Content uploaded by Chul-Sung Huh
Author content
All content in this area was uploaded by Chul-Sung Huh on Mar 01, 2023
Content may be subject to copyright.
J. Microbiol. Biotechnol.
J. Microbiol. Biotechnol. (2015), 25(12), 2160–2168
http://dx.doi.org/10.4014/jmb.1509.09021
Research Article
jmb
Review
Clinical Evidence of Effects of Lactobacillus plantarum HY7714 on
Skin Aging: A Randomized, Double Blind, Placebo-Controlled Study
Dong Eun Lee
1†
, Chul-Sung Huh
2†
, Jehyeon Ra
1
,
Il-Dong Choi
1
, Ji-Woong Jeong
1
, Sung-Hwan Kim
1
,
Ja Hyun Ryu
3
, Young Kyoung Seo
3
, Jae Sook Koh
3
, Jung-Hee Lee
1
, Jae-Hun Sim
1
, and Young-Tae Ahn
1
*
1
Korea Yakult Co., Ltd., Yongin 446-901, Republic of Korea
2
Graduate School of International Agricultural Technology, Institute of Green Bio Science & Technology, Seoul National University,
Pyeongchang 232-916, Republic of Korea
3
Dermapro Skin Research Center, DERMAPRO Ltd., Seoul 137-843, Republic of Korea
Introduction
Skin aging has intrinsic and extrinsic components.
Intrinsic aging is related to genetic factors and is a set of
physiologic processes related to the passage of time that
includes thinning of epidermal and dermal skin layers and
increasing dryness [4, 25]. Extrinsic aging is caused by
environmental factors such as UV-radiation, or toxins such
as cigarette smoke. The extrinsic skin-aging process is
characterized by coarse wrinkles, loss of elasticity, epidermal
thickening, dryness, laxity, rough appearance, and
pigmentation disorder [4, 24]. The most marked age-related
changes occur on the face, neck, forearm, and dorsal hands
[27]. Extrinsic and intrinsic aging signs are combined with
the passage of time and accelerate the aging process mainly
at these areas. Although intrinsic and extrinsic aging are
triggered by different factors, both involve similar molecular
mechanisms [18, 25, 27]. The benefits of probiotics on gut
health have been extensively researched [3]. Probiotics
alter the composition of the intestinal microbiome, produce
antimicrobial substances, and stimulate the body's immune
response [16]. There is now accumulating evidence to
suggest that probiotics are also able to regulate protective
mechanisms in the skin [11]. Recent clinical trials have
shown protective effects of dietary supplements containing
Lactobacillus johnsonii
alone [17] or combined with carotenoids
Received: September 7, 2015
Revised: September 23, 2015
Accepted: September 25, 2015
First published online
October 2, 2015
*
Corresponding author
Phone: +82-70-7835-6037;
Fax: +82-31-8005-7831;
E-mail: ytahn@re.yakult.co.kr
†
These authors contributed
equally to this work.
pISSN 1017-7825, eISSN 1738-8872
Copyright
©
2015 by
The Korean Society for Microbiology
and Biotechnology
The beneficial effects of probiotics are now widely reported, although there are only a few
studies on their anti-aging effects. We have found that
Lactobacillus plantarum
HY7714
(HY7714) improves skin hydration and has anti-photoaging effects, and in the present study,
we have further evaluated the anti-aging effect of HY7714
via
a randomized, double blind,
placebo-controlled clinical trial. The trial included 110 volunteers aged 41 and 59 years who
have dry skin and wrinkles. Participants took 1 × 10
10
CFU/day of HY7714 (probiotic group)
or a placebo (placebo group) for 12 weeks. Skin hydration, wrinkles, skin gloss, and skin
elasticity were measured every 4 weeks during the study period. There were significant
increases in the skin water content in the face (
p
< 0.01) and hands (
p
< 0.05) at week 12 in the
probiotic group. Transepidermal water loss decreased significantly in both groups at weeks 4,
8, and 12 (
p
< 0.001 compared with baseline), and was suppressed to a greater extent in the
face and forearm in the probiotic group at week 12. Volunteers in the probiotic group had a
significant reduction in wrinkle depth at week 12, and skin gloss was also significantly
improved by week 12. Finally, skin elasticity in the probiotic group improved by 13.17%
(
p
< 0.05 vs. controls) after 4 weeks and by 21.73% (
p
< 0.01 vs. controls) after 12 weeks. These
findings are preliminary confirmation of the anti-aging benefit to the skin of
L. plantarum
HY7714 as a nutricosmetic agent.
