Net Study Ultrasonographic assessment of skin structure

according to age

Diana Crisan, Monica Lupsor1, Andreea Boca2, Maria Crisan3, Radu Badea4

Student, Departments ABSTRACT

of 1Ultrasonography,
2
Pharmacoloy, 3Histology, and Background: High-frequency ultrasound is a noninvasive tool that offers characteristic
4
Ultrasonography, University
of Medicine and Pharmacy markers, quantifying the cutaneous changes of the physiological senescence process.
“Iuliu Hatieganu,” Cluj-Napoca, Aims: The aim was to assess the changes in skin thickness, dermal density and echogenicity,
Romania as part of the ageing process, with different age intervals. Methods: The study was performed
on 160 patients, aged 40.4 ± 21.2, divided into four age categories: <20, 21-40, 41-60, 61-80.
Address for correspondence: Ultrasonographic images (Dermascan device) were taken from three sites: dorsal forearm
Dr. Maria Crisan, (DF), medial arm (MA), zygomatic area (ZA). We assessed the thickness of epidermis
Department of Histology/
Dermatology, UMPh Iuliu
and dermis (mm), number of low, medium, high echogenicity pixels, the ratio between the
Hatieganu, Cluj-Napoca, echogenicity of the upper and lower dermis (LEPs/LEPi), and SLEB (subepidermal low
Romania echogenicity band). The statistical analysis was performed using SPSS 15.00. A P value
Email: <0.05 was considered significant. Results: On all examined sites, it was found that the dermal
[email protected] thickness increases in the 21 to 40 year interval (P<0.0001). After the 21 to 40 year interval,
the number of low echogenic pixels increases significantly, especially on photoexposed sites.
High-echogenic pixels follow the same pattern on all examined sites: they increase in the 21 to
40 year interval and decrease in the 3rd and 4th age category. The LEPs/LEPi ratio increases
significantly with age, at all sites (P<0.05), due to an increase of hypoechogenic pixels in the
upper dermis. Conclusions: High-frequency ultrasound is a noninvasive “histological” tool
that can assess the cutaneous structure and age-related changes. It offers imagistic markers,
comparable to the histological parameters and also characteristic ultrasonographic markers.
Histology remains the gold standard for the investigation of the integumentary system.

Key words: Aging, echogenicity, high-frequency ultrasound

INTRODUCTION It also represents an important research tool for the

characterization of skin properties with different age
High-frequency ultrasound is a new, noninvasive intervals, allowing the establishment of an imagistic
method that allows an “in vivo assessment” of aging model of the integumentary system.[2] The use
the physiological and pathological aspects of the of high-frequency ultrasound in dermatology allows
integumentary system.[1] It represents a more desirable a clear identification of the skin layers (epidermis,
and less emotionally involving alternative to skin dermis, subcutis) and thus tissue assessment. At
biopsy, routinely used in the dermatological field. frequencies above 10 MHz, it was proven that the
technology provides enough resolution to characterize
Access this article online
microstructures.[3-5]
Quick Response Code: Website:
www.ijdvl.com
Cutaneous aging is a complex, biological phenomenon,
DOI:
divided into two components: intrinsic and extrinsic
10.4103/0378-6323.98096
aging.[6] Extrinsic aging is caused by environmental
PMID: exposure, mainly to UV rays, and is more commonly
*****
termed photoaging. On photoexposed sites of the

How to cite this article: Crisan D, Lupsor M, Boca A, Crisan M, Badea R. Ultrasonographic assessment of skin structure according to age.
Indian J Dermatol Venereol Leprol 2012;78:519.
Received: October, 2011. Accepted: April, 2012. Source of Support: Nil. Conflict of Interest: None declared.
Crisan, et al. Ultrasonographic assessment of skin

