Upload
chiper-zaharia-daniela
View
10
Download
1
Embed Size (px)
DESCRIPTION
a
Citation preview
Review Article
Axillary skin: biology and care
R. L. Evans, R. E. Marriott and M. Harker
Port Sunlight Laboratory, Unilever Research and Development, Quarry Road East, Bebington Wirral, CH63 3JW, U.K.
Received 17 April 2012, Accepted 14 May 2012
Keywords: axillary skin, hair removal, irritation, post-inflammatory hyperpigmentation (PIHP), skin care technology, stratum corneum
Synopsis
In skin care, the axilla is a biologically unique site requiring
specialized attention and care. This area of skin is often subject to
hair removal techniques, such as shaving and plucking. These pro-
cedures damage the skin leading to erythema and dryness in the
short term, and in some cases, post-inflammatory hyperpigmenta-
tion (PIHP) in the long term. This study will (i) briefly review the
biology and unique properties of axillary skin, and (ii) describe the
characteristics of the irritation and damage induced by contempo-
rary skin care habits and resolution of these responses by the use
of efficacious skin moisturizing technology. With respect to the
latter, we propose that there are five groups of compounds, defined
according to their mechanism of action, which are particularly
relevant to the care of damaged axillary skin.
Resume
Dans le domaine des soins de la peau, l’aisselle est un site
biologiquement unique qui necessite une attention et des soins
specialises. Cette zone de la peau est souvent exposee a des tech-
niques d’epilation, tels que le rasage et l’arrachage. Ces procedures
endommagent la peau ce qui peut conduire a des erythemes et
provoquer de la secheresse a court terme, et dans certains cas, une
hyperpigmentation post-inflammatoire (PIPH) dans le long terme.
Cet article (i) passe brievement en revue la biologie et les proprietes
uniques de la peau axillaire, et (ii) decrit les caracteristiques de
l’irritation et des dommages induits par les habitudes actuelles des
soins de la peau, pour proposer les solutions a ces reactions cuta-
nees qui consistent en une technologie efficace d’hydratation. En ce
qui concerne ce dernier point, nous estimons qu’il y a cinq groupes
de composes, definis en fonction de leur mecanisme d’action, qui
sont particulierement pertinents pour le soin de la peau axillaire
endommage.
Introduction
The skin is the largest organ in the human body. Its primary
function is to act as an epidermal barrier to water loss, whilst pro-
viding protection from ultraviolet radiation, and a variety of exoge-
nous substances [1, 2]. This concept of ‘barrier function’ is now
known to specifically reside in the protective properties of the
uppermost layer of the skin, the stratum corneum. Until quite
recently, the stratum corneum was perceived as being the dead,
cornified layer of skin that interfaced directly with the environ-
ment. Researchers have now established that the stratum corneum
is in fact catabolically alive and plays a key role in maintaining the
physiological status of normal skin [2–4].The stratum corneum is adept at signalling alterations in its
mechanical and chemical condition, which can result in rapid
repair when necessary. Data have shown that water activity is the
key driver of this property [5, 6]. Environmental stresses, particu-
larly decreases in humidity, such as those associated with dry and/
or cold weather, bring about a variety of physiological changes
that help promote barrier repair and reduce skin dehydration [4].
In some individuals, the axillary skin may face additional chal-
lenges including leaching of lipids and proteins from the stratum
corneum by cleansing surfactants, or additional irritation induced
by shaving and plucking [7]. Under these types of duress, damage
to the skin may initiate an output of pro-inflammatory cytokines
from the epidermis, and from mast cell degranulation [8], which
can in turn impair the pattern of keratinocyte proliferation, or
stimulate nerve endings leading to irritation, itch and erythema [9]
(depicted in Fig. 1). During these conditions, the stratum corneum
is further damaged by the loss of rafts of incorrectly differentiated
corneocytes at the surface (dry skin), by the increased sensitivity of
the weakened axillary skin barrier to additional challenge by exter-
nal factors, or from mechanical damage to the skin surface by
scratching in response to itch (Fig. 1). These responses perpetuate
the existing damage and can lead to further inflammation.
Dry, irritated and/or damaged skin is most effectively treated by
the application of skin care formulations containing moisturizing
actives [10–12]. Moisturizers have traditionally been classified into
three key groups: humectants, occlusives and emollients. We now
propose that there at least five different groups of compounds
which are particularly relevant to the care of axillary skin damaged
by hair removal and that these can be defined according to their
mechanism of action. The most commonly used molecules are
humectants, which help bind water in the skin and keep it there
for longer. Glycerol is a classic example [12, 13]. Although glycerol
may not be the most effective humectant in terms of its ability to
bind water, its uniqueness comes from its ability to be transported
to sites that require it by aquaporin proteins expressed by the
keratinocytes [14]. Occlusive compounds form a barrier layer
across the skin surface, trapping water in the skin. Petrolatum has
been used effectively for many years [15]. Barrier integrity actives
Correspondence: Richard L. Evans, Unilever Research and Develop-
ment, Quarry Road East, Bebington, Wirral CH63 3JW, U.K. Tel.: +44
(0)151 641 3369; fax: +44 (0)151 641 1861; e-mail: richard.evans@
unilever.com
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie 389
International Journal of Cosmetic Science, 2012, 34, 389–395 doi: 10.1111/j.1468-2494.2012.00729.x
(classically ‘emollients’) boost biological functions in the skin
barrier and normalize cellular proliferation, improving barrier
performance. Well-known examples include the application of skin
lipids such as ceramides, unsaturated fatty acids such as
conjugated linoleic acid and related triglycerides such as sunflower
seed oil (SSO) [16], which can be broken down by the skin to the
essential fatty acid linoleic acid, a precursor of ceramide synthesis.
