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Topical application of green and white tea extracts provides protection from solar-simulated ultraviolet light in human skin

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Tea is one of the most widely consumed beverages in the world and has been heralded for its antioxidant and anti- cancer properties. Green tea has received much interest because of the beneficial role polyphenols play in skin cancer prevention (1,2,3). Its benefits against UV-induced effects were first demonstrated in human skin by Elmets and co-workers (4). White tea is the least processed of the teas and may retain higher levels of polyphenols. In one study, white tea proved more effective than green tea in preventing intestinal tumorigenesis (5). However, there are no published data on white tea for the prevention of detri- mental ultraviolet radiation (UVR) effects on the skin. Multiple mechanisms contribute to UVR-induced carcino- genesis, including direct DNA damage and indirect damage secondary to reactive oxygen species (ROS) (6). UVR also induces cutaneous immunosuppression, potentially allow- ing dysplastic cells to go undetected and progress to neo- plasms (7). The overall goal of this study was to compare, in humans, the protective effects of topical white tea or green tea against markers of UVR damage that are associ- ated with immune suppression and carcinogenesis. This was accomplished by performing: (i) immunohistochemical analysis for oxidative DNA damage and for epidermal Langerhans cells (LCs) from biopsies obtained after in vivo irradiation of human skin in the presence or absence of the topical tea formulations; (ii) assessments of in vivo contact hypersensitivity using the contact sensitizer dinitrochloro- benzene (DNCB); and (iii) an analysis of UVR-induced epidermal LC depletion in vitro, using a skin explant model.
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Content Preview
DOI:10.1111/j.1600-0625.2008.00818.x
www.blackwellpublishing.com/EXD
Original Article
Topical application of green and white tea extracts
provides protection from solar-simulated ultraviolet
light in human skin
Melissa M. Camouse1, Diana Santo Domingo1, Freddie R. Swain1, Edward P. Conrad1, Mary S.
Matsui2, Daniel Maes2, Lieve Declercq3, Kevin D. Cooper1,4, Seth R. Stevens1,4 and Elma D. Baron1,4
1Department of Dermatology, University Hospitals Case Medical Center Cleveland, OH, USA;
2Estee Lauder Companies, Melville, NY, USA;
3Estee Lauder Companies, Oevel, Belgium;
4Department of Dermatology, Cleveland Veterans Affairs Medical Center, Cleveland, OH, USA
Correspondence: Elma D. Baron, MD, University Hospitals Case Medical Center, 11100 Euclid Ave., Lakeside 3500, Cleveland, OH 44106, USA,
Tel.: 2163684971, Fax: 2163680212, e-mail: elma.baron@uhhospitals.org
Accepted for publication 23 October 2008
Background: Tea polyphenols have been found to exert bene?cial
Results: Topical application of green and white tea offered
effects on the skin via their antioxidant properties.
protection against detrimental effects of UV on cutaneous
immunity. Such protection is not because of direct UV absorption
Aims: We sought to determine whether topical application of
or sunscreen effects as both products showed a sun protection
green tea or white tea extracts would prevent simulated solar
factor of 1. There was no signi?cant difference in the levels of
radiation-induced oxidative damages to DNA and Langerhans
protection afforded by the two agents. Hence, both green tea and
cells that may lead to immune suppression and carcinogenesis.
white tea are potential photoprotective agents that may be used in
Methods: Skin samples were analysed from volunteers or skin
conjunction with established methods of sun protection.
explants treated with white tea or green tea after UV irradiation.
Key words: contact hypersensitivity – ())-epigallocatechin-3-
In another group of patients, the in vivo immune protective
gallate – green tea – Langerhans cells – photoprotection –
effects of green and white tea were evaluated using contact
polyphenols – white tea
hypersensitivity to dinitrochlorobenzene.
Please cite this paper as: Topical application of green and white tea extracts provide protection from solar-simulated ultraviolet light in human skin.
Experimental Dermatology 2009; 18: 522–526.