Keywords:
Anti-wrinkle,
Lactobacillus plantarum
, skin elasticity
,
skin gloss, skin hydration
Probiotics Ameliorate Skin Aging 2161
December 2015
⎪
Vol. 25
⎪
No. 12
[2] against early UV-induced skin
via
regulation of immune
cells and inflammatory cytokines. Other trials have shown
that atopic dermatitis and dry skin are relieved by
probiotic supplements [6, 9, 12, 20]. Recent experiments in
hairless mice have suggested that in addition to regulating
immune responses in the skin, orally administered probiotics
may exert anti-aging effects by suppressing wrinkle formation
and increasing skin elasticity [22, 23]. Furthermore, our
recent experiments in hairless mice have shown that oral
administration of
L. plantarum
HY7714 (HY7714) exerts
anti-photoaging effects through reduction of wrinkle
formation and suppression of epidermal thickening [14] and
that skin hydration increases in association with increasing
ceramide level
via
regulation of serine palmitoyltransferase
and ceramidase expression in the mice skin [19]. Based on
these findings, in this study, we have evaluated the anti-
aging effects of HY7714 in humans
via
a randomized
controlled clinical trial. Changes in parameters, including
dryness, wrinkles, gloss, and elasticity, were compared in a
group of Korean women aged 41 to 59 years with wrinkles
and dry skin.
Materials and Methods
Dietary Supplements
HY7714 was isolated from the breast milk of healthy women,
and a dietary supplement with 1 × 10
10
CFU per packet HY7714
was used as the probiotic agent. The placebo comprised the same
product without HY7714.
Study Volunteers
We recruited 129 healthy women aged 41 to 59 years. Inclusion
criteria were corneometer-confirmed dry skin (readings below 48
arbitrary units and crow’s feet greater than grade 4, as described
in the standard operating procedures of Dermapro Ltd., Seoul,
Korea). The clinical trial was conducted in accordance with good
clinical practice guidelines, and was approved by a local ethics
committee (Dermapro Ltd. Institutional Review Board) (DICN14001).
All study participants gave written consent to participate in the
study after they had been informed of the purpose of and the
expectations from the study. Of 129 healthy female volunteers
who were initially included in the trial 110 completed the study
and were included in the final analysis.
Exclusion Criteria
1. Pregnancy, possible pregnancy, or lactating
2. Medication or a medical history that may affect the skin’s
response
3. Any active skin disease that may interfere with the study’s
aim
4. Taking oral or topical steroid medication within 6 months of
the start of the study
5. The use of anti-inflammatory, corticoid, retinoid, or laser
therapies within 3 months of the start of the study
6. Participation in a previous study without an appropriate
intervening period between the studies
7. The presence of a chronic disease, including diabetes, asthma,
and high blood pressure
8. The presence of serious renal disorders or hepatic dysfunction
9. The presence of damaged skin in or around the measurement
sites, including sunburn, uneven skin tones, tattoos, scars, or
other forms of disfiguration
10. History of excessive exposure to sunlight or UV radiation
Study Design
This randomized, double blind, placebo-controlled clinical trial
was accepted and conducted by Dermapro Ltd. (Seoul, Korea).
This trial was conducted with study participants divided into
probiotic (
n
= 61) and placebo (
n
= 49) groups. Participants in the
probiotic group consumed 2 g daily of a powder containing
HY7714 (1 × 10
10
CFU) for 12 weeks. The participants (
n
=49) in
the placebo group consumed an identical powder without
HY7714 for 12 weeks. The skin condition of each subject was
assessed by dermatologists at baseline and at 4, 8, and 12 weeks
after initiation of the study. All participants washed their face and
then rested for 30 min in a climate-controlled waiting room
(temperature 22 ± 2°C, relative humidity 50 ± 5%) prior to each
skin examination in order to maintain homogeneous environmental
and measurement conditions as much as possible.