The fourth group of compounds are anti-irritant actives that aim to
prevent inflammation (erythema) and itching, protecting the bar-
rier from repetitions of the skin irritation cycle (Fig. 1). Finally, it
has recently been proposed that some compounds can stabilize lipid
structures within the skin by altering their packing co-ordination.
These actives have been named ‘internal occlusives’ and are an
emerging interest area for cosmetic ingredient suppliers [17, 18].
All five classes of actives serve to increase the quality of the
stratum corneum barrier, and therefore the general condition of
the skin, in accordance with the outside-inside-outside solution
originally proposed by Elias [19].
Eccrinegland
Apocrinegland
Sebaceousgland
Hairfollicle
Bulb
Melanocytes
Stratum corneum
Stratum basale
Dermis
Sensory nerves
Epidermis
Epidermis
Dermis
Stratumcorneum
Corneocytesremoved by shaving
Weakened underarmskin barrier
Greater susceptibility to external factors
Keratinocyte
Mastcell
mediators andgrowth factors
3
Underarm skin barrierdamage (loss of cells,
lipids, proteins and NMF)
2
5
7
1
Irritation/itch/erythema
6Incorrect epidermal
differentiation/hyperproliferation
Changes in nerve sensitivity (mediated by neutrophins e.g. BDNF)
4
Sensorynerves
External factors (shaving, plucking, waxing, harsh
cleansing, low pH)
Razor Tweezers
(a)
(b)
Figure 1 Structure of axillary skin (a) and the axillary irritation cycle (b). Schematic (a) shows a longitudinal section through axillary skin. Typical append-
ages are shown: the hair follicle and bulb, the eccrine sweat gland (which secretes clear, hypotonic sweat onto the skin surface to facilitate thermoregulation)
and apocrine sweat gland (which produces a milky, high lipid content, secretion directly into the hair follicle across the stratum basale), the sebaceous gland
and the melanocytes (which synthesize melanin and can drive axillary post-inflammatory hyperpigmentation following various skin care regimens in suscepti-
ble individuals). Schematic (b) depicts the steps by which external factors such as hair shaving, plucking or waxing and harsh cleansing and/or low pH prod-
ucts (typically aluminium salt-containing anti-perspirants with pH below 4.0) can trigger a sequence of events that result in axillary irritation, which is
sustainable by repeat events. Thus, removal of corneocytes from the stratum corneum by shaving for example (1), results in axillary skin barrier damage (2;
loss of cells, lipids, proteins and NMF), which in turn triggers the release of pro-inflammatory mediators and growth factors from keratinocytes and mast cells
(3). These mediators either directly drive skin irritation and erythema (5), or enhance it via changes in nerve sensitivity (4) resulting in itching and/or pain.
The latter may lead to additional physical skin damage as a consequence of a response such as scratching. Irritated skin responds by repairing itself via changes
in keratinocyte differentiation and proliferation (6), resulting in barrier repair in the case of acute external damage, or, further weakening of the skin barrier
(7) in the case of chronic damage.
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395390
Axillary skin: biology and care R. L. Evans et al.
This study will (i) briefly review the biology and unique proper-
ties of axillary skin, and (ii) describe the characteristics of irritation
and damage induced by contemporary skin care habits [including
post-inflammatory hyperpigmentation (PIHP)] and the resolution of
these responses by the use of products delivering efficacious skin
moisturizing technology.
Axillary skin
The human axilla represents a unique skin site on the human body
[20]. As well as containing large numbers of hair follicles and seba-
ceous glands, it is densely populated with eccrine and apocrine
sweat glands [21] (Fig. 2). The biology of these skin appendages
has been described in detail in several reviews [22–25].The median surface area of axillary skin has been shown for a
single axilla to be 116 cm2 for men and 65 cm2 for women [26].
Several studies have shown that the general properties of axillary
skin are distinctly different from those of other body sites. Thus,
trans-epidermal water loss (TEWL) and corneosurfametry have
revealed reduced barrier integrity in the axilla, compared with the
volar forearm [27, 28], whereas a recent confocal Raman study
has reported that cholesterol, ceramide 3 and lactic acid (also a
component of sweat) levels are elevated, and NMF amounts lower,
when compared with the forearm [29]. In addition, axillary
cornified envelopes have been found to be smaller than those found
on forearm skin, indicative of a shorter stratum corneum turnover,
even though there appeared to be no significant difference in
corneocyte maturation [20, 30]. ‘Skin dryness’ squamometry mea-
surements have indicated that the axillary stratum corneum
retains more incompletely desquamated material on its surface
than the forearm, and this is correlated with decreased levels of the
desquamatory stratum corneum chymotryptic enzyme in the
surface layers of the skin [20].