skin, aging involves changes in cellular biosynthetic was performed with a 20 MHz high-frequency
activity that leads to important disorganization of the Dermascan C device (Cortex Technology, Denmark),
dermal matrix.[7] Intrinsic aging, the natural aging that allows the “in vivo” acquirement of cross-sectional
process, is genetically determined and represents images of the skin (B mode) up to 2.5 cm in depth.[10]
an inevitable change attributable to the passage of
time, characterized by physiologic alterations of the The device consists of a transducer, an elaboration
skin structure. In human dermis, intrinsic aging is system, and a data storing system. The ultrasonic wave
characterized by three features: dermal atrophy due to is partially reflected at the boundary between adjacent
collagen loss, degeneration in the elastic fiber network, structures and generates echoes of different amplitudes.
and loss of hydration.[8] The intensity of the reflected echoes is evaluated by
a microprocessor and visualized as a colored two-
High-frequency ultrasound allows, as the senescence dimensional image.[10] The color scale of echogenicity
process progresses, the identification of variations in is: white-yellow–red–green–blue–black. On a normal
both skin thickness and echogenicity. The extracellular cutaneous image, the epidermal echogenicity appears
matrix changes, consisting of variations in dermal as a white band, the dermis is expressed as a two color
density and echogenicity throughout the physiological composition: yellow and/or red, and the subcutaneous
senescence process, can easily be identified with the layer appears either green or black [Figure 1a].
use of high-frequency ultrasound.[9]
The ultrasonographic images are saved and processed
The purpose of the study is to identify, investigate, and with specific image analysis software (Dermavision,
characterize the specific ultrasonographic changes of Cortex Technology), that has a certain property: the
the cutaneous structure related to different intervals of amplitudes of the echoes of the pixels are given as a
age and degree of photoexposure.
value on a numerical scale that ranges from 0 to 255. On
this scale, the low-echogenity pixel area corresponds
METHODS
to the 0–30 interval, the medium echogenity pixels to
50–150, and the high echogenity pixels to the 200–255
Patients
interval.[11]
The study was performed during July-October 2011
(Dermatology Clinic, Cluj-Napoca, Romania) on 160
The gain curve was adjusted to a value of 20 dB,
subjects, with a mean age of 40.4 ± 21.2 (STDEV), 50%
whereas the speed of ultrasound at tissue level was of
male and 50% female, divided into four age categories,
each category with 40 subjects: <20 , 21-40, 41-60, 61- 1580 m/s. The ultrasonographic gel was applied on the
80 years. aperture of the ring of the transducer, which was placed
perpendicularly to the skin surface for the acquirement
All subjects were submitted to an ultrasonographic of the cross-sectional image. The scanning of the skin
evaluation, consisting of the acquirement of was performed on two photoexposed sites of the skin
ultrasonographic images from three sites: dorsal (DF and ZA) and on a photoprotected one (MA).
forearm (DF), medial arm (MA), and zygomatic area
(ZA). The dorsal forearm (DF) and zygomatic area (ZA) For every subject, we assessed the thickness of the
sites were chosen as prototypes of photoexposed areas, epidermis and dermis (mm), the number of LEP (low
where the dynamics of the extrinsic aging process can echogenic pixels), MEP (medium echogenic pixels),
be assessed. The ultrasonographic study of the medial HEP (high echogenic pixels), SLEB (subepidermal low
arm (MA) site, a photoprotected area, allowed the echogenicity band), LEPs/LEPi ratio (number of low
dynamic study of the intrinsic aging process. echogenic pixels in the upper dermis/number of low
echogenic pixels in the lower dermis). The thickness of
The study was approved by the ethical committee. the epidermis was obtained by establishing the mean
Every subject was informed about the nature and of three measurements performed in A-mode at three
purpose of the study, and signed an acceptance form different sites of each image (the two extremities of
before enrolling into the study. the analyzed image and the center of the image). The
thickness of the dermis was obtained in the B-mode, by
Ultrasonographic evaluation measuring the distance between the dermo-epidermal
The ultrasonographic assessment of the integument and the dermo-hypodermic junction at the same three
Crisan, et al. Ultrasonographic assessment of skin

Figure 1a: Ultrasonographic aspect of normal skin (Dermascan Figure 1b: Subepidermal low echogenicity band (SLEB)
device, Cortex Technologies)

different sites and by establishing the mean of the (0.157±0.022 to 1.178±0.038 mm, P=0.035). It can
three values. By selecting a certain interval from the also be noticed that the epidermis tends to decrease
0-255 pixel scale, we obtained values corresponding after the age of 60 on photoexposed sites (DF, ZA), and
to the low, medium- and high-echogenic pixels, to increase on photoprotected ones (MA).
present in the analyzed image. SLEB was defined as a
well delimited, subepidermal low echogenicity band The thickness of the dermis shows certain variations.
(0- 30), situated in the upper dermis, mainly present on
On all examined sites, the dermal thickness increases
photoexposed sites[12] [Figure 1b].
in the 21- to 40-year interval. At facial level, from
a mean of approximately 1.339±0.329 mm in the
Additionally, the LEP were quantified separately in <20-year interval, the dermis reaches a value of
the upper (LEPs) and lower (LEPi) dermis. To separate 1.689±0.343 mm for the subjects taking part in the
the two areas, we drew a parallel line to the epidermal >60-year interval (P<0.0001). Generally, the dermis
entrance echo, dividing the dermis into two equally increases from the 0- to 20- to the 21- to 40-year
thick parts. The ratio of the LEP number in the upper intervals and decreases slightly in the 41-60 interval.
and lower dermis (LEPs/LEPi) was calculated.