Introduction
secondary to reactive oxygen species (ROS) (6). UVR also
induces cutaneous immunosuppression, potentially allow-
Tea is one of the most widely consumed beverages in the
ing dysplastic cells to go undetected and progress to neo-
world and has been heralded for its antioxidant and anti-
plasms (7). The overall goal of this study was to compare,
cancer properties. Green tea has received much interest
in humans, the protective effects of topical white tea or
because of the bene?cial role polyphenols play in skin
green tea against markers of UVR damage that are associ-
cancer prevention (1,2,3). Its bene?ts against UV-induced
ated with immune suppression and carcinogenesis. This
effects were ?rst demonstrated in human skin by Elmets
was accomplished by performing: (i) immunohistochemical
and co-workers (4). White tea is the least processed of the
analysis for oxidative DNA damage and for epidermal
teas and may retain higher levels of polyphenols. In one
Langerhans cells (LCs) from biopsies obtained after in vivo
study, white tea proved more effective than green tea in
irradiation of human skin in the presence or absence of the
preventing intestinal tumorigenesis (5). However, there are
topical tea formulations; (ii) assessments of in vivo contact
no published data on white tea for the prevention of detri-
hypersensitivity using the contact sensitizer dinitrochloro-
mental ultraviolet radiation (UVR) effects on the skin.
benzene (DNCB); and (iii) an analysis of UVR-induced
Multiple mechanisms contribute to UVR-induced carcino-
epidermal LC depletion in vitro, using a skin explant
genesis, including direct DNA damage and indirect damage
model.
ª No claim to original US government works
522
Journal compilation ª 2009 Blackwell Munksgaard, Experimental Dermatology, 18, 522–526

Protection from ssUVR by topical application of green and white tea extracts
Materials and methods
and 50 mJ ? cm2 were enrolled. This is equivalent to about
2–7 J ? cm2 of full spectrum UV (i.e. UVA + UVB) delivered
All procedures were approved by the Institutional Review
by the solar simulator. Excluded were subjects with signi?-
Board of University Hospitals of Cleveland. Volunteers
cant medical and ? or dermatological history, abnormal
were enrolled after written informed consent.
photosensitivity and recent signi?cant sun exposure.
Subjects were randomized into three treatment groups:
Immunohistochemical analyses of skin biopsies
no treatment, topical green tea and topical white tea.
Ten healthy volunteers, FST I-III were enrolled and under-
Each treatment group was further subdivided into three
went standard minimum erythema dose (MED) testing using
groups according to the dose of ssUVR (i.e. 0, 0.75·
solar-simulated ultraviolet radiation (ssUVR) exposure
MED or 2· MED). In vivo sun protection factor (SPF)
(1000 W xenon arc lamp, 290–400 nm; Oriel Corporation,
testing of the two products performed on the ?rst ?ve
Stratford, CT, USA). The irradiance of the light source was
subjects revealed an average SPF of 1. Contact hypersensi-
measured using an IL1700 radiometer (International Light,
tivity assay was performed similar to previous publications
Newburyport, MA, USA), with a UVA and a UVB sensor.
(8,9). Brie?y, the test product was applied 15 min prior
Twenty-four hours later, ssUVR-irradiated sites were analy-
to ssUVR irradiation, as well as immediately after irradia-
sed via colorimetry (Minolta CR 300 chromometer, Tokyo,
tion. Three days later, sensitization was performed on the
Japan) and MED was calculated as the ssUVR dose that
ssUVR-irradiated site with 40 lg ? 38 ll of DNCB. Two
results in erythema equivalent to a delta a of 2.5. Three areas
weeks later, DNCB elicitation was performed on the con-
on the buttock, each measuring 6 · 8 cm, were then chosen
tralateral arm using ?ve graded concentrations of DNCB
for test product application (one product per skin site), con-
(0–0.0625%). Forty-eight hours later, the elicitation sites
taining either green tea, white tea or vehicle. Tea extracts
were evaluated clinically and by measurement of skin fold
were formulated in a vehicle containing deionized water, 1,3
thickness (SFT) (Mitutuyo micrometer, Tokyo, Japan).
butylene glycol, carbopol 980 triethanolamine and methyl
For each subject, the contact hypersensitivity (CHS)
paraben. Both investigator and subject were blinded to the
response was evaluated by the total millimetre increase in
identity of the test agents. Each test agent was applied at a
SFT. Mean SFT increases were calculated for each of the
dose of 2.5 mg ? cm2 and allowed to dry for 15 min prior to
study groups and differences analysed by unpaired t-tests
ssUVR-irradiation with 2· the MED. Repeat application of
(P < 0.05).
products was performed immediately after ssUVR exposure.
