Skin aging as a mechanical phenomenon: The main weak links

2.1Layered structure of the composite skin/sWAT

In a general case, human skin must be considered as a multi-layer composite containing the SC/viable epidermis/papillary dermis/reticular dermis layers with different geometrical characteristics and mechanical properties (Fig. 2). Further, we are describing the single layers i of such composite by their thicknesses, h_i, Young’s moduli, E_i, and Poisson’s ratios, ν_i. Such a description limits further consideration of mechanical loadings with low strains and low strain rates and neglects the anisotropic and viscoelastic properties of the skin.

Typical average thicknesses of the facial SC layer, h_sc, epidermis, h_e, papillary dermis, h_pd, and reticular dermis, h_rd, are about 15–20μm, 100–150μm, 20–30μm, and 1–1.5 mm, respectively [37]; the thickness of the adjacent sWAT layer, h_f, can be several fold bigger than the thickness of the dermis, which is h_d = h_pd + h_rd. Typical thickness ratios η_esc = h_e/h_sc, η_de = h_d/h_e, and η_fd = h_f/h_d in the facial skin are about 10–15, 10–15, and 2-3, respectively.

Fig. 2

Layered composite skin/sWAT with adherences between single layers.

The thickness of single layers demonstrate significant variations even within a specific site. Application of reflectance confocal microscopy revealed the within-site variations of SC and epidermis thicknesses of 59% and 49%, respectively [38]. This should be connected with the fact that the interfaces between the single layers in the composite skin/sWAT are not flat and demonstrate typical undulations. These undulations as well as their reduction and smoothening in aging are well-known for the dermal-epidermal interface where they are named rete ridges or papillae. Such deformations of the interfacial area are strongly connected with mechanical properties of the papillary dermis which appears to be much more compliant than the adjacent epidermal layer. Similar undulations were also described on the dermal-sWAT interface and were connected with existence of the special dWAT sub-layer [29], which is supposed to be much more compliant than the adjacent reticular dermis. Whereas such undulations were not directly described for the SC-viable epidermis interface, their existence should be also strongly assumed based on the high within-site variations of SC thickness observed in [38].

Adherence between adjacent layers does not allow them to slide past each other under mechanical deformation, thus causing the separate layers to have very different mechanical properties to a single laminated composite. When the adherence between the layers is weak, they fail to exchange the mechanical energy with each other and thus cannot produce the single composite with some effective mechanical properties. Adhesive strength was shown to be an important parameter defining the appearance and propagation of structural instabilities in laminate structures [3], which makes it especially important for the description of the mechanical properties of the skin in aging.

The Young’s modulus of the SC layer, E_sc, is three to four orders of magnitude bigger than the corresponding modulus of the dermis, which, in turn, is much bigger than the Young’s modulus of the adjacent sWAT layer. At low strain rates, it can generally be assumed that E_f << E_rd << E_sc. Typical reported values for the Young’s moduli are 1–20 kPa in the sWAT [39–41], and 30–100 kPa in the dermis [42, 43], whereas the absolute values are strongly dependent on the measurement procedure. For example, the Young’s moduli of SC and dermis obtained with suction methods were reported to be about 2 MPa and 66 kPa, respectively [5].

The ratio between the Young’s moduli in adjacent skin layers strongly depends on the strain rates applied to the composite. At the strain rates of 0–10 s^–1, this modulus in porcine skin was reported to be about 1000-fold bigger than in the sWAT, at the strain rates over 1,000 s^–1 it was just about 7-fold bigger [41]. Additionally, mechanical pre-loading can significantly influence the Young’s modulus; this effect is especially pronounced in tissues having high content of fibrotic structures [39].