Statistical analysis Generally, considering the total thickness of the

The data we obtained were statistically assessed, based integument, a significant increase may be noticed
on the ANOVA and Student T test, using the SPSS especially at facial site (P<0.0001). Also, comparing
program version 15.0 (SPSS Inc., Chicago, IL, USA). the two extreme age intervals, 0-20 and 61-80, we
We evaluated the differences between values referring can notice that the integument is thinner in the 61-
to different intervals of age at the three examined sites. to 80-year interval at the level of dorsal forearm, has
A P value <0.05 was considered significant. comparable values on the medial arm and increases at
facial level.
RESULTS
Assessment of low, medium, and high echogenicity
Epidermis and dermis thickness pixels
The obtained data concerning the epidermis and The number of hypoechogenic pixels shows a
dermis thickness show different values for the four significant variation in the case of all three examined
intervals of age taken into study [Table 1]. sites: hypoechogenic pixels decrease significantly
on the dorsal forearm in the 21- to 40-year interval
The thickness of the epidermis remains at similar compared to the 0-20 interval (9642.22±3672 vs.
values on all examined sites, except for the epidermis 11240.29±4379, P<0.05) and increase significantly in
from DF level, where a significant increase is noticed the 61-80 interval. At medial arm level, hypoechogenic
between the 21- to 40- and 41- to 60-year intervals pixels increase significantly from the 21- to 40-year
Crisan, et al. Ultrasonographic assessment of skin

Table 1: Mean epidermal and dermal thickness in mm (±SD) on four age intervals, at three examined sites: dorsal forearm, medial
arm and zygomatic area
Age interval
<20 21-40 41-60 61-80
Investigated area DF Epidermal thickness (mm) 0.175±0.033 0.157±0.022 0.178±0.038 0.171±0.037
Dermal thickness (mm) 1.209±0.272 1.279±0.294 1.256±0.230 1.220±0.223
MA Epidermal thickness (mm) 0.155±0.030 0.162±0.121 0.157±0.040 0.177±0.043
Dermal thickness (mm) 0.908±0.165 0.924±0.159 0.884±0.135 0.941±0.209
ZA Epidermal thickness (mm) 0.137±0.036 0.157±0.163 0.145±0.075 0.136±0.028
Dermal thickness (mm) 1.339±0.329 1.608±0.283 1.468±0.370 1.689±0.343
DF: Dorsal forearm, MA: Medial arm, ZA: Zygomatic area

