mobile cameras have been introduced as an alternative to huge, classic cameras that allow performing tests after connecting the head to a tablet or even a smartphone, but they do not have all the options that are available in large cameras (Fig. 3) [24,25].
As described, the apparatuses intended for skin examination are called high-frequency devices, because they are equipped with transducers with a frequency above 20 MHz.These are one-piece mechanical heads that can have a frequency of 20 to 100 MHz (Fig. 3).Currently, there are several manufacturers of this type of camera on the market.All devices known to the authors of this article are small and easy to carry [23,24].
Both in classic devices and in most high-frequency ultrasound scanners, images are obtained in the B presentation in grayscale.In some high-frequency apparatuses, it is possible to select a scale other than grayscale.

A -linear transducer B -mechanical transducer
It is impossible to unequivocally decide which device is better for skin diagnostics.The choice of ultrasound machine depends on the purpose of the examination and the structures to be imaged.

ULTRASONOGRAPHIC IMAGE OF HEALTHY SKIN
The ultrasound image of healthy skin, regardless of the type of the device, shows three basic layers [18,24,26] (Fig. 4): 1) epidermis -light, thin line; 2) dermis -heterogeneous structure, in which lighter (hyperechoic) refl ections from collagen fibers and darker (hypoechoic) refl ections from the extracellular matrix can be observed in the lower part.In this layer, small blood vessels, hair follicles, and glands can also be visualized; 3) subcutaneous tissue -made of darker refl ections coming from adipose lobules and lighter, linear refl ections from connective tissue fibers.Depending on the type of ultrasound used for the examination, the upper part or all of the subcutaneous tissue can be captured.In addition to the three layers of skin described, some images also show a dark band located between the epidermis and the dermis.It is a subepidermal anechoic or low echogenic band (SLEB, subepidermal low echogenic band, otherwise referred to as SENEB, subepidermal non-echogenic band) (Fig. 5).Most often, SLEB occurs in areas of the body exposed to intense sunlight and therefore is treated as a marker of skin photoaging [27,28].

ASSESSMENT OF ULTRASOUND IMAGES -PARAMETERS TO BE ASSESSED
The skin images obtained during the examination are subject to both quantitative and qualitative analysis.Qualitative analysis is performed by one or more researchers and consists of a visual assessment of the image and possibly comparing images from the same location, but taken at diff erent times.
Quantitative analysis is determining specific parameters by taking measurements.Currently, all ultrasound scanners enable the assessment of the thickness of the epidermis, dermis, subcutaneous tissue, SLEB, or other assessed.Taking thickness measurements, especially of such thin structures as the epidermis, is subject to a high risk of making a measurement error, which is why some high-frequency ultrasound scanners have introduced the possibility of automatic measurement (Fig. 6).
The measurement of the surface area is also very useful and can be used depending on the purpose of the examination, for instance, to measure the surface area of subcutaneous tissue bands growing into the dermis, which is the case with cellulite.Some of the high-frequency devices have the option of measuring pixels assigned to a given degree in grayscale, thanks to which it is possible to observe changes in the echo structure of tissues [24].On the other hand, classic highquality devices also allow the assessment of blood flow and tissue stiff ness (hardness) and their susceptibility to deformation using the elastography option [29].The latest novelty is the introduction of the MicroFlow fl ow imaging option, which allows the detection and assessment very slow and weak blood fl ow even in small vessels, which was not possible before [30].
Fig. 6 Ultrasound thickness measurements.A -manual measurement of the thickness of the epidermis and dermis using an ultrasound scanner with a 50 MHz mechanical probe, B -manual measurement of the thickness of the dermis using an ultrasound scanner with a 48 MHz mechanical probe, C -automatic measurement of the thickness of the epidermis using an ultrasound scanner with a 48 MHz mechanical probe, D -manual measurement of subcutaneous tissue using an ultrasound scanner classic.Source: Authors' own compilation.

SKIN USG TECHNIQUE
Conducting an ultrasound examination of the skin is similar to the technique of performing classic ultrasound examinations.In the case of the skin, however, structures much smaller than internal organs are imaged, so it is important to perform the examination in exactly the same place, especially when the obtained results are to be compared over different periods of time.In addition, when imaging the skin, a large amount of gel should always be applied, producing the so-called "gel pillow".Alternatively, ready-made ultrasound spacers can be used.The ultrasound transducer should be held just above the gel pad and should not be in direct contact with the skin.Therefore, the examined person should be placed in a supine position, and the person performing the examination should have a supported hand in which they hold the transducer.It is also important to make small movements of the head on the skin, literally by a few millimeters.

SUMMARY
Ultrasound examination of the skin allows for safe and reliable imaging of its basic layers.Therefore, it can be used to diagnose the skin, plan therapies in the field of cosmetology and aesthetic medicine, as well as monitor the course of the procedure in real-time and evaluate the effectiveness of the undertaken therapies.Considering that currently aesthetic medicine and cosmetology do not have a method that would enable performing all the above-mentioned activities, ultrasound has a chance to become popular and be present in every beauty salon.The limitation that has so far slowed down the dissemination of ultrasonography in the field of cosmetology and aesthetic medicine was the high price of ultrasound devices.However, taking into account the technological development and the introduction of mobile classic devices for sale, the price of which is several times lower compared to stationary ultrasound scanners, it can be assumed that this barrier will soon be eliminated.The authors of the article see a greater threat to the dissemination of ultrasonography than the price of the equipment in the acquisition of knowledge and competence to perform examinations, as it is a method that cannot be mastered in a short time.

Fig. 2
Fig. 2 Increase in the number of scientific publications on high-frequency ultrasound of the skin in the years 1978-2021 based on data from the PubMed database.Source: Authors' own study.

Fig. 3
Fig. 3 Ultrasound transducers used in skin examinations.A -multi-element linear transducer used in classic devices operating in the 4-12 MHz range, Bsingle-element mechanical transducer used in ultrasonographs for skin examinations with a frequency of 35 MHz.Source: Authors' own study.

Fig. 5
Fig. 5 Ultrasound imaging of the SLEB de-echogenic band (yellow arrows).A -high-frequency ultrasound scanner with a 50 MHz mechanical transducer, B -high-frequency ultrasound scanner with a 48 MHz mechanical transducer Source: Authors' own study