2.2Pre-stress conditions in the skin

Normally, both the skin and the sWAT are subject to different types of external thermic and mechanical stresses, and the composite SC/epidermis/dermis/sWAT can demonstrate different reactions depending on the stress type [44]. At the same time, these layers are pre-stressed, i.e. they are under stress even without application of external mechanical forces. Human skin in vivo is normally in a state of tension [35, 36], whereas the absolute values of this tension are spatially heterogenous. Loss of tension in aging skin was connected with reduction of underlying sWAT layer [45] and it was supposed that this process can influence the wrinkle appearance in the skin. Skin can be additionally stressed, for example, through local inflammation or through UV irradiation, which can modify its mechanical properties in a dose- and time-dependent manner [46, 47].

Stress conditions in the sWAT layer are connected with its expansion or reduction. Expansion of the sWAT is generally caused by such processes as local inflammation or application of cold or heat, whereas its reduction is typical, for example, in involution and in development of local fibrosis [48–50].

Expansion or reduction of the sWAT layer can produce additional stress in the skin. Such effect should be especially pronounced in sWAT depots having the compartmental and thus spatially limited structure, which is the case for the facial sWAT [51]. Boundaries between different facial fat compartments consist of fibrous septae. These fibrotic structures not only separate distinct compartments, but also clamp the fat tissue at the compartments’ edges, thus producing additional mechanical stress in sWAT.

Different facial fat compartments have distinct structures, whereas generally two main types of them can be described according to [52]. Fat compartments of the type 1 are characterized by a loosed interface and relatively weak adherence between the skin and underlying sWAT, which can be anatomically easily separated from each other. Such type of adherence was found in the medial and lateral midface, in some parts of the periorbital area, in the temple, forehead, and neck [51]. SWAT in these compartments was classified as “structural” adipose tissue. Fat compartments of the type 2 are characterized by a strong adherence between the skin and the sWAT and were found in the perioral and nasal areas as well as in the proximity of the eyebrows. SWAT in these compartments was classified as “fibrous” adipose tissue. Thus, different facial fat compartments demonstrate various mechanical properties and must produce different mechanical stress in a covering skin. Less is known about the “vertical” correlation of collagen content and of corresponding Young’s moduli in adjacent areas of reticular dermis and sWAT, whereas it can be strongly assumed that such correlations exist.

3.1A thin stiff film on a thick compliant substrate

Different structural instabilities can appear in a stiff thin film adhered to a thick compliant pre-strained substrate (further, SFCS model) after this substrate was released. Such instabilities were described for the substrates with elastic [53] or viscoelastic [6] properties, having infinite or finite thickness [54, 55], and appearing as a single layer or a bi-layer structure [56]. Structural instabilities occur when the strain in the film exceeds some critical value, and they demonstrate a hierarchy in their appearance [3, 57]. The occurrence of these structures and their propagation reduces the strain energy in the stiff film, which is transferred to a more compliant substrate to minimize the total energy of the composite. Of note, the type of appearing instability is strongly dependent on the type of mechanical stress – tensile or compressive – applied to the film. Recently, this model was extended to the case of SFCS containing the fiber-reinforced layers [58] as well as to the case of a soft interfacial layer located between the film and the substrate [24], which are both the typical features of the composite SC/epidermis/dermis/sWAT.

Fig. 3

Bi-layer composite epidermis/dermis.

Mechanical stability of the film in the SFCS model is dependent on different dimensionless parameters. For such instability as wrinkles which appear under application of tensile stress to the film, these are the ratios of stiffness, E¯fm/E¯st, of tensile stiffness, E¯fmhfm/E¯sthst, and of bending stiffness, E¯fmhfm3/E¯sthst3. From here, the onset of instabilities in the film depends only on the ratios of the elastic moduli between the layers and their relative thicknesses, but not on their absolute values.

Generally, every system can be destroyed by deformations which are strong enough. Because of this, critical strains required for the loss of structural stability is the most important parameter providing the possibility to compare different systems under various loading conditions. Further, we are concentrating our discussion on the critical strain to compare the influence of different structural units of the layered skin on its stability.