A series of studies have been directed at determining the skin
surface pH of the axilla and in particular whether gender differ-
ences exist [31, 32]. The results are contradictory with Burry et al.
reporting no difference in the pH of male and female axillary skin
surface/sweat pH, (when correcting sweat pH for carbon dioxide
lost post-secretion), whereas Williams et al. [32] reported that
women have a lower axillary skin surface pH than men before and
after washing with water. The differences in these findings can be
attributed to differences in the techniques used to measure skin
surface pH, and as consequence, the area is still open to debate.
Burry et al. also reported large differences in the skin surface pH of
the vault and fossa regions of the axilla and attributed these to
higher sweat rates in the vault [31]. This phenomenon is thought
to arise from the reduced period of time available for the eccrine
gland duct to reabsorb bicarbonate from the sweat during its
journey to the skin surface [25, 33].
Circadian rhythms have also been shown to impact axillary skin
pH. Thus, in male subjects, skin surface pH has been reported to be
pH 5.9 in the morning and pH 5.5 in the evening [34]. These
observations may reflect a diurnal fluctuation in stratum corneum
enzyme function [35] and sebum production [36].
Axillary irritation and changes because of hairremoval
The personal care regimes of many female consumers involve use
of anti-perspirants and deodorants to reduce wetness and mal-
odour, and shaving or plucking to remove axillary hair. These
practices may be accompanied by visible and/or sensory irritation
and for some consumers (especially skin types Fitzpatrick III and
above) axillary skin darkening [37, 38].
Although there is a history of investigation into the effects of
shaving on facial skin in particular [39, 40], it is only recently that
comparative studies on axillary skin have been performed. Thus, it
is well reported that the primary cause of shaving-induced irrita-
tion is the removal of the uppermost layers of the skin (stratum
corneum). In the case of male facial shaving, up to 20% of the
material removed during the process is skin [40], and it is this
which ultimately leads to the post-shaving skin dryness and flaki-
ness associated with this area [39]. Similar observations have now
been made for the underarm, with the average proportion of skin
debris removed reported to be even higher at 36% [7]. Axillary
shaving also causes irritation because of physical damage (cuts,
nicks and a decrease in skin smoothness), and this further impairs
the natural barrier to exogenous irritants [7, 8, 41]. The initial
response to shaving is highly visible irritation (erythema; Fig. 3a)
[8, 41], which histamine iontophoresis has demonstrated occurs in
both the shaved vault and fossa areas, with neurogenic flare being
more prevalent in the latter (Fig. 3a; [7]). This is not surprising
given that axillary skin is characterized, as mentioned earlier, by
reduced barrier functionality compared with other body sites owing
to its enhanced cholesterol: ceramide ratio [28, 29]. More frequent
shaving has been shown to promote a higher level of visible
HF
EG
EG
EG
AG
SC
PE
SG
E
D
Figure 2 Histological section of axillary skin. Longitudinal section of
human axillary skin showing main anatomical features: stratum corneum
(SC), epidermis (E), dermis (D), hair follicle (HF), piloerector muscle (PE),
sebaceous gland (SG), eccrine sweat gland (EG) and apocrine gland (AG).
Notice the significant amount of epidermal folding. Staining is haematoxylin
and eosin. Scale bar represents 100 lm. (Image kindly provided by Prof.
Douglas Bovell, Glasgow Caledonian University).
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395 391
Axillary skin: biology and care R. L. Evans et al.
irritation, although this was not accompanied by significant
changes in composition and quality of the stratum corneum lipid
barrier over the study period [41]. A further insight into the
molecular basis of this irritation was provided by intradermal
microdialysis experiments, which showed that neurotrophin levels
(NGF and BDNF) increased in shaved underarms following an acid
challenge (similar to the low pH of most standard anti-perspirants)
[42], and confirmed that the inflammatory response to shaving
leads to the visible and/or sensory signs of irritation. There is also
evidence that the vault has adapted to frequent shaving, notably
by the development of a thickened epidermis [7]. We can conclude
that, while the axillary vault may have adapted to frequent shav-
ing, this adaptation may not be sufficient to fully protect the skin
from additional shaving events.
The biochemistry of skin darkening in general, which is driven
by an increase in melanin synthesis (melanogenesis), typically in
response to UV radiation, has been well documented in recent
reviews [22, 43, 44] and is an area of continuous development. In
brief, melanogenesis occurs in the pigment-producing cells of the
epidermis, the melanocytes. Exposure to UV enhances the activity
of the key enzyme tyrosinase, located in the melanosomes, small
vesicles in the cytoplasm of the melanocyte. Tyrosinase has two
functions. It catalyses the production of L-DOPA from L-tyrosine
and subsequent oxidation of L-DOPA to L-dopaquinone. The latter,
is then modified, via different pathways into either eumelanin
(brown-blackish colour) or pheomelanin (red-yellow in colour).