Skin Hydration
Skin hydration was measured in the stratum corneum of the
cheek (using the intersection of a vertical line from the corner of
the eye and a horizontal line from the tip of the nose as the
sampling point), the forearm, and the hand using a corneometer
(CM825; Courage and Khazaka Electronic GmbH, Cologne,
Germany). This device measures the variation in the electrostatic
capacity, which is dependent on the moisture content in the
stratum corneum. Measurements are reported in arbitrary units of
the electrostatic capacity. Transepidermal water loss from the
face, forearm, and hand were measured using a vapometer
(SWL4001, Delfin, Finland). This device has a humidity sensor in a
cylindrical measurement chamber that records changes in relative
humidity inside the chamber during the measurement and
automatically calculates transepidermal water loss (g/m
2
h). All
hydration and water loss measurements were performed three
times at each point and the averages were used in the analysis.
Three-Dimensional Imaging for Analysis of Facial Skin Wrinkles
Facial wrinkles were measured using a 3D skin imaging system
(PRIMOS Premium; GFMesstechnik GmbH, Teltow, Germany)
that makes optical 3D measurements based on digital stripe
projections using digital micromirror device technology. This
system permits a quantitative analysis of wrinkles at the skin
2162 Lee et al.
J. Microbiol. Biotechnol.
surface. Skin wrinkles were measured at the outer corners of the
left or right eye and analyzed in terms of the parameters described
in Table 1.
Skin Gloss
Facial skin gloss was measured by a glossmeter (Delfin
Technologies, Kuopio, Finland). This device consists of a 635 nm
red semiconductor diode laser and a mirror in a chamber. When
the chamber is placed on the skin, skin gloss is measured by the
degree of specular or light scattering. Skin gloss was measured
three times at the left or right cheek at the point where a vertical
line from the pupil meets a horizontal line from the end of the
nose, and the average values of the measurements were used in
the analysis.
Skin Elasticity
Skin elasticity was measured by using a cutometer (MPA580;
Courage and Khazaka Electronic GmbH). The measuring principle
is based on suction and elongation. The device generates 450 mbar
of negative pressure, and the skin is drawn into the aperture of
the probe under constant negative pressure for 2 sec (on-time).
The negative pressure is switched off for 2 sec to allow the skin to
return to its original shape (off-time). Each measuring cycle
consists of three repetitions of on-time/off-time. Skin elasticity
was measured at the left or right cheek using the point marked by
the intersection of a vertical line from the outer corner of the eye
and the horizontal line from the tip of the nose and the R2 value
(gross elasticity; Ua/Uf) was analyzed.
Statistical Analysis
All statistical analyses were performed using the SPSS Package
Program (IBM, USA). Normality of the distribution of data was
assessed using kurtosis and skewness, and prior homogeneity was
analyzed using an independent
t
-test. The statistical significance
of the differences between two groups was determined using
repeated measures ANOVA. A
p
-value of <0.05 was considered
statistically significant.
Results
Baseline Characteristics
A total of 110 (49 placebo group, average age 48.57 ± 4.52
years; 61 probiotic group, average age 49.82 ± 4.96 years) of
129 female volunteers who were included in the study
completed it. Of the 19 volunteers who were excluded from
the final analysis, 12 were eliminated before the beginning
of the study (9 due to laboratory abnormalities and 3 due to
personal circumstance) and 7 dropped out after 4 weeks (3
due to personal circumstance, 2 lost to follow-up, and 2 for
violation of protocol). Comprehensive questionnaire surveys
of the baseline skin characteristics were completed for all
volunteers (Table 2). We next evaluated the prior homogeneity
between probiotic and placebo groups through statistical
analysis of skin parameters (hydration, transepidermal
water loss, wrinkle quality, skin gloss, and skin elasticity)
at baseline, using an independent
t
-test. As a result, there
was no statistically significant difference between the
groups, exerting homogeneity of the placebo and probiotic
groups (Table 3).
Skin Hydration
To evaluate the effect of HY7714 on skin hydration, we
first measured the water content of the face, forearm, and
hand of subjects using a proprietary device called the
Corneometer CM825. As shown in Fig. 1A, the water content
in both groups was significantly increased (
p
<0.001) from
baseline at weeks 4, 8, and 12, and the rates of retention of
water content in the face and hand were significantly
higher in the probiotic group than in the placebo group
(
p
< 0.01, face; and <0.05, hand) at week 12 (Figs. 1B, 1C,
and 1D). We used a proprietary device called the Vapometer
SWL4001 to measure transepidermal water loss at the same
locations. Water loss was significantly decreased from
baseline in both groups at weeks 4, 8, and 12 (
p
<0.001)
(Fig. 2A). The magnitudes of the decrease in transepidermal
water loss from the face and forearm were significantly
larger in the probiotic group compared with the controls at
weeks 4 and 12 (face) and weeks 8 and 12 (forearm)
(Figs. 2B, 2C, and 2D).