3.2Epidermal instabilities appearing in a bi-layer model epidermis/dermis with and without bending

The SFCS model allows a simple analytical solution for the critical strain, ɛcr∞, required for the onset of wrinkles in the case of infinite substrate. For this, the total energy of the composite, containing the bending and membrane energies of the film as well as the strain energy of the substrate, should be minimized. Appearance of wrinkles releases a part of the strain energy in the film but simultaneously increases this energy in the substrate.

This description corresponds to the skin/sWAT model presented in Fig. 2 where the layers 1 and 2 are combined into an effective stiff “epidermal” layer, and the layers 3 and 4 produce an effective compliant “dermis” layer (Fig. 3). In this model, sWAT layer is considered to have no adherence to the dermis, which excludes this layer from a mechanical description. The critical strain required for the appearance of epidermal wrinkles ɛcr∞ and the wavelength of these wrinkles λ_∞ in the case of infinitely thick dermal layer can be found similar to the SFCS model [1, 53] as

Expression (1) provides the critical strain required for the skin wrinkling of ɛcr∞=0.52% at E¯e/E¯d∼103. This critical strain is very small and can be easily produced under physiological conditions even in the young skin, which contradicts the well-known fact that wrinkling appears only in chronologically or externally aged skin. This contradiction is connected with some oversimplifications of the above model and especially with the assumption that the substrate (dermis) has the infinite thickness. This is, however, not the case in the skin, where the thickness ratio between the layers is just about η_de = h_e/h_d ∼ 10.

Generalization of the bi-layer SFCS model to the case of the substrate of a finite thickness was provided in [54, 55]. One important prediction from these models is that the behavior of a thin film on a finite thickness substrate is mainly dependent on the bending stiffness ratio between the layers, which for the bi-layer epidermis/dermis is γed=E¯ehe3/E¯dhd3. The wavenumber k of wrinkles (k = 2π/λ, where λ is the wavelength) appearing in the skin, can be found from equation [54]

Fig. 4

Wrinkling in the bi-layer skin model with bending: a – bi-layer composite epidermis/dermis; b – bending of this composite; c – wrinkling of the bended composite (modified after [55]).

Critical strain in epidermis required for its wrinkling can be found from the minimization of the potential energy of the system epidermis/dermis including the bending energy and the strain energy in the epidermis and the dermis with respect to the strain. The result is strongly dependent on the bending ability of the skin. If skin bending is not allowed, after straightforward calculations similar to [55], the critical strain can be presented in the form

From (3), the critical strain quickly reduces with increasing thickness ratio η_de = h_d/h_e and reaches the value of ɛcr∞ in the case of the infinite dermis thickness h_d→ ∞, since in this case limhd→∞a(khd)=1/2. This leads to a surprising conclusion that a standalone thickening of the dermis does not increase but reduce the skin stability against wrinkling. At the same time, critical strain increases with increasing ratio of bending stiffness. For example, at h_d = 1 mm and η_de = 10, the critical strain will be about ɛ_cr = 27.9% ;72.7 %, and 245.6% for the ratios of bending stiffness of γ_ed = 0.1 ; 1.0, and 10.0, respectively. It is seen that the critical strain quickly increases with increasing ratio of bending stiffness between epidermis and dermis.

If the skin is able to undergo arbitrary bending deformation, the critical strain for wrinkling will be much higher. Its theoretically maximum value is

Expression (4) shows an interesting property of such layered skin composite: bending can increase the critical strain up to 4-fold, making the appearance of epidermal wrinkles under physiological conditions almost impossible. The reason for this is that bending of the film and substrate is energetically more favorable than their wrinkling; consequently, skin bending must take place before the onset of its wrinkling (Fig. 4). Thus, when such a layered system as human skin can bend, it will first pump the energy into the bending modes and does not produce the structural instabilities on its surface. From the physical point of view, bending is the first and wrinkling is the second order bifurcation taking place in such layered composite.

Fig. 5

Tri-layer skin model containing an intermediate compliant layer.