Tyrosinase is the main target for therapies for regulating skin col-
our and treating clinical conditions. From a cosmetic point of view,
there are also molecules known to affect the transfer of melanin
from the melanocyte to the keratinocytes (e.g. niacinamide) [45],
as well as agents that promote desquamation and loss of melanin-
containing corneocytes (e.g. retinoic acid) [46] and considerable
interest has been focussed here.
In the case of the axilla, it is irritation caused by shaving or
plucking, combined with anti-perspirant use, rather than exposure
to UV radiation, that leads to skin darkening in susceptible individ-
uals (Fig. 3b). However, it should be noted that other factors such
as increased Body Mass Index, which can lead to more underarm
rubbing, and background skin tone are also strongly correlated
with axillary darkening [47], in fact more so than either product
use or the hair removal method [47]. James et al. have proposed
that axillary skin darkening is best defined as mild PIHP, character-
ized by increased epidermal melanin production, following mild
irritation or stimulation of the skin [38, 48]. Histological
evaluation of female Filipino axillary skin showed that the trauma
of underarm hair plucking is associated with melanosome leakage
into the dermis and hence increased pigmentation, as well as
mononuclear cell and macrophage infiltration. Interestingly,
because hyperpigmented areas display greater melanosome release
into the dermis, and because the macrophage infiltration response
is associated with production of inflammatory cytokines, the cycle
is self-perpetuating as melanocytes are then stimulated to produce
more pigment-containing melanosomes. There is also a close rela-
tionship between the density of epidermal pigment, amount of der-
mal pigment and increased infiltration of macrophages. Dark skin
sites from hyperpigmented panellists exhibit significantly increased
anti-tyrosinase and/or anti-TRP1 staining, indicative of melanocyte
stimulation and increased melanogenesis [38, 49, 50]. These test
sites also demonstrate a tendency for increased transfer of pigment
to the spinous cells of the upper epidermis, in some cases forming
melanin caps over the nuclei [38]. As with general melanogenesis,
the points of intervention for modulating PIHP are the same,
namely tyrosinase inhibition, melanin transfer and control of des-
quamation of corneocytes containing residual melanin.
Assessment of axillary skin condition and skin caresolutions
As documented, it is established that shaving of axillary skin leads
to redness, dryness and soreness, and in certain skin types, this may
also result in hyperpigmentation. The condition of the axillary skin
can be assessed by a number of techniques. Thus, expert assessors
can visually score darkening, redness and dryness. Well-established
biophysics methods such as TEWL and corneosurfametry [8, 28]
have been successfully used under conditions that prevent emo-
tional or thermoregulatory sweating, to determine barrier integrity
in terms of water loss and physical quality. Increasingly, new meth-
ods such as confocal Raman spectroscopy have been applied to pro-
vide more detailed information on the concentration profiles of fatty
acids, cholesterol, key lipids, water and natural moisturizing factor
as a function of depth, of which the last two which can be used
together to determine stratum corneum thickness [29, 51, 52].
The observations obtained with all of the methods above support
a consistent picture; mild shaving and hair plucking activities
result in weakening of the skin barrier, which leads to poor desqua-
mation and dry, flaky skin. Repetitive or harsh shaving will lead to
an inflammatory response, which results in redness and ultimately
soreness and poor barrier repair. By this stage, a cycle of irritation
has been set up (Fig. 1), and the solution is to stop shaving, or
apply skin benefit actives to encourage enhanced barrier repair.
(a) (b)
Figure 3 Examples of (a) shaving-induced underarm erythema (notice red area of skin in the fossa in the lower half of the photograph), and (b) plucking-
induced axillary post-inflammatory hyperpigmentation (PIHP; notice darkened axillary skin, with higher levels in the skin folds/creases). [References: Fig. (a)
Unilever unpublished data (Axillary skin condition study. Port Sunlight, UK, 2011). Image used with individual consent. Fig. (b) Unilever unpublished data
(Axillary skin lightening study. Port Sunlight, UK, 2010). Image used with individual consent].
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395392
Axillary skin: biology and care R. L. Evans et al.
As mentioned in the introduction, dry, irritated skin can be
returned to normal function by the use of skin care formulations
that contain moisturizing and barrier-boosting actives [10–12], ofwhich five different classes have been suggested to be of importance
to axillary skin care. However, relatively few specific studies have
been reported. Those that have demonstrated that a successful
solution is to use an anti-perspirant roll-on formulation that
restores the moisture levels within the stratum corneum using
humectants, such as glycerol, and oils such as SSO [7, 53]. Endog-
enous glycerol is known to be a natural determinant of stratum
corneum hydration [54], whereas applied glycerol is effective in
enhancing stratum corneum hydration in sufferers of atopic derma-
titis [55], and in accelerating the recovery of barrier function in
individuals subject to tape stripping [56, 57]. It is most likely that
similar responses to applied glycerol occur in the damaged axilla.
