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Original Paper
Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/0 00361053
Antioxidants in Asian-Korean and
Caucasian Skin: The Influence of
Nutrition and Stress
SoraJung a MaximE.Darvin a Hyoung-SeokChung d BenaJung c
Sang-HyukLee f KlausLenz b Wan-SeokChung e Ruo-XiYu a
AlexaPatzelt a Bich-NaLee a WolframSterry a JuergenLademann a
a Center of Experimental and Applied Cutaneous Physiology, Department of Dermatology, Venerology and
Allergology and
b Institute of Medical Biometrics and Clinical Epidemiology, Charité – Universitätsmedizin Berlin,
Berlin , and c Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-
Eppendorf, Hamburg , Germany; d Department of Orthopaedic Surgery, Medical Center, Chung-Ang University, and
e Division of Information Communication Engineering, Dongguk University, Seoul , and
f Department of Industrial
Engineering, Ulsan University, Ulsan, South Korea
Results: In the present study South Korean residents showed
a significantly higher antioxidant status than both native
German residents and Korean immigrants living in Germany
(p < 0.001). The first generation of Korean immigrants to
Germany over the age of 50 mostly preserved Korean dietary
habits, showing significantly higher concentrations (p <
0.001) than the German-born second and third Korean gen-
erations under the age of 50. Conclusion: The results of the
study indicate that a healthy nutrition alone does not pro-
vide a high antioxidant status unless the stress exposure can
be reduced simultaneously. © 2014 S. Karger AG, Basel
Introduction
Free radicals are continuously formed in the human
skin as a result of metabolic processes. Their substantial
increase occurs subsequent to contact with environmental
pollutants, solar radiation and the influence of stress fac-
tors
[1–3] . At low physiological concentrations, these high-
Key Words
Carotenoids · Antioxidants · Free radicals ·
Korean nutrition · Stress · Sociocultural influences ·
South Korea · Reflectance spectroscopy
Abstract
Background: The antioxidant status of the human skin pro-
vides protection against the destructive action of free radi-
cals. Most antioxidants cannot be synthesized by the human
organism itself, but have to be ingested with a healthy nutri-
tion rich in fruit and vegetables. The Korean cuisine is known
to be one of the healthiest worldwide. This binational study
investigated the cutaneous carotenoid concentrations in
German subjects, South Korean subjects and immigrant
Korean subjects resident in Germany and examined whether
dietary- and lifestyle-related differences are reflected in the
cutaneous carotenoid concentrations. Methods: Measure-
ments of the carotenoid concentrations of 714 healthy vol-
unteers were performed using a non-invasive spectroscopic
measurement system based on reflectance spectroscopy.
Received: December 17, 2013
Accepted after revision: March 3, 2014
Published online: June 26, 2014
Sora Jung
Charité – Universitätsmedizin Berlin
Department of Dermatology, Center of Experimental and Applied Cutaneous Physiology
Charitéplatz 1, DE–10117 Berlin (Germany)
E-Mail sora.jung @ charite.de
© 2014 S. Karger AG, Basel
1660–5527/14/0276–0293$39.50/0
www.karger.com/spp
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Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/000361053
294
ly reactive molecules are beneficial for fighting viruses and
bacteria and have a signalling function
[4] , whereas at high
concentrations they are able to damage or even destroy
cells and cell compartments
[1, 2] . Premature skin aging [3,
5, 6] , immunosuppression [7] and even skin cancer can be
the consequences
[8] . The human skin has developed a
protection system against the detrimental effects of reac-
tive oxygen species based on the action of different anti-
oxidants
[9] , the most efficient of them being carotenoids,
vitamins and enzymes. The intake of antioxidants such as
vitamin C and β-carotene was shown to enhance the recov-
ery from oxidative damage in human lymphocytes
[10]
and to be positively associated with physical performance
[11] , and even reduced mortality [12] , in subjects aged over
65 years. Furthermore, various epidemiological studies
demonstrated the association of carotenoid-rich food in-
take with a reduced risk of chronic diseases
[13] .