An additional skin area that did not receive any product
Analysis of LCs using a skin explant model
application was also irradiated with 2· MED of ssUVR to
The effects of white tea and green tea were examined in vi-
serve as an untreated UV-irradiated control. Seventy-two
tro using a skin explant model. Discarded abdominal skin
hours later, a 4-mm punch biopsy was obtained from each of
tissue from a 31-year-old female who underwent plastic
the four irradiated sites. A punch biopsy was also obtained
surgery was obtained. The tissue was divided into 51 biop-
from an untreated, unirradiated site. Tissue samples were
sies (B 12 mm) isolated and maintained in basal essential
embedded in optimal cutting temperature (OCT) and frozen
medium (BEM) survival media. These biopsies were then
at )70°C for immunostaining using anti-CD1a (1:100)
treated at a dose of 2 mg ? cm2 with test material identical
(Pharmingen, San Diego, CA, USA) for epidermal LCs, and
to that used in the in vivo clinical study; either vehicle,
anti-8-hydroxy-2¢-deoxyguanosine (OHdG) (1:50) (Trevigen,
white tea or green tea, 4 h prior to UV exposure. The tis-
Gaithersburg, MD) to detect oxidative DNA damage. Appro-
sues were then irradiated using an Oriel solar simulator
priate isotype controls and manufacturer-recommended pro-
with Xenon lamp (900 W ? cm2). Using 1.78 J ? cm2 as the
tocols were utilized. After developing with diaminobenzidine
estimated UV dose corresponding to 1 MED for this skin
(DAB) and counterstaining with methyl green, tissue sections
type (FST II), the biopsies were exposed to a range of 0–
were analysed using Optimas Image Analyzer, which calcu-
3.0 MED. The untreated and vehicle-treated tissue samples
lated the percentage of positively stained areas per 40· ?eld.
were exposed to doses of 0, 0.45 (0.25 MED), 0.89 (0.5
Results were summarized as the average of ?ve 40· ?elds per
MED), 1.78 (1.0 MED), 3.56 (2.0 MED) and 5.34 J ? cm2
tissue section. Paired t-tests were used to analyse differences
(3.0 MED), while the tea-treated samples were exposed to
between experimental and control skin samples, and a value
doses of 0, 0.89, 1.78 and 3.56 J ? cm2. Twenty-four hours
of P < 0.05 was considered signi?cant.
after exposure, the tissue samples were cut and allocated
for freezing or paraf?n embedding, from which 5-lm serial
In vivo contact hypersensitivity assay to
sections were immunolabelled with anti-CD1a and visual-
dinitrochlorobenzene
ized using DAB or FITC. Frozen tissues were treated with
Ninety healthy volunteers from 18 to 60 years of age, with
dispase to separate the epidermis for horizontal examina-
Fitzpatrick skin types I-III, and MED values between 20
tion, for better evaluation of LC dendricity. Vertical
ª No claim to original US government works
Journal compilation ª 2009 Blackwell Munksgaard, Experimental Dermatology, 18, 522–526
523

Camouse et al.
sections across the entire epidermis were taken into
Oxidative DNA damage levels
account for quanti?cation of the number of residual LC.
18
No UV
16
UV only
14
UV + Vehicle
Results
12
UV + WT
10
UV + GT
Both green tea and white tea partially prevented
8
UV-induced depletion of CD1a+ cells and UV-
6
induced generation of 8-OHdG in healthy subjects
4
% 8-OHdG staining
irradiated in vivo
2
0
Figure 1 shows the mean percentage of CD1a+ per unit
area in each experimental condition from a total of 10
Figure 2. Oxidative damage was measured via levels of 8-hydroxy-2¢-
volunteers. After receiving 2 MED of ssUVR, untreated
deoxyguanosine (OhdG) staining in skin biopsies obtained 72 h after a
single 2 MED dose of SSR. Untreated and vehicle-treated skin showed
skin and vehicle-treated skin showed an almost identical
increased 8-OhdG, whereas 8-OhdG levels in white tea (WT)-treated
reduction (approximately 57%) in the level of CD1a+
and green tea (GT)-treated skin were not different from control
staining compared with unirradiated skin. This indicates
unirradiated skin.