The role of unsaturated triglycerides such as SSO is more complex.
The oil provides some occlusive benefits to irritated skin sites [58],
and presumably those damaged by hair removal. However, if occlu-
sion were the primary requirement, materials such as petrolatum
would be preferred, albeit with sensorial negatives. Sunflower seed
oil is chosen because it is a recognized source of essential fatty
acids, such as linoleic acid [59], which is incorporated into stratum
corneum lipids [60]. It has been further shown that linoleic acid
can also act as a PPAR activator [61, 62], which in turn promotes
epidermal regeneration [12], and it may also be metabolized to
13-hydroxyoctadecadienoic acid (13-HODE), which acts as an
anti-inflammatory and anti-proliferative [63, 64]. Thus, the
combination of glycerol and SSO, when delivered in roll-on format,
is uniquely effective at reducing shaving-induced axillary skin
irritation compared with a standard anti-perspirant control in just
3-4 days [7] (Fig. 4). It also improves self-assessment of the axillary
condition over the same time frame [7].
Compared to aqueous formulations, the problem with anhydrous
formulations is the incompatibility of the humectant glycerol with
the aluminium-containing anhydrous base. In this case, alterna-
tives include use of the humectant polyethylene glycol, which is an
effective substitute. Critically, SSO can still be included in the for-
mulation. This combination has also been shown to reduce shav-
ing-induced skin irritation relative to control formulations in just a
few days [65].
The glycerol/SSO combination has also been shown to be effec-
tive in control of axillary PIHP [66]. As documented previously,
the two actives are effective in the control of irritation (inflamma-
tion), and this alone will help prevent the initiation of hyperpig-
mentation. A clinical study on Latin American women using 4%
SSO alone has shown that both axillary erythema and dryness
were significantly reduced, as was visual hyperpigmentation. This
observation was supported by data from a skin-like coculture of
human melanocytes and keratinocytes (MelanoDerm R) which
showed that SSO increased the lightness of this substrate in a dose-
dependent manner. In addition, SSO inhibited melanogenesis in a
mouse melanoma cell assay [66]. Literature evidence suggest that
the active component of SSO is linoleic acid [67], which has been
shown to induce skin lightening in a clinical study on melasma
patients [68]. Thus, SSO appears to be effective against axillary
PIHP by reducing inflammation, promoting the loss of pigmented
cells (by PPAR activation) and potentially inhibiting melanogene-
sis.
Conclusions
It is clear that compared with other locations on the body surface,
the axilla is indeed a biologically unique site. Axillary skin has spe-
cial requirements based on the desire to avoid wetness and odour
and the requirement to remove hair, which brings the associated
risk of irritation, erythema and potentially hyperpigmentation. Cos-
metic science is able to provide solutions for these outcomes via
careful selection of appropriate skin care technology. In particular,
using humectants and oils containing essential fatty acids, as well
as occlusives and anti-irritants helps prevent shaving-induced irri-
tation. However, the scope still exists to develop improved formula-
tions for consumers using actives from the five groups of skin care
compounds identified in this study.
Acknowledgements
We thank Clive Harding for helpful discussions and suggestions
during the preparation of this manuscript, Prof. Douglas Bovell,
Glasgow Caledonian University, for permission to use the histologi-
cal section shown in Fig 2, and Unilever colleagues who provided
study data for illustrative purposes. All authors are direct employ-
ees of Unilever PLC, UK, who provided funding for figure prepara-
tion (Fig. 1) only during the preparation of this manuscript.
References
1. Lindberg, M. and Forslind, B. The skin as a
barrier. In: Dry Skin and Moisturozers:
Chemistry and Function (Loden, M. and
Maibach, H.I., eds), pp. 9–21. CRC Taylor
and Francis Group, Boca Raton, FL, USA
(2006).
2. Harding, C.R. The stratum corneum:
structure and function in health and
disease. Dermatol. Ther. 17, 6–15
(2004).
3. Elias, P., Wood, L.C. and Feingold, K.R.
Epidermal pathogenesis of inflammatory
dermatoses. Am. J. Contact Dermat. 10, 119
–126 (1999).
4. Marks, R., Leveque, J.-L. and Voegeli, R.
Section I. Stratum corneum anatomy and
Irritation after Provocation
0.00.20.40.60.81.01.21.41.6
0 2 4 6 8Day
Mea
n sc
ore
Test (with glycerol and SSO) Control
Figure 4 Skin care actives improve shaving-induced axillary irritation. An
aqueous roll-on formulation containing 4% glycerol and 4% sunflower seed
oil (SSO) significantly reduces axillary irritation after provocation compared
with a glycerol and SSO-free formulation (Control). The initial irritation was
generated using an exaggerated shaving and product use protocol in the
run-in phase. [Reference: Unilever unpublished data (Axillary skin condition
study. Port Sunlight, UK, 2006)].
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395 393
Axillary skin: biology and care R. L. Evans et al.
physiology. In: The Essential Stratum Corne-
um (Marks, R., Leveque, J.-L. and Voegeli,
R., eds), pp. 3–95. Martin Dunitz Ltd, Taylor
& Francis Group, London, UK (2002).