It should be noted that the expression (4) is valid only for the case of the optimal bending, since it was obtained by minimization of the potential energy with respect to the substrate curvature, i.e. it was assumed that the substrate can be deformed to any degree. The optimal curvature leading to the maximal stability of the layered system film/substrate can be calculated from minimization of the total potential energy of the system with respect to the skin curvature, which provides the following result:

Here we have taken into account the expression (4) and the relationship between the tensile stiffness in two skin layers: E¯dhd<<E¯ehe. From (5), the optimal curvature of the skin reduces with increasing skin thickness. For example, at h_d = 1.0mm, 1.5 mm, and 2.0 mm and the critical strain of ɛcrbend=20.0%, the optimal curvatures leading to the relation (4) will be 0.3 mm^–1, 0.2 mm^–1, and 0.15 mm^–1, respectively. These values correspond to the local radii of dermis bending of 3.3 mm, 5.0 mm, and 6.7 mm, respectively.

To bend, the dermal layer should contain elastic fibers which support the skin deformation. Gradual loss of these fibers in aging must lead to continuous reduction of the strain threshold required for the onset of structural instabilities. Concentration of elastic fibers in the dermis is indeed gradually reduced in aging skin [59, 60]. This process leads to corresponding gradual reduction of the critical strain from its maximum value described by (4) to the minimum value in the case of no bending described by (3), thus making the aging skin less resistant to wrinkling. This special effect, which to our best knowledge was not considered before, can significantly contribute to the development of structural instabilities in aging skin.

In this context, it should be noted that the increment of the underlaying sWAT layer leads to enlargement of adipocytes, and this effect correlates with increased degradation of dermal elastic fibers [61, 62]. This mechanism demonstrates how the sWAT layer can directly influence the mechanical properties of the skin.

To assess the plausibility of these results, we need the information concerning the natural strains existing in the skin. This parameter was calculated in [13, 27] from the data for the initial stress and Young’s modulus in different age and gender groups and had the average value of about 6% for the group of 30–40 years old females. In this context, it should be noted that the stress and strain fields in the skin can demonstrate gradients near the skin projections of the boundaries between the neighboring facial fat compartments, which together with variable SC thickness can serve as the weak links for the onset of structural instabilities.

Skin aging was reported to be connected with an increase of the effective Young’s modulus of the epidermis, E¯e, and dermis, E¯d, after 30 years [13]. More complicated is the behavior of the skin thickness which in women was reported to increase by about 30% up to 30–40 years and then decrease by about 20–30% up to 80–90 years. As seen from (3), simultaneous increase of cutaneous Young’s modulus and dermal thickness can effectively reduce the critical strain in the skin required for its wrinkling.

3.3Epidermal instabilities appearing in a tri-layer model SC/“upper” dermis/“lower” dermis

Next, we consider the tri-layer skin model containing the layers SC/“upper” dermis/“lower” dermis (Fig. 5). The “upper” dermis is an effective skin layer containing the viable epidermis and papillary dermis (layers 2 and 3 in Fig. 2), the “lower” dermis is the reticular dermis layer, and sWAT layer will be further considered to have no adherence to the dermis. The “upper” dermis has the Young’s modulus which is much smaller than both the Young’s moduli of the SC and “lower” dermis [21]. Existence of such intermediate compliant skin layer can significantly change the mechanical properties of the skin and its resistance against wrinkling.

The tri-layer SFCS model containing an additional intermediate soft layer placed between the stiff film and the elastic substrate of the infinite thickness was recently considered in [24]. The critical strain required for the onset of instabilities in SC in the case of very thick reticular dermis can be found by minimization of the total potential energy of the composite with respect to ɛ_cr in the form

Here k is the wave number of appearing wrinkles; h_ud is the thickness of the “upper” dermis layer; E¯ud and E¯rd are the plane Young’s moduli of the “upper” and “lower” (reticular) dermis, respectively. At a first approximation, we have neglected the Poisson’s effect in the dermis considering this layer to be almost incompressible, and thus having the Poisson’s ratio of ν_rd ≈ 0.5.