Most antioxidants cannot be produced by the human
organism itself. They have to be ingested with healthy
food containing high amounts of fruit and vegetables
[14] . It was demonstrated that systemically applied anti-
oxidants are efficiently accumulated in the human plasma
[15] and the skin [16] and that individuals with high an-
tioxidant concentrations in their skin showed less pro-
nounced skin aging than subjects of the same age with low
concentrations of dermal antioxidants
[17] . Consequent-
ly, a healthy diet could serve as a protection strategy
against skin aging. The aging process in Asian skin is de-
layed in time and shows differences compared to European
skin
[18–20] . Furthermore, living conditions and food
habits differ notably. Investigations of the antioxidant sta-
tus of German residents of African, Caucasian and Asian
origin showed no significant differences in the past
[21] ,
but neither nutritional habits nor the antioxidant status
ofAsian residents have been investigated by comparison.
The aim of our study was to investigate whether differ-
ences in the nutritional and cultural habits as well as stress
behaviour between Korean and German volunteers are re-
flected in the antioxidant status of the skin. In addition, the
dietary habits and antioxidant status of immigrant Korean
volunteers living in Germany were investigated by com-
parison. Many studies, especially from the USA, show that
immigrant populations can provide important informa-
tion about the effects of nutritional behaviour and envi-
ronmental and lifestyle factors on individual health. Sev-
eral previous studies showed that acculturation to a more
Western diet and lifestyle is associated with a higher fat
intake and obesity, which leads to a higher prevalence of
diabetes, coronary heart disease, cancer and diabetes in im-
migrated Asian populations in Western countries
[22–24] .
Difference between the Traditional Korean and
German Diet
Due to historical reasons that are associated with the
preparation of traditional dishes the Korean cuisine is
particularly healthy, as it is largely based on fruit and veg-
etables such as kimchi
[25, 26] , red chili peppers [27] and
seaweeds
[28, 29] , which have been proven to have strong
antioxidative effects. For several decades, the Korean gov-
ernment and private Korean entrepreneurs and institu-
tions have been taking action to preserve and popularize
traditional Korean cooking
[30, 31] . Resulting from that,
traditional dishes and side dishes containing uncooked
vegetables are popular nationwide in South Korea
[31, 32]
and more standardized than in Europe or the USA, so that
the variety and differences in food preparation are con-
siderably reduced. Therefore, the Korean population rep-
resents an interesting survey group regarding not only
healthy, but also relatively standardized nutrition.
Traditional Korean food preparation contains high
amounts of crude, fermented and pickled vegetables and
a reduced amount of total fat compared to Western
[33]
and even other Asian countries such as China or Japan
[30, 31] . The absence of thermal treatment leads to large-
scale preservation of the antioxidants and the ratio of veg-
etable intake to meat and fish intake is on average above
2
[30, 33] . In addition to that, fresh fruits are tradition-
ally often served as desert.
The German cuisine provides a larger variety in dishes.
It includes bakery products and milk products as well as
dishes based on potatoes, noodles or rice
[34] . Compared
to the Korean cuisine many ingredients, especially vege-
tables, are cooked or fried. Therefore, the amount of an-
tioxidants can in general be seen as lower.
Thus, it is our hypothesis that Korean individuals
show notably higher antioxidant concentrations in their
skin than Germans.
Materials and Methods
Vol unte e rs
A total of 714 healthy volunteers aged from 7 to 75 years, includ-
ing 279 Koreans (resident in Korea), 332 Germans and 103 immi-
grant Korean volunteers in Germany, were recruited and measured
on a voluntary basis during the summer months, i.e. from June to
August, in South Korea and Germany. We included only Korean im-
migrants with a Korean background of both parents in our study, who
were either born in Germany or immigrated to Germany and had
been continuously living in Germany for at least 1 year. Volunteers
were recruited in public institutions, restaurants, private educational
institutions, expositions, sports clubs, cultural associations, church
services, dormitories and hospitals in South Korea and Germany.