that the vehicle alone offered no protection against CD1a
depletion. Pretreatment with either white tea or green tea
the level of protection against UV-induced 8-OHdG forma-
resulted in signi?cantly higher percentages of CD1a+
tion (P = 0.08).
staining compared with vehicle-protected skin (P = 0.002
and 0.003, respectively). UV-irradiated skin treated with
In-vivo CHS assay
white tea showed a 22% reduction, and UV-exposed
A total of 90 subjects, 34 females and 56 males, with age
green tea-treated skin showed a 35% reduction in
range of 19–58 years (mean 28 years), Fitpatrick skin types
CD1a+ staining relative to unirradiated skin. There was
I–III, MED of 20–50 mJ ? cm2 UVB or 2–7 J ? cm2 full spec-
no statistical difference between green tea versus white
trum UV (i.e. UVA + UVB) completed the CHS portion of
tea
in
terms
of
protection
against
LC
depletion
the study. In vivo SPF testing in the ?rst ?ve subjects, con-
(P = 0.09).
?rmed that both products had an SPF of 1 (mean white tea
Similarly, application of either green tea or white tea
SPF = 1.21 and mean green tea SPF = 1.05). Results of the
showed partial prevention of UV-induced oxidative DNA
CHS assay are presented in Fig. 3 for the untreated (i.e. no
damage in the form of 8-OHdG (Fig. 2). Exposing skin to
topical test agent) versus the test agent-treated groups across
2· MED of ssUVR resulted in 40% increase in 8-OHdG,
all three doses of ssUVR (0, 0.75 and 2· MED). The unirra-
relative to unirradiated skin. Application of vehicle resulted
diated test agent-treated controls (0 MED groups) had
in an even higher (69%) increase in 8-OHdG. However,
similar CHS responses (untreated = 3.55 ± 0.55, green
levels of 8-OHdG in ssUVR-irradiated skin pretreated with
tea = 3.49 ± 1.26, white tea = 3.6 ± 1.09 mm SFT), indicat-
white tea and green tea were not signi?cantly different
ing that green tea and white tea, by themselves, did not alter
from control unirradiated skin (P = 0.95 nd 0.12, respec-
DNCB sensitization rates. In the groups not treated with
tively), and were signi?cantly different from vehicle-treated
skin (P = 0.002 and 0.0001, respectively). Again, there was
no signi?cant difference between green tea and white tea in
Mean contact hypersensitivity (CHS) responses
5.00
Control
Epidermal Langerhans cells
4.00
Green tea
No UV
White tea
30
UV only
3.00
25
UV + Vehicle
2.00
UV + WT
20
UV + GT
1.00
15
Skin fold thickness (mm) 0.00
10
0
0.75
2
% CD1a+ staining
5
Figure 3. Each vertical bar represents an n of 10 subjects. X-axis
denotes the amount of UV irradiation, expressed in MED. Y-axis
0
denotes degree of contact hypersensitivity response to
Figure 1. Biopsies obtained 72 h after a single simulated solar radiation
dinitrochlorobenzene (DNCB), expressed as total millimetre increase in
(SSR) irradiation of 2 MED showed decreased epidermal CD1a+
skin fold thickness (SFT) over the DNCB elicitation sites. There was a
Langerhans cells (LC) in untreated and vehicle-treated skin. White tea
trend towards greater contact hypersensitivity (CHS) responses in green
(WT) and green tea (GT) application 15 min prior and immediately after
tea and white tea-treated subjects compared with untreated subjects,
irradiation partially prevented SSR-induced LC depletion.
in the 0.75 and 2 MED groups.
ª No claim to original US government works
524
Journal compilation ª 2009 Blackwell Munksgaard, Experimental Dermatology, 18, 522–526

Protection from ssUVR by topical application of green and white tea extracts
topical test agents, there was a signi?cant difference in
(a)
Dose-dependent depletion of Langerhans cells
immune response (P = 0.01) between unirradiated and
in ex vivo skin
25
irradiated (0.75 MED) subjects, which was not observed in
1 MED
20
either white or green tea subjects. In contrast, the immune
15
response of subjects who received 0.75 MED but who were
10
pretreated with either green tea or white tea was not signi?-
5
cantly different from the immune response of unirradiated
Number of LC/mm
0
0
1
2
3
4
5
6
controls (P = 0.31 and 0.48, respectively). However, within
SSR dose (J/cm2)
each ssUVR dose group, there was no signi?cant difference
(b) Dose-dependent effect of SSR on Langerhans
cells in ex vivo skin treated with white tea
between unprotected control versus white tea or unprotected
18
16
control versus green tea subjects (P = 0.35 and 0.30 for white
14
tea; P = 0.63 and 0.20 for green tea) although the treated
12
10
subjects consistently demonstrated higher CHS responses.