Expression (6) takes the form similar to (1), which in this case describes the composite SC/“effective dermis”, when the intermediate layer is absent (E¯ud=E¯rd), the ratio of tensile stiffness is small (E¯ehe<<E¯dhd), and the reticular dermis is infinitely thick (h_rd → ∞), since in this case limhrd→∞a(khrd)=1/2.

This behavior is dramatically modified if the “upper” dermis is much softer than the “lower” dermis, i.e. if E¯ud<<E¯rd<<E¯sc, which is indeed the case for the skin in vivo [21]. Numerical calculations provided in [24] revealed an important feature of such tri-layer systems having an intermediate compliant layer: critical strain required for the onset of wrinkles in the stiff film placed on the top of such composite can be several times lower than the corresponding critical strain obtained for the bi-layer model without intermediate soft layer. Thus, the existence of a very compliant “upper” dermis layer located between the very stiff SC and moderately compliant reticular dermis significantly reduces the mechanical stability of the skin and increases its susceptibility to wrinkling. This supports the idea that the papillary dermis is critically involved in the skin aging process [63].

3.4Structural instabilities appearing on the dermal-epidermal and dermal-subcutaneous interfaces

Till now we have considered the epidermal mechanical instabilities appearing on the top of the bi-layer (epidermis/dermis) and tri-layer (SC/”upper” dermis/”lower” dermis) skin models. Now we consider the question what may respresent the mechanical reason for the structural undulations appearing on the dermal-epidermal interface.

For this, we will consider the tetra-layer skin model SC/viable epidermis/papillary dermis/reticular dermis with flat dermal-epidermal interface and without adherence on the dermal-sWAT interface. To the best of our knowledge, there is no reliable independent measurements for the Young’s moduli of the viable epidermis, papillary dermis and reticular dermis in the same subjects, but it can be strongly assumed that E¯pd<<E¯νe<<E¯sc. Application of relatively low mechanical stress to such tetra-layer system can lead to a special phenomenon which is not evident: dermal-epidermal interface will undergo mechanical deformation leading to production of wrinkling instability first not in the SC layer which is too stiff to undergo the bifurcation at relatively low strains, but on the interface between two more compliant layers epidermis/papillary dermis. This effect must be dependent on the adherence between epidermis and papillary dermis [64].

Morphologically, adherence between epidermis and dermis is mainly determined by properties of the basement membrane, which is structurally connected with both layers [65]. The basement membrane in healthy skin reveals the typical structure known as rete ridges (papillae) – interpenetrations of epidermis and dermis whose amplitude is determined by adhesive strength. Very recently, it was reported that rete ridges are not present in the neonatal skin and appear gradually over the first 3 months of life [66]. It is known that the dermal-epidermal interface is connected with the dermal ECM through a protein network containing COL1, COL4, COL5α1, COL6α3, COL15, and laminin-111 [67].

Adhesive strength on the dermal-epidermal interface is dependent on the effective interfacial contact area which continuously reduces with aging. Increased aging correlates with effacement of rete ridges, decreases of their height and a reduction of dermal papillary projections (Fig. 3) [68]. The number of rete ridges per unit skin surface length in the aged skin decreases to about half of what young skin displays [69]. The expression of collagen along the dermal-epidermal interface can be significantly suppressed by UV irradiation [70]. At the same time, the appearance of epidermal wrinkles as mechanical instabilities is only possible if the adhesive strength between the layers is high. This means that the initial onset of wrinkling should take place in a relatively young skin having a good adherence on the dermal-epidermal interface. This well correlates with observations that the skin wrinkling rate undergoes a step-like increase in early thirties indicating that the wrinkle morphologies in young and old skins must be different [27].

The dermal-sWAT interface also demonstrates undulations, which can reflect mechanical instabilities appearing in this area in an analogous fashion. Deep adipose indentations into the dermis in the thigh area were observed in women with cellulite comparing with women without cellulite or with men, which led to conclusion that such indentations should be the characteristic marker of cellulite [71, 72]. Indeed, it was shown that the architecture of the dermal-sWAT interface correlates with cellulite severity [73] and that this interface can quickly react to mechanical loading with decrease of its surface area [71].