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A Comparative Study between South
Korea and Germany
Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/000361053
295
Measurement System
Carotenoids were measured as marker substances for the anti-
oxidant status of the human skin
[35, 36] . It has been shown that
antioxidative substances form protective chains in the skin, pro-
tecting each other from the destructive effects of free oxygen spe-
cies
[36] . The concentration of cutaneous carotenoids correlates to
the concentration of serum carotenoids, thus serving as a biomark-
er for the antioxidant capacity of the human organism
[37] . Mea-
surements were conducted non-invasively on the thenar eminence
located on the hand palm of each volunteer using a miniaturized
spectroscopic system. The hand palm was chosen due to its acces-
sibility, the absence of strong pigmentation variations, which can
influence measurements, and the proven reliability and reproduc-
ibility of measurement results in previous studies
[21] . The used
measurement system is based on reflectance spectroscopy
[35]
(Opsolution GmbH, Kassel, Germany) containing an optical win-
dow on the undersurface. The radiation of LED emits in the maxi-
mum of the absorption spectrum of the carotenoids at 465 ± 25
nm,whereas another LED emits beyond this absorption spectrum
to determine the background signals. The radiation penetrates the
skin to a depth of 150–200 μm. Concentrations were presented in
a line 1–12 scale, with the concentration 12 corresponding to
1.2nmol·g
–1 [35] . Each measurement session was accompanied by
measurements of the cutaneous carotenoid concentration of the
main investigator, who was measured at the start of each measure-
ment session as a control measurement to ensure the functionality
of the measurement system and the accuracy of measurements.
Data Acquisition
A compilation of the assessed data is given in table1 . Personal
data were collected using a questionnaire completed by included
volunteers containing information about gender, age, BMI, sub-
jective stress level, vegetable and fruit consumption, smoking and
Korean or Western dietary habits. The subjective stress level was
assessed using a grading of stress intensity ranging from 0 (= no
stress) to 4 (= very much stress) including both occupational and
personal stress. All volunteers were asked about their current
stress level based on their individual subjective perception. Infor-
mation on vegetable and fruit consumption was collected regard-
ing the frequency of both raw and processed vegetable and fruit
consumption.
Korean dietary habits were defined as nutritional habits based
on main dishes involving rice in combination with traditional
Korean beverages, such as, among others, kimchi
[25, 26] , namul
(traditionally seasoned vegetable dishes), soybean products, fish,
meat and seaweed. Western dishes were defined as dishes lacking
traditional Korean beverages or ingredients, such as dishes based
on bread, potatoes or dairy products.
S t a t i s t i c s
Statistical analysis was conducted using IBM SPSS
® Statistics
version19.0.0, using Student’s t test, analysis of variance
( ANOVA), analysis of covariance (ANCOVA), post hoc Scheffé’s
test and post hoc Tamhane’s T2 test when appropriate. Microsoft
Office Excel 2007 was used for data acquisition and the generation
of diagrams. In order to avoid confounding by heterogeneous dis-
tributions of gender and age characteristics among the three pop-
ulation groups, mean concentrations, standard errors (SE) and
significances were determined, adjusting to gender and age by
using ANCOVA.
R e s u l t s
Comparison of the Antioxidant Status of the Three
Ethnic Groups
The age- and gender-adjusted mean concentration
and the SE of the carotenoid concentration in Korean
volunteers living in South Korea was measured at 5.81±
0.11, being significantly higher (p< 0.001) than the mean
carotenoid concentration in German volunteers which
had been measured at 4.62 ± 0.1. With a mean concen-
tration of 4.77 ± 0.18 the carotenoid concentration of the
immigrated Korean volunteers living in Germany ranged
between the German and the South Korean mean con-
centrations, as presented in figure 1 . This