Skin Wrinkles
We examined the effect of HY7714 on facial skin wrinkles
Tab le 1.
Definition of skin wrinkle parameters.
Parameter Definition
Ra Arithmetic average value of profile peaks within the total measuring length
Rmax Maximum of all peak-to-valley values Rt, measured over the assessment length
Rp Maximum profile peak height
Rv Maximum profile valley depth
Rz Average maximum height of the profile
Probiotics Ameliorate Skin Aging 2163
December 2015
⎪
Vol. 25
⎪
No. 12
over time using a 3D skin imaging system. The results
showed improvement from baseline in all wrinkle parameters
(Ra, Rmax, Rp, Rv, and Rz) in both groups (Fig. 3). By week
12, decreases in the parameters were 43.48% (Ra), 65.22%
(Rmax), 7.80% (Rp), 106.82% (Rv), and 30.75% (Rz). Decreases
in Ra, Rmax, and Rv were significantly larger (Ra, Rmax,
p
<0.05; Rv,
p
< 0.01) in the probiotic group vs. the placebo
group at week 12. Representative digital and 3D images of
facial skin following week 12 are shown in Fig. 4.
Skin Gloss
We used a proprietary device called the GlossMeter to
evaluate the effect of HY7714 on skin gloss. The result
showed that skin gloss improved in both groups during the
study period, but that the rates of improvement were much
better (16.54%,
p
< 0.05) in the probiotic group by week 12
(Fig. 5).
Skin Elasticity
We used a proprietary device called the Cutometer
MPA580 to measure skin elasticity. As shown in Fig. 6, skin
elasticity increased gradually in both groups during the
study period, but the degree of improvement at week 4
(13.17%,
p
< 0.05) and week 12 (21.73%;
p
< 0.01) was
significantly higher in the probiotic group compared with
the placebo group.
Tab le 2.
Skin characteristics of subjects in the probiotic (
n
= 61) and placebo (
n
= 49) groups.
Probiotic group Placebo group
Item Classification Frequency (
n
)Percentage (%) Frequency (
n
)Percentage (%)
Skin type Dry 39 63.93 27 55.10
Normal 20 32.79 18 36.73
Oily 1 1.64 0 0.00
Dry and oily 1 1.64 4 8.16
Problematic 0 0.00 0 0.00
Hydration Sufficient 0 0.00 0 0.00
Normal 29 47.54 19 38.78
Deficient 32 52.46 30 61.22
Sebum Glossy 1 1.64 4 8.16
Normal 37 60.66 28 57.14
Deficient 23 37.70 17 34.69
Surface Smooth 14 22.95 10 20.41
Normal 45 73.77 32 65.31
Rough 2 3.28 7 14.29
Thickness Thin 18 29.51 14 28.57
Normal 39 63.93 32 65.31
Thick 4 6.56 3 6.12
Time of UV exposure Less than 1 h 25 40.98 13 26.53
1
-
3 h 29 47.54 31 63.27
More than 3 h 7 11.48 5 10.20
Sleeping hours Less than 5 h 8 13.11 2 4.08
5
-
8 h 49 80.33 38 77.55
More than 8 h 4 6.56 9 18.37
Irritability Yes 2 3.28 2 4.08
No 59 96.72 47 95.92
Stinging Yes 0 0.00 0 0.00
No 61 100.00 49 100.00
Adverse reaction Yes 0 0.00 0 0.00
No 61 100.00 49 100.00
2164 Lee et al.
J. Microbiol. Biotechnol.
Fig. 1.
Changes of skin water content after 12 weeks.
(
A
)
The skin water content was measured at three areas (face, forearm, and hand) every 4 weeks from baseline to week 12. (
B
),
(
C
),
and
(
D
)
show
the average rates of
change in water content in the face, forearm, and hand, respectively, in the placebo and probiotic groups. Results are
expressed as the mean ± SEM for all subjects.
***
p
< 0.001 vs. baseline;
††
p
< 0.001,
†
p
< 0.05 probiotic vs. placebo group.
Tab le 3 .
Statistical analysis of skin parameters by independent
t
-test.