Undulations of the interface with interpenetration of neighboring layers similar to rete ridges are typical for the bimodular substrates having the tension-compression asymmetry, i.e. very different tensile and compressive mechanical moduli [74]. Moreover, it was found that the inward dimples typical for rete ridges appear in the case when the tensile modulus is bigger than the compressive one. This is generally the case for collagen networks, where the Young’s modulus can be an order of magnitude lower under compression than under extension [75].

3.5Influence of the sWAT layer on the onset of epidermal wrinkles

In the above models, the low adhesive strength on the dermal-sWAT interface completely excludes the mechanical involvement of the sWAT layer in modulation of the mechanical properties of the skin. We now assume that the adherence between the dermis and sWAT is strong and discuss how such bonding can affect the critical strain required for the onset of epidermal wrinkling. For this, we consider the system dermis/sWAT as a mechanical bi-layer substrate (Fig. 6). The mechanical behavior of a stiff thin film on a bi-layer substrate with the bottom substrate (in our case, sWAT) having the infinite thickness was discussed in [56].

Fig. 6

Surface instabilities in the film placed on a bi-layer substrate. The adherence between dermis and sWAT is so strong that this bi-layer must be considered as a mechanical composite.

To consider the influence of a bi-layer substrate with single layers of finite thicknesses on the onset of epidermal wrinkling, we will introduce the effective elastic modulus of the composite dermis/sWAT. Let us consider dermis and sWAT to be mutually confined and unable to slide past each other, i.e. we will assume that the dermal-sWAT interface has very high adhesive strength. If the loading producing the stress in the skin is directed in-plane to the skin surface, the effective Young’s modulus of such bi-layer can be approximately presented in the form [44]

Here η_df = h_d/h_f is the thickness ratio between the dermis and sWAT. Thus, the effective Young’s modulus of the mutually confined dermis/sWAT layers is smaller than the corresponding dermal modulus whereas the effective substrate thickness is (1 + η_df)/η_df times bigger than h_d.

Next, we will compare the critical strains required for the onset of wrinkling in the bi-layer epidermis/dermis described by Eqs. (2)-(3) and in the bi-layer epidermis/”effective dermis”, where the Young’s modulus of the dermis should be replaced by E¯df|| and its thickness should be replaced by (1 + η_df) h_d/η_df. Numerical solution of Equation (2) at E¯e/E¯d∼103, h_e = 100 μm, h_d = 1mm, and η_df = 0.5 (sWAT layer is 2-fold thicker than dermis) provides the values of k = 1.129mm^–1 and a(khdeff)=0.536. Substituting these values into the expression (3), we obtain ɛ_cr = 26.7%, which is smaller than the critical strain ɛ_cr = 72.7% obtained above for the bi-layer epidermis/dermis neglecting the influence of the sWAT layer. At the same time, for the thickness ratio of η_df = 0.25 (sWAT layer is four times thicker than dermis), the corresponding strain will be just ɛ_cr = 18.2%. These values will be further reduced if we take into account the mechanical sandwich structure of the skin described in the previous section. Thus, presence of a thick sWAT layer having strong adherence to reticular dermis can significantly influence the appearance of skin wrinkles.

This consideration is valid for the case of the stress applied in-plane to the skin surface. When mechanical loading is directed normal to the skin, the effective Young’s modulus of the bi-layer dermis/sWAT can be approximately described as [44, 76]

Whereas the effective Young’s modulus of the bi-layer dermis/sWAT is mainly determined by the Young’s modulus of the dermis in the case of mechanical stress applied in-plane to the skin surface, this modulus is much lower and mainly determined by mechanical properties of the more compliant sWAT layer in the case of the mechanical loading applied perpendicular to the skin. This effect will significantly increase the elastic mismatch between the epidermis and the composite dermis/sWAT and consequently reduce the critical strain required for the onset of structural instabilities in the skin.