5. Scott, I.R. and Harding, C.R. Filaggrin
breakdown to water binding compounds
during development of the rat stratum cor-
neum is controlled by the water activity in
the environment. Dev. Biol. 115, 84–92
(1986).
6. Grubauer, G., Elias, P.M. and Feingold, K.R.
Transepidermal water loss: the signal for
recovery of barrier structure and function. J.
Lipid Res. 30, 323–333 (1989).
7. Turner, G.A., Moore, A.E., Marti, V.P.J. et al.
Impact of shaving and anti-perspirant use
on the axillary vault. Int. J. Cosmet. Sci. 29,
31–38 (2007).
8. Marti, V.P.J., Lee, R.S., Moore, A.E. et al. Effect
of shaving on axillary stratum corneum. Int.
J. Cosmet. Sci. 25, 193–198 (2003).
9. Summey, B.T. and Yosipovitch, G.. Itch
associated with dryness of the skin: the
pathophysiology and influence of moisturiz-
ers. In: Dry Skin and Moisturizers: Chemistry
and Function (Loden, M. and Maibach, H.I.,
eds), pp. 127–133. CRC Taylor and Francis
Group, Boca Raton, FL, USA (2006).
10. Rawlings, A.V., Scott, I.R., Harding, C.R.
and Bowser, P.A. Stratum corneum moistur-
ization at the molecular level. J. Invest.
Dermatol. 103, 731–740 (1994).
11. Harding, C.R., Watkinson, A., Rawlings, A.
V. and Scott, I.R. Dry skin, moisturization
and corneodesmolysis. Int. J. Cosmet. Sci.
22, 21–52 (2000).
12. Rawlings, A.V. Trends in stratum corneum
research and the management of dry skin
conditions. Int. J. Cosmet. Sci. 25, 63–95
(2003).
13. Fluhr, J.W., Bornkessel, A. and Berardesca,
E. Glycerol – Just a moisturizer? Biological
and biophysical effects. In: Dry Skin and
Moisturizers: Chemistry and Function (Loden,
M. and Maibach, H.I., eds), pp. 227–243.
CRC Taylor and Francis Group, Boca Raton,
FL, USA (2006).
14. Boury-Jamot, M., Sougrat, R., Tailhardat, M.
et al. Expression and function of aquaporins
in human skin: Is aquaporin-3 just a glyc-
erol transporter? Biochem. Biophys. Acta
1758, 1034–1042 (2006).
15. Morrison, D.S.. Petrolatum. In: Dry Skin and
Moisturizers: Chemistry and Function (Loden,
M. and Maibach, H.I., eds), pp. 289–298.
CRC Taylor and Francis Group, Boca Raton,
FL, USA (2006).
16. Rhodes, L.E. and Storey, A. Essential fatty
acids: Biological functions and potential
applications in the skin. In: Dry Skin and
Moisturizers: Chemistry and Function (Loden, M.
and Maibach, H.I., eds), pp. 319–340. CRC
Taylor and Francis Group, Boca Raton, FL,
USA (2006).
17. Wiechers, J.W., Dederen, C.J. and Rawlings,
A.V. Moisturization mechanisms: Internal
occlusion by orthorhombic lipid phase stabi-
lizers – a novel mechanism of action of
moisturization. In: Skin Moisturization
(Rawlings, A.V. and Leyden, J.J., eds), pp.
309–321. Informa Healthcare USA Inc.,
New York, USA (2009).
18. Pennick, G., Harrison, S., Jones, D. and
Rawlings, A.V. Superior effect of isostearyl
isostearate on improvement in stratum cor-
neum water permeability barrier function as
examined by the plastic occlusion test. Int. J.
Cosmet. Sci. 32, 304–312 (2010).
19. Elias, P.M., Hatano, Y. and Williams, M.L.
Basis for the barrier abnormality in atopic
dermatitis: Outside-inisde-outside pathogenic
mechanisms. J. Allergy Clin. Immunol. 121,
1337–1343 (2008).
20. Watkinson, A., Lee, R.S., Moore, A.E. et al.
Is the axilla a distinct skin phenotype? Int. J.
Cosmet. Sci. 29, 60 (2007).
21. Wilke, K., Wick, K., Keil, F.J. et al. A strat-
egy for correlative microscopy of large skin
samples: towards a holistic view of axillary
skin complexity. Exp. Dermatol. 17, 73–80
(2007).
22. Tobin, D.J. Biochemistry of human skin –
our brain on the outside. Chem. Soc. Rev.
35, 52–67 (2006).
23. Wilke, K., Martin, A., Terstegen, L. and Biel,
S.S. A short history of sweat gland biology.
Int. J. Cosmet. Sci. 29, 169–179 (2007).
24. Quinton, P.M., Elder, H.Y., McEwan
Jenkinson, D. and Bovell, D.L. Structure and
function of human sweat glands. In: Antiper-
spirants and Deodorants (Cosmetic Science &
Technology Series, Vol 20) (Laden, K. and
Felger, C.B., eds), pp. 17–57. Marcell Dekker
Inc., New York. (1999).