8
6
Vehicle
This may be because of the wide variability of CHS responses
4
White tea
when measured by SFT, which may limit the power to detect
2
Number of LC/mm
0
statistically signi?cant differences with an n = 10 per dose
0
1
2
3
4
5
6
group. The trend, however, suggests that tea-treated subjects
SSR dose (J/cm2)
had greater preservation of their CHS response after ssUVR
(c)
Dose-dependent effect of SSR on Langerhans
cells in ex vivo skin treated with green tea
exposure, relative to untreated subjects.
20
15
Ex vivo skin explant model
10
Results are expressed as the residual number of LC per
Vehicle
mm2 epidermis as a function of ssUVR dose. The effect of
5
Green tea
UV exposure on the sites that were not treated by either
Number of LC/mm
0
green or white tea was observed as a dose-dependent
0
1
2
3
4
SSR dose (J/cm2)
decrease in the number of LC per mm2 epidermis (Fig. 4a).
Similarly, sites treated with vehicle showed a dose-depen-
Figure 4. (a) Skin explant experiments showed decreasing numbers of
dent decrease in LC numbers. In contrast, skin treated with
Langerhans cells with increasing SSR dose. Above data were obtained
from unprotected skin harvested from an individual with FST II;
white tea showed no decrease in the number of LC per
estimated MED was less than 2 J ? cm2 (b) Compared with vehicle-
mm epidermis, up to a dose of 3.56 J ? cm2. This dose is
treated skin explants, white tea-treated skin demonstrated retention of
roughly equivalent to 2 MED based on the phototype of
Langerhans cells after SSR irradiation (c) Green tea-treated skin explants
this skin explant (Fig. 4b). Similar to white tea, green tea
also demonstrated better retention of Langerhans cells relative to
also prevented a decrease in the number of LC per mm2
vehicle-treated skin, after SSR irradiation.
epidermis, up to a dose of 3.56 J ? cm2 (Fig. 4c).
protection agents, as con?rmed by a consensus paper by
Discussion
sun protection experts worldwide (8). UV diminishes both
epidermal concentration and function of LCs, the dendritic
Despite the increased public awareness of the dangers of
antigen presenting cells responsible for induction of immu-
solar UV exposure, the incidence of both melanoma and
nity in the skin (15–17). Within hours of UV-exposure,
non-melanoma skin cancers continues to rise at an alarm-
LCs begin to migrate from the epidermis without the func-
ing rate (National Cancer Statistics 2005). Whereas UVB is
tional maturity to produce an effective immune response
the spectrum that primarily causes direct DNA damage,
(15,18). The immature LCs preferentially activate Th2 cells,
UVA likewise exerts detrimental effects via the production
resulting in an increased generation of T cells with suppres-
of ROS (6). As greater than 90% of the UV radiation that
sor ? regulatory function. Oxidative stress from UV exposure
reaches the earth’s surface is UVA, the role of UVA in skin
also induces nucleic acid base modi?cations such as the
carcinogenesis cannot be ignored and has become a major
formation of 8-OHdG, which was also evaluated in this
focus of research (10). UVA, as well as UVB, can suppress
study. Previous studies have shown that even without UV
the immune system, and studies have con?rmed that better
irradiation, there is some amount of 8-OHdG that will be
protection against UVA leads to improved immune pro-
detectable in tissue (19). This amount substantially
tection (9,11–14), again suggesting that UVA-triggered
increases with UVR exposure and via base excision repair
photooxidative mechanisms need to be addressed by sun
pathways, returns to near normal levels by 72–96 h (19).
protection
agents.
The
contact
hypersensitivity
assay
Hence, although we could have obtained more robust
remains a valid tool in the in vivo analysis of sun
increases in 8-OHdG at earlier time-points (e.g. within
ª No claim to original US government works
Journal compilation ª 2009 Blackwell Munksgaard, Experimental Dermatology, 18, 522–526
525

Camouse et al.