age interval to the 61-80 one (4404.15±2244 vs. The LEPs/LEPi ratio displays a significant growth
6138.5±3048, P=0.013) whereas at facial level, there with age, at all three examined sites (P<0.05), due to
is a significant increase of low echogenic pixels from a significant growth of hypoechogenic pixels in the
the first to the fourth age category (13283.39±6513 vs. upper dermis [Figure 2].
18480.82±6219, P<0.0001).
Assessment of subepidermal low echogenicity band
The number of medium echogenic pixels varies in a SLEB was qualitatively assessed by identifying the
statistically significant manner at dorsal forearm level: presence of the low echogenic band in the acquired
they increase in the 21- to 40-year interval (P=0.02) images. We noticed the presence of SLEB in all subjects
and decrease in subjects belonging to the 41-60 and over the age of 20, especially on photoexposed sites
61-80 interval (P=0.01). At facial and medial arm (DF, ZA).
level, medium echogenic pixels also tend to increase
in the second age category, followed by a decrease in DISCUSSION
the third age interval. At medial arm level, in all age
Ultrasonography is well-established clinical
categories, the amount of medium echogenic pixels
medicine as a noninvasive method of diagnosis.
has higher values than on the other two-photoexposed
During the past decade, diagnostic ultrasonography
sites: facial level and dorsal forearm. has been extended to clinical dermatology as well.
Classical ultrasound (7.5-10 MHz) is not common in
The hyperechogenic pixels increase significantly at dermatology, due to a lack of detail, but ultrasound
the dorsal forearm level in the 21- to 40-year interval systems with probes of at least 20 MHz can provide
(964.87±822 vs. 1702.075±1026, P=0.01) followed useful information regarding tumoral extension,
by a decrease in the 41-60 interval (P=0.03) and the inflammatory infiltrate, etc. High-frequency
last age category, >60. At facial site, high echogenic ultrasound in dermatology is also an accurate
pixels decrease in the 21-40 interval (389.92±548 vs. method for determining skin thickness and collagen
480.97±637, P<0.05) and 41-60 interval of age and content in various anatomical regions, with different
increase after the age of 60 (376.37 ±371 P<0.05). intervals of age.[1,13,14] Skin thickness is considered
At medial arm level, there is a significant increase of an objective, physiological parameter that allows
the assessment of the influence of endogenous or
high echogenic pixels in the 21- to 40-year interval
environmental factors, such as UV-rays at tissue
(2908.67±1507 vs. 2210.52±966, P=0.03) followed by
level.[10] Many techniques were used for assessing
a decrease of HEP from the 21- to 40-year age interval
skin thickness: pulsed ultrasound, conventional
to the 61-80 one (2908.67±1507 vs. 1493.025±836, ultrasound, skin-fold measurements etc.[15,16]
P=0.026) [Table 2].
High-frequency ultrasound allows a highly accurate,
Assessment of the LEPs/LEPi ratio objective, noninvasive assessment of the epidermal and
The ultrasound study shows different echogenicity dermal thickness of the integument, regardless of the
degrees for the upper (LEPs) and lower (LEPi) dermis site of examination. Even though there are numerous
with a consequent variation of the LEPs/LEPi ratio studies regarding the imagistic assessment of the
[Table 3]. cutaneous aging process, this research has an original
Crisan, et al. Ultrasonographic assessment of skin

Table 2: Mean variation of the number of low, medium and high echogenic piels on age intervals at the three examined sites
      Age interval
  <20 21-40 41-60 61-80
Investigated are MD 0-30 11240.29±4379.7 9642.22±3672.84 11298.39±3775.47 11203.03±3558.35
50-150 2805±1244.47 3803.9±1310.05 3127.31±1264.32 2969.22±1022.26
200-255 964.87±822.76 1702.07±1026.98 1126.68±879.76 1067.1±744.73
BM 0-30 4917±2460.52 4404.15±2244.83 4842.87±2181 6138.5±3048.8
50-150 3577.65±766.58 3803.35±809.36 3541.24±808.98 3453.2±1059.15
200-255 2210.52±966.19 2908±1507.6 1943±986.8 1493.02±836.94
F 0-30 13283.39±6513.02 17099.18±4691.01 16881.76±4917.25 18480.82±6219.18
  50-150 2941.97±1693.78 2984.2±1457.08 2599.48±1434.73 2809.32±1505.21
    200-255 480.97±637.65 389.92±548.69 304.56±251.72 376.37±371.344

Table 3: Variation of the mean of LEPs/LEPi ratio with age and site of examination
      Age interval
  <20 21-40 41-60 61-80
Investigated area DF LEPS/LEPI 1.278±0.353 1.636±0.658 1.662±0.738 1.688±0.621
MA LEPS/LEPI 1.335±0.351 1.3445±0.439 1.417±0.479 1.424±0.478
ZA LEPS/LEPI 0.876±0.216 1.007±0.223 1.268±0.296 1.306±0.419
DF: Dorsal forearm, MA: Medial arm, ZA: Zygomatic area

volume, especially on photoprotected sites, induced

by various intrinsic and extrinsic factors.[18]

It was also noticed that the dermal thickness has a

tendency to increase in the 21- to 40-year interval on all
examined sites and decreases after the age of 40. This
particular tendency indicates the presence of intense
synthesis processes until the age of 40, followed by the
degenerative phenomena of the extracellular matrix. A
significant growth of the dermis with age is noticed at
facial level, a highly photoexposed area[19-21] [Figure 3].