25. Sato, K. The physiology, pharmacology and
biochemistry of the eccrine sweat gland.
Rev. Physiol. Biochem. Pharmacol. 79, 51–
131 (1977).
26. Cowan-Ellsberry, C., McNameeb, P.M. and
Leazer, T. Axilla surface area for males and
females: measured distribution. Reg. Toxicol.
Pharmacol. 52, 46–52 (2008).
27. Watkinson, A., Lee, R., Moore, A. et al.
Identification of a barrier deficiency in the
stratum corneum of the axilla. J. Invest. Der-
matol. 117, 415 (2001).
28. Watkinson, A., Lee, R.S., Moore, A.E. et al.
Reduced barrier efficiency in axillary stra-
tum corneum. Int. J. Cosmet. Sci. 24,
151–161 (2002).
29. Wu, J.Q. and Kilpatrick-Livermore, L. Char-
acterizing the composition of underarm and
forearm skin using confocal raman spectros-
copy. Int. J. Cosmet. Sci. 33, 257–262
(2011).
30. Harding, C.R., Long, S., Richardson, J. et al.
The cornified cell envelope: an important
marker of stratum corneum maturation in
healthy and dry skin. Int. J. Cosmet. Sci. 25,
1–11 (2003).
31. Burry, J.S., Coulson, H.F., Esser, I. et al.
Erroneous gender differences in axillary skin
surface/sweat pH. Int. J. Cosmet. Sci. 23, 99
–107 (2001).
32. Williams, S., Davids, M., Reuther, T. et al.
Gender differences of in vivo skin surface pH
in the axilla and the effect of a standardized
washing procedure with tap water. Skin
Pharmacol. Physiol. 18, 247–252 (2005).
33. Sato, K., Kwang, W.-H., Saga, K. and Sato,
K.T. Biology of sweat glands and their
disorders. I. Normal sweat gland function. J.
Am. Acad. Dermatol. 20, 537–563 (1989).
34. Burry, J.S., Coulson, H.F. and Roberts, G.
Circadian rhythms in axillary skin surface
pH. Int. J. Cosmet. Sci. 23, 207–210
(2001).
35. Yosipovitch, G., Xiong, G.L., Haus, E. et al.
Time-dependent variations of the skin
surface barrier function in humans:
transepidermal water loss, stratum corneum
hydration, skin surface pH, and skin temper-
ature. J. Invest. Dermatol. 110, 20–24
(1998).
36. Parra, J.L., Paye, M. and EEMCO Group.
EEMCO guidance for the in vivo assessment
of skin surface pH. Skin Pharmacol. Appl.
Skin Physiol. 16, 188–202 (2003).
37. Taylor, S., Grimes, P., Lim, J. et al. Postin-
flammatory hyperpigmentation. J. Cut. Med.
Surg. 13, 183–191 (2009).
38. James, A.G., Pople, J.E., Parish, W.E. et al.
Histological evaluation of hyperpigmentation
on female Filipino axillary skin. Int. J. Cos-
met. Sci. 28, 247–253 (2006).
39. Bhaktaviziam, C., Mescon, H., Matoltsy, A.
G. and Shaving, I. Study of skin and
shavings. Arch. Dermatol. 88, 242–247
(1963).
40. Elden, H.R. Advances in understanding
mechanisms in shaving. Cosmet. Toiletries
100, 51–62 (1985).
41. Marti, V., Brennan, G., Clarke, P. et al.
Assessing the irritation potential of anti-per-
spirants. J. Invest. Dermatol. 117, 961
(2001).
42. Paterson, S., Schmelz, M., McGlone, F. et al.
Facilitated neurotrophin release in sensitized
human skin. Eur. J. Pain 13, 399–405
(2009).
43. Yamaguchi, Y., Brenner, M. and Hearing, V.
J. The regulation of skin pigmentation.
J. Biol. Chem. 282, 27557–27561 (2007).
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395394
Axillary skin: biology and care R. L. Evans et al.
44. Gillbro, J.M. and Olsson, M.J. The melano-
genesis and mechanisms of skin-lightening
agents – existing and new approaches. Int.
J. Cosmet. Sci. 33, 210–221 (2011).
45. Greatens, A., Hakazaki, T., Koshoffer, A.
et al. Effective inhibition of melanosome
transfer to keratinocytes by lectins and nia-
cinamide is reversible. Exp. Dermatol. 14,
498–508 (2005).
46. Craven, N.M. and Griffiths, C.E.M. Topical
retinoids and cutaneous biology. Clin. Exp.
Dermatol. 21, 1–10 (1996).
47. James, A.G., Pople, J., Moore, A. and Paris,
W. Factors influencing axillary skin
hyperpigmentation in Southeast Asia. J. Am.
Acad. Dermatol. 54, AB90 (2006).
48. Lacz, N.L., Vafaie, J., Kihiczak, N.I. and
Schwartz, R.A. Postinflammatory hyperpig-
mentation: a common but troubling condi-
tion. Int. J. Dermatol. 43, 362–365
(2004).