24 h of UV irradiation), the levels detected at 72 h may be
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15 Granstein R D, Matsui M S. UV radiation-induced immunosuppression and skin
cancer. Cutis 2004: 74: 4–9.
immune system. It is also the ?rst demonstration of the
16 Bestak R, Halliday G M. Chronic low dose UVA irradiation induces local sup-
prevention of UV immune suppression via topical applica-
pression of contact hypersensitivity, Langerhans cell depletion and suppressor
cell activation in C3H ? HeJ mice. Photochem Photobiol 1996: 64: 969–974.
tion of white tea. Overall, the two products performed to a
17 Dumay O, Karam A, Vian L et al. Ultraviolet AI exposure of human skin results
comparable degree. Our results con?rm that photoprotec-
in Langerhans cell depletion and reduction of epidermal antigen-presenting
cell function: partial protection by a broad-spectrum sunscreen. Br J Dermatol
tive effects of polyphenols involve the prevention of UV-
2001: 144: 1161–1168.
18 Shreedhar V K, Pride M W, Sun Y et al. Origin and characteristics of ultraviolet-B
induced LC depletion as was shown after in vivo irradiation
radiation-induced suppressor T lymphocytes. J Immunol 1998: 161: 1327–1335.
of human skin, as well as by an in vitro skin explant model.
19 Ahmed N U, Ueda M, Nikaido O, Osawa T, Ichihashi M. High levels of 8-
hydroxy-2¢-deoxyguanosine appear in normal human epidermis after a single
The fact that both products had an SPF of 1 also con-
dose of ultraviolet radiation. Br J Dermatol 1999: 140: 226–231.
?rmed that their protective effects on the skin’s immune
20 Wright T I, Spencer J M, Flowers F P. Chemoprevention of nonmelanoma skin
cancer. J Am Acad Dermatol 2006: 54: 933–946.
system did not result from direct UV absorption or a ‘sun-
21 Afaq F, Mukhtar H. Botanical antioxidants in the prevention of photocarcino-
genesis and photoaging. Exp Dermatol 2006: 15: 678–684.
screen effect’. In light of these observed bene?ts from topi-
22 Katiyar S K, Elmets C A, Agarwal R, Mukhtar H. Protection against ultraviolet-
cal tea extracts, we recommend that tea polyphenols be
B radiation-induced local and systemic suppression of contact hypersensitivity
and edema responses in C3H ? HeN mice by green tea polyphenols. Photochem
considered among compounds that could be developed as
Photobiol 1995: 62: 855–861.
photoprotective agents that may be used in conjunction
23 Katiyar S K, Mukhtar H. Green tea polyphenol ())-epigallocatechin-3-gallate
treatment to mouse skin prevents UVB-induced in?ltration of leukocytes,
with established sun protection strategies such as sunsc-
depletion of antigen-presenting cells, and oxidative stress. J Leukoc Biol 2001:
69: 719–726.
reens, protective clothing and sun avoidance. Interestingly,
24 Katiyar S K, Challa A, McCormick T, Cooper K, Mukhtar H. Prevention
despite differences in the processing of white tea, believed
of UVB-induced immunosuppression in mice by the green tea polyphenol
())-epigallocatechin-3-gallate may be associated with alterations in IL-10- and
to result in slightly higher polyphenolic content, it did not
IL-12 production. Carcinogenesis 1999: 20: 2117–2124.
signi?cantly differ in the ability to provide immune protec-
25 Hsu S, Dickinson D, Borke J et al. Green tea polyphenol induces caspase 14 in
epidermal keratinocytes via MAPK pathways and reduces psoriasiform lesions
tive bene?ts from green tea. However given white tea’s
in the ?aky skin mouse model. Exp Dermatol 2007: 16: 678–684.
26 Puch F, Samson-Villeger S, Guyonnet D et al. Consumption of functional
lighter colour, it may prove to be more acceptable in topi-
fermented milk containing borage oil, green tea and vitamin E enhances skin
cal preparations intended for regular use on areas such as
barrier function. Exp Dermatol 2008: 17: 668–674.
the face.
ª No claim to original US government works
526
Journal compilation ª 2009 Blackwell Munksgaard, Experimental Dermatology, 18, 522–526

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