Item Site Levene’s test for equality of variances
t
-Test for equality of means
FSig. tdf Sig.
a
Mean difference Std. error difference
Hydration Face 6.231 0.014 -0.863 94.944 0.390 -0.354 0.410
Forearm 0.056 0.814 -0.538 108.000 0.592 -0.388 0.721
Hand 5.365 0.022 -1.816 107.771 0.102 -1.515 0.834
TEWL Face 2.330 0.130 -0.858 108.000 0.393 -0.309 0.360
Forearm 0.831 0.364 0.722 108.000 0.472 0.160 0.221
Hand 2.079 0.152 1.995 108.000 0.109 0.628 0.315
Skin
wrinkle
Ra 3.360 0.070 0.297 108.000 0.767 0.193 0.652
Rmax 0.468 0.495 0.958 108.000 0.340 4.447 4.641
Rp 1.148 0.286 0.299 108.000 0.765 0.520 1.737
Rv 0.018 0.893 1.333 108.000 0.185 4.455 3.341
Rv 1.644 0.203 0.472 108.000 0.638 1.494 3.169
Skin gloss 1.963 0.164 0.001 108.000 0.999 0.001 0.617
Skin elasticity 2.222 0.139 -1.589 108.000 0.115 -0.112 0.007
a
p
> 0.1: significant homogeneity
between two groups.
Probiotics Ameliorate Skin Aging 2165
December 2015
⎪
Vol. 25
⎪
No. 12
Discussion
Daily intake of HY7714 for 12 weeks significantly increased
the skin moisture content and reduced signs of facial aging
by limiting wrinkles and improving elasticity and skin
gloss in women with dry skin and wrinkles. Quantitative
and qualitative data supported the multifunctional activity
of HY7714. Strain HY7714 was selected on the basis of our
earlier studies showing its beneficial effects on skin
hydration [19] and its anti-photoaging [14] activities
in vitro
Fig. 2.
Changes in transepidermal water loss (TEWL) after 12 weeks.
(
A
) TEWL was measured at three points (face, forearm, and hand) every 4 weeks from baseline to week 12 and average rates of change for the
face, forearm, and hand (
B
,
C
, and
D
, respectively) were compared between placebo and probiotic groups. Results are expressed as the mean ±
SEM.
***
p
< 0.001,
**
p
< 0.01,
*
p
< 0.05 compared with baseline;
†††
p
< 0.001,
††
p
< 0.01,
†
p
< 0.05 probiotic vs. placebo group.
Fig. 3.
Changes in skin wrinkle measurements after 12 weeks.
Facial skin wrinkles were measured every 4 weeks from baseline to week 12. Results are expressed as the mean ± SEM for all subjects.
***
p
< 0.001,
**
p
< 0.01 vs. baseline;
††
p
< 0.01,
†
p
< 0.05 probiotic vs. placebo group.
2166 Lee et al.
J. Microbiol. Biotechnol.
and
in vivo
.
Dry skin is caused by an imbalance between the amount
of moisture in the stratum corneum and the intercellular
lipids, which is a prominent clinical manifestation of the
skin-aging process [1]. Because the skin is the outermost
part of the body, it is susceptible to effects of environmental
factors, including humidity, ultraviolet rays, and temperature.
Internal factors such as hormones can also affect skin
balance [1, 13]. Since dry skin plays an important role in the
formation of fine wrinkles, many people make an effort to
moisturize their skin using cosmetics or dietary supplements.
Fig. 4.
Images of skin wrinkle changes after 12 weeks.
These images are representative of the overall results in each group. Upper row, digital photographs; Lower row, three-dimensional imaging. The
subjects shown are probiotic group Volunteer No. 33 and placebo group Volunteer No. 44.
Fig. 5.
Changes in skin gloss after 12 weeks.
Facial skin gloss was measured 4 weeks from baseline to week 12.
Results are expressed as the mean ± SEM for all subjects.
***
p
< 0.001
vs. baseline;
†
p
< 0.05 probiotic vs. placebo group.
Fig. 6.
Changes of skin elasticity after 12 weeks.
Skin elasticity was measured on the face every 4 weeks from baseline
to week 12. The results are expressed as the mean ± SEM for all
subjects.
***
p
< 0.001 vs. baseline;
††
p
< 0.01,
†
p
< 0.05 probiotic vs.
placebo group.
Probiotics Ameliorate Skin Aging 2167
December 2015
⎪
Vol. 25
⎪
No. 12
In the present study, we measured both water content and
transepidermal water loss at three separate areas (face,
forearm, and hand) in order to confirm the probiotic
efficacy, and statistically significant improvements were
shown in least at two areas (face and hand, water content;
face and forearm, water loss). In particular, in the face,
water content was significantly increased while the rate of
water loss was significantly reduced.