49. Tokofuku, K., Wada, I., Valencia, J.C. et al.
Oculocutaneous albinism types 1 and 3 are
retention diseases: mutation of tyrosinase or
Tryp1 can affect the processing of both
mutant and wild-type proteins. FASEB J.
15, 2149–2161 (2001).
50. Rad, H.H., Yamashita, T., Jin, H.-Y. et al.
Tyrosinase related proteisn suppress tyrosi-
nase-mediated cell death of melanocytes and
melanoma cells. Exp. Cell Res. 298,
317–328 (2004).
51. Egawa, M. and Tagami, H. Comparison of
the depth profiles of water and water-bind-
ing substances in the stratum corneum
determined in vivo by Raman spectroscopy
between the cheek and volar forearm skin:
effects of age, seasonal changes and artificial
forced hydration. Br. J. Dermatol. 158,
251–260 (2008).
52. Crowther, J.M., Sieg, A., Blenkiron, P. et al.
Measuring the effects of topical moisturizers
on changes in stratum corneum thickness,
water gradients and hydration in vivo. Br. J.
Dermatol. 159, 567–577 (2008).
53. Rawlings, A., Harding, C., Watkinson, A.
et al. The effect of glycerol and humidity on
desmospme degradation in stratum corneum.
Arch. Dermatol. Res. 287, 457–464 (1995).
54. Choi, E.H., Man, M.-Q., Wang, F. et al. Is
endogenous glycerol a determinant of stra-
tum corneum hydration in humans? J.
Invest. Dermatol. 125, 288–293 (2005).
55. Breternitz, M., Kowatzki, D., Langenauer, M.
et al. Placebo-controlled, double-blind,
randomized, prospective study of a glycerol-
based emollient on eczematous skin in
atopic dermatitis: biophysical and clinical
evaluation. Skin Pharmacol. Physiol. 21,
39–45 (2007).
56. Fluhr, J.W., Gloor, M., Lehmann, L. et al.
Glycerol accelerates recovery of barrier
function in vivo. Acta Derm. Venereol. 79,
418–421 (1999).
57. Fluhr, J.W., Darlenski, R. and Surber, C.
Glycerol and the skin: holistic approach to
its origin and functions. Br. J. Dermatol.
159, 23–34 (2008).
58. Loden, M. and Andersson, A.-C. Effect of
topically applied lipids on surfactant-irritated
skin. Br. J. Dermatol. 134, 215–220 (1996).
59. Prottey, C., Hartop, P.J. and Press, M. Cor-
rection of the cutaneous manifestations of
essential fatty acid deficiency in man by the
application of sunflower-seed oil to the skin.
J. Invest. Dermatol. 64, 228–234 (1975).
60. Wertz, P.W. and Downing, P.T. Metabolism
of linoleic acid in porcine epidermis. J. Lipid
Res. 31, 1839–1844 (1990).
61. Mayes, A.E.. PPARa activators: Petroselinic
acid as a novel skin benefit agent for
antiperspirants. Proceedings of the 22nd
IFSCC Congress, Edinburgh (2002).
62. Moya-Camerena, S.Y., Heuvel, J.P.V., Blan-
chard, S.G. et al. Conjugated linoleic acid is
a potent naturally occuring ligand and
activator of PPARa. J. Lipid Res. 40,
1426–1433 (1999).
63. Cho, Y. and Ziboh, V.A. Incorporation of
13-hyroxyoctadecadienoic acid (13-HODE)
into epidermal ceramides and phospholipids:
phospholipase C-catalyzed release of novel
13-HODE-containing diacylglycerol. J. Lipid
Res. 35, 255–262 (1994).
64. Ziboh, V.A. The significance of polyunsatu-
rated fatty acids in cutaneous biology. Lipids
31, S249–S253 (1996).
65. Fletcher, N.R., Massaro, M., Muscat, J. and
Turner, G.A. Anhydrous spray compositions
containing a particulate antiperspirant
active and a moisturising agent.
EP1909916B1 (2009).
66. James, A.G., Marti, V., Pople, J. and Paterson,
S. A sunflower seed oil-containing antiperspi-
rant for controlling axillary darkening in
Latin American women. J. Am. Acad. Derma-
tol. 56, AB172 (2007).
67. Ando, H., Funasaka, Y., Oka, M. et al.
Possible involvement of proteolytic degrada-
tion of tyrosinase in the regulatory effect of
fatty acids on melanogenesis. J. Lipid Res.
40, 1312–1316 (1999).
68. Lee, M.-H., Kim, H.-J., Ha, D.-J. et al.
Therapeutic effect of topical application of
linoleic acid and linomycin in combination with
betamethasone valerate in melasma patients. J.
Korean Med. Sci. 17, 518–523 (2002).
� 2012 Society of Cosmetic Scientists and the Societe Francaise de Cosmetologie
International Journal of Cosmetic Science, 34, 389–395 395
Axillary skin: biology and care R. L. Evans et al.