Studies have revealed that in highly photoexposed skin,

the amount of glycosaminoglycans and proteoglycans
Figure 2: Variation of the LEPs/LEPi ratio on the three examined is increased in the dermal ground substance, while
sites in the four age categories
collagen fibers decrease. The thinning of the skin with
aging results as a consequence of a decrease in dermal
approach, is performed on a greater number of subjects collagen synthesis.[22,23]
(160), quantifies concomitantly several markers and
offers results that are in concordance with the field Also, we noticed that the dermis is thinner on
literature. photoprotected sites than on the photoexposed ones in
all age intervals. The data we obtained was correlated
From the histological point of view, chronologically with literature in the field.[24]
aging skin is characterized by little changes in
epidermal thickness and integrity of the stratum The echogenicity of the skin is given by the
corneum.[17] The study has shown that the epidermal extracellular matrix density. Skin echogenicity
thickness, assessed by high-frequency ultrasound, varies significantly with age, correlated with local
does not vary in a significant manner on any of the degradation processes that occur as the senescence
examined sites, having values between 0.15 and 0.17 process evolves. In time, the dermis becomes
mm. Histological data points out a dermal loss of hypocellular, the number of fibroblasts decreases, and
Crisan, et al. Ultrasonographic assessment of skin

Figure 3: Age-related ultrasonographic aspects of the skin proving

objective changes of skin thickness and dermal density

a dermal volume loss is noticed.[25-28] Also, collagen

fibers undergo a degeneration process, elastic fibers Figure 4: Histological section: skin elastosis (H and E, ×10)
become disorganized and most of the subepidermal
fibers are resorbed.[29]
the HEP is significantly higher than on photoexposed
ones; therefore, HEP can be considered an imagistic
Concerning the assessment of pixels, after the 21- to
marker of the intrinsic aging process.
40-year interval, we notice a significant increase of
the number of low echogenic pixels (LEP), especially
The LEPs/LEPi ratio increases in all age categories, on all
on photoexposed sites such as dorsal forearm and
examined sites, having the most significant increase at
zygomatic area that is due to the accumulation of
facial and dorsal forearm level, the highest photoexposed
elastotic material, increase of glycosaminoglycans and
sites. In these two sites, we noticed a significant increase
proteoglycans amount, aspects visible on histological
of the LEPs in the upper dermis, and a decrease of the
sections. LEP, according to literature, quantify
LEPi. The LEPs/LEPi ratio allows an assessment of the
the degree of cutaneous hydration, inflammatory
processes, solar elastosis, collagen degeneration[2] density and integrity of the extracellular matrix, both
[Figure 4]. from the upper and lower dermis, which vary according
to age, UV-ray exposure, and therapy.[32]
We also mention that SLEB becomes visible mainly
after the 21- to 40-year interval especially on According to literature, LEPs/LEPi is considered
photoexposed sites. SLEB is the correspondent of an objective, imagistic marker for the photoaging
both the histologically identified Grenz zone (collagen process. The dynamics of the repartition of the pixels
neofibrills and glycosaminoglycans) and elastosis, amplitude in the case of the 20-40 “critical interval” on
which are present on photoexposed sites. Grenz zone, all studied sites indicates the initiation of important
a very thin band located below the epidermis is an area morphological, structural, and functional reactions at
of tissue regeneration of the actinic-induced lesions. cutaneous level.[32] We consider that the photoinduced
According to literature, SLEB may be considered cutaneous pathology that may usually be evidenced
an objective marker of the photoaging process.[30,31] after the age of 45, as well as the local, cutaneous
Medium echogenic pixels (MEP) have higher values at changes, can be improved through efficient protection
medial arm level compared to the photoexposed sites. measures applied until the age of 40.
Together with the high echogenic pixels (HEP), they
quantify the proteic structures as well as the degree of The identification of a general, ultrasonographic pattern
assembly into microfibrills or mature fibers.[32] regarding both intrinsic and extrinsic aging, may be
of great use for the noninvasive assessment of the
High echogenic pixels (HEP) follow the same pattern regenerative effect of various personalized cutaneous
on all three examined sites: they increase in the 21- antiaging therapies.[33] High-frequency ultrasound
to 40-year interval and decrease gradually in the third can therefore be used for preventive monitoring
and fourth age category. The decrease is significant in of skin, prohpylaxis of the skin aging process, and
the 41-60 interval in all examined sites. Also, it was personalized therapy assessment. Also the variation
noticed that on photoprotected sites, the mean value of of the identified ultrasonographic parameters can be
Crisan, et al. Ultrasonographic assessment of skin

used for the noninvasive evaluation of the efficacy of evaluation with image analysis of normal skin: Variations
according to age and sex. Skin Pharmacol 1994;7:201-9.
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