Other changes associated with aging include loss of
elasticity, change in skin texture (from smooth to rough),
and wrinkles. Wrinkle formation is associated with
damage to the structural proteins (collagen and elastin) of
the connective tissue of the dermis. Because collagen acts
along with elastin to enhance the tensile strength of skin,
loss of collagen by attrition or destruction leads to wrinkle
formation. There has been much evidence showing that the
major alterations in aging skin occur in the dermal
extracellular matrix. In young skin (usually under 30 years
of age), intact collagen fibrils are abundant, densely packed,
and well organized, whereas in very old skin (usually over
80 years), collagen fibers are fragmented and disorganized
[7, 8, 18]. Loss of collagen impairs the structural integrity of
the skin. Young skin has a reticulated healthy structure,
whereas the area of this dense structure is loosened in
aging skin [10, 21]. The collagen fibers of the deep dermis
become rearranged in parallel with advancing years, which
results in deep furrows, skin roughness, and loss of
elasticity and skin gloss [15, 21]. In the present study,
volunteers in the probiotic group responded positively and
noticed subjective reductions in wrinkles during the study
period, and the measured parameters of wrinkle formation
also showed statistically significant differences between
the probiotic group and the placebo group at week 12.
Gloss and elasticity were also significantly improved in the
probiotic group compared with the placebo group. Taken
together, these results suggest that HY7714 reduces skin
aging through a variety of pathways.
As we have previously reported, oral ingestion of
HY7714 in hairless mice was associated with regulation of
the expression of genes related to skin hydration [19].
HY7714 also suppressed UVB-induced signal transduction
in fibroblasts [14], which suggests that oral HY7714 may
contribute to the molecular control of signaling pathways
and gene expression in the skin cells after being absorbed
by the intestine. The precise mechanisms of amelioration of
skin aging by probiotics should be a topic of continued
research in the future.
In conclusion, healthy skin is regarded as an indicator of
overall health, and the skin condition is influenced by diet
and oral medications [4, 5]. Thus, it is appropriate to
consider the potential anti-aging effects of natural dietary
supplements [26]. The present study has provided clinical
evidence that oral consumption of HY7714 increases skin
hydration, alleviates facial wrinkling, and improves
elasticity and skin gloss. These results suggest that HY7714
would be a useful anti-aging nutricosmetic agent.
References
1. Baek JH, Lee MY, Koh JS. 2011. Relationship between
clinical features of facial dry skin and biophysical
parameters in Asians.
Int. J. Cosmet. Sci.
33:
222-227.
2. Bouilly-Gauthier D, Jeannes C, Maubert Y, Duteil L, Queille-
Roussel C, Piccardi N
, et al.
2010. Clinical evidence of
benefits of a dietary supplement containing probiotic and
carotenoids on ultraviolet-induced skin damage.
Br. J.
Dermatol.
163:
536-543.
3. Chiu YH, Lin SL, Tsai JJ, Lin MY. 2014. Probiotic actions on
diseases: implications for therapeutic treatments.
Food Funct.
5:
625-634.
4. Cho S. 2014. The role of functional foods in cutaneous anti-
aging.
J. Lifestyle Med.
4:
8-16.
5. Draelos ZD. 2010. Nutrition and enhancing youthful-
appearing skin.
Clin. Dermatol.
28:
400-408.
6. Elazab N, Mendy A, Gasana J, Vieira ER, Quizon A, Forno
E. 2013. Probiotic administration in early life, atopy, and
asthma: a meta-analysis of clinical trials.
Pediatrics
132:
e666-
e676.
7. Fisher GJ, Varani J, Voorhees JJ. 2008. Looking older:
fibroblast collapse and therapeutic implications.
Arch. Dermatol.
144:
666-672.
8. Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees
JJ. 1997. Pathophysiology of premature skin aging induced
by ultraviolet light.
N Engl. J. Med.
337:
1419-1428.
9. Foolad N, Brezinski EA, Chase EP, Armstrong AW. 2013.
Effect of nutrient supplementation on atopic dermatitis in
children: a systematic review of probiotics, prebiotics,
formula, and fatty acids.
JAMA Dermatol.
149:
350-355.
10. Gao Q, Yu J, Wang F, Ge T, Hu L, Liu Y. 2013. Automatic
measurement of skin textures of the dorsal hand in
evaluating skin aging.