At E¯f=1kPa, η_df = 0.5, d_d = 1mm, and ν_f ≈ 0.4 [77], the effective Young’s modulus E¯df⊥ will be approximately 3.2 kPa, and the effective substrate thickness is 3 mm. Accordingly, the effective bending stiffness ratio in this system will be about γ_ed ≈ 0.579 instead of 1 (as considered above for the case of no adherence on the dermis-sWAT interface), and the critical strain will be ɛ_cr = 55.1%. This ratio and the critical strain will be reduced to γ_ed ≈ 0.325 and 0.205, and ɛ_cr = 42.1% and 34.4% at ν_f ≈ 0.45, and 0.47, respectively. It can be seen that the onset of wrinkles under transverse compression of the skin is dependent on the Poisson’s effect in the sWAT, and that more compressible sWAT layer will better protect the skin from wrinkling.

At η_df = 0.25, the corresponding values are γ_ed ≈ 0.694, 0.391, and 0.247, and ɛ_cr = 37.1%, 29.1%, and 24.3% at ν_f ≈ 0.4, 0.45, and 0.47, respectively. Thus, the critical strain required for the onset of wrinkling decreases with increasing sWAT thickness. In other words, under other equal conditions, the skin must be more susceptible to wrinkling when the sWAT layer is thicker. This effect increases with increasing adhesive strength on the dermis-sWAT interface.

Thus, the adherence on the dermal-sWAT interface must, additionally to the adherence on the dermal-epidermal interface, influence the mechanical behavior of the composite skin/sWAT. While less is known about morphological structures involved in dermal-sWAT adherence, it can be strongly assumed that COL6 [78] and CLMP (Coxsackie virus and adenovirus receptor-like membrane protein) [79, 80] participate on this junction. It was stated that CLMP, also known for adipose tissue as adipocyte adhesion molecule (ACAM), is strongly involved in production of zonula adherence between the cells and significantly influences the integral mechanical strength of the tissue [79]. It can be also supposed that the dermal-sWAT adherence is dependent on the sWAT type. Consequently, different facial fat compartments must demonstrate distinct adhesive properties, which was indeed observed anatomically [51, 52].

Mechanical behavior of the dermal-sWAT interface must be similar to that of the dermal-epidermal interface, since this surface also demonstrates the undulations. Whereas this item was not investigated properly, it can be strongly assumed that these undulations are connected with tension-compression asymmetry existing in sWAT and must be more pronounced in sWAT compartments with high collagen content.

Recapitulating, the sWAT layer of the finite thickness having a strong adherence to the reticular dermis can significantly decrease the critical strain needed for the onset of epidermal wrinkles, whereas this effect must be dependent on the direction of the mechanical loading. Taking into account that different facial fat compartments have various thicknesses of the sWAT layer, different sWAT structures (with correspondingly distinct Young’s moduli and Poisson’s ratios), and demonstrate different adherences on the dermis-sWAT interface, it should be clear that these compartments must differently influence the appearance of skin wrinkling. This effect must be at least partly responsible for the spatial differences in the facial topography of wrinkles in aging skin.

3.6Nutritional effects on fat layers and aging

Both subcutaneous and dermal adipose tissue are affected by nutritional status. At the same time, different depots expand and shrink by different mechanisms. Some depots undergo hyperplasia (i.e. recruitment of additional fat cells), while in other depots, exposure to excess nutrients primarily affects hypertrophy (i.e. an increase in cell size). The subcutaneous fat depots primarily rely on hypertrophic expansion [49]. Contrarily, the dermal fat layer can expand in size and cell number in response to high fat diet, though the underlying mechanisms have not yet been fully explored. Such dietary modulation of the sWAT layer structure must significantly influence the mismatch in mechanical properties between tissue layers. Moreover, it is very likely that nutritional components also influence the adhesion strength between adjacent layers and consequently also modify the aging process. This effect has however not been examined properly.