Skin Res. Technol.
19:
145-151.
11. Gueniche A, Philippe D, Bastien P, Blum S, Buyukpamukcu
E, Castiel-Higounenc I. 2009. Probiotics for photoprotection.
Dermatoendocrinology
1:
275-279.
12. Han Y, Kim B, Ban J, Lee J, Kim BJ, Choi BS
, et al.
2012. A
randomized trial of
Lactobacillus
plantarum
CJLP133 for the
treatment of atopic dermatitis.
Pediatr. Allergy Immunol.
23:
667-673.
13. Kawada C, Yoshida T, Yoshida H, Sakamoto W, Odanaka
W, Sato T
, et al.
2015. Ingestion of hyaluronans (molecular
weights 800 k and 300 k) improves dry skin conditions: a
2168 Lee et al.
J. Microbiol. Biotechnol.
randomized, double blind, controlled study.
J. Clin. Biochem.
Nutr.
56:
66-73.
14. Kim HM, Lee DE, Park SD, Kim YT, Kim YJ, Jeong JW
, et al.
2014. Oral administration of
Lactobacillus
plantarum
HY7714
protects hairless mouse against ultraviolet B-induced
photoaging.
J. Microbiol. Biotechnol.
24:
1583-1591.
15. Lagarde JM, Rouvrais C, Black D. 2005. Topography and
anisotropy of the skin surface with ageing.
Skin Res. Technol.
11:
110-119.
16. Marietta E, Rishi A, Taneja V. 2015. Immunogenetic control
of the intestinal microbiota.
Immunology
145:
313-322.
17. Peguet-Navarro J, Dezutter-Dambuyant C, Buetler T, Leclaire
J, Smola H, Blum S
, et al.
2008. Supplementation with oral
probiotic bacteria protects human cutaneous immune
homeostasis after UV exposure
-
double blind, randomized,
placebo controlled clinical trial.
Eur. J. Dermatol.
18:
504-511.
18. Quan T, Fisher GJ. 2015. Role of age-associated alterations
of the dermal extracellular matrix microenvironment in
human skin aging: a mini-review.
Gerontology
61:
427-434.
19. Ra J, Lee DE, Kim SH, Jeong JW, Ku HK, Kim TY
, et al.
2014. Effect of oral administration of
Lactobacillus
plantarum
HY7714 on epidermal hydration in ultraviolet B-irradiated
hairless mice.
J. Microbiol. Biotechnol.
24:
1736-1743.
20. Raone B, Raboni R, Patrizi A. 2014. Probiotics reduce gut
microbial translocation and improve adult atopic dermatitis.
J. Clin. Gastroenterol.
48:
95-96.
21. Ryu JH, Seo YK, Boo YC, Chang MY, Kwak TJ, Koh JS.
2014. A quantitative evaluation method of skin texture
affected by skin ageing using replica images of the cheek.
Int. J. Cosmet. Sci.
36:
247-252.
22. Satoh T, Murata M, Iwabuchi N, Odamaki T, Wakabayashi
H, Yamauchi K
, et al.
2015. Effect of
Bifidobacterium
breve
B-3
on skin photoaging induced by chronic UV irradiation in
mice.
Benef. Microbes
6:
497-504.
23. Sugimoto S, Ishii Y, Izawa N, Masuoka N, Kano M, Sone T
,
et al.
2012. Photoprotective effects of
Bifidobacterium
breve
supplementation against skin damage induced by ultraviolet
irradiation in hairless mice.
Photodermatol. Photoimmunol.
Photomed.
28:
312-319.
24. Udompataikul M, Sripiroj P, Palungwachira P. 2009. An oral
nutraceutical containing antioxidants, minerals and
glycosaminoglycans improves skin roughness and fine
wrinkles.
Int. J. Cosmet. Sci.
31:
427-435.
25. Vierkotter A, Krutmann J. 2012. Environmental influences on
skin aging and ethnic-specific manifestations.
Dermatoendocrinology
4:
227-231.
26. Vranesic-Bender D. 2010. The role of nutraceuticals in anti-
aging medicine.
Acta Clin. Croat.
49:
537-544.
27. Wlaschek M, Tantcheva-Poor I, Naderi L, Ma W, Schneider
LA, Razi-Wolf Z
, et al.
2001. Solar UV irradiation and
dermal photoaging.
J. Photochem. Photobiol. B
63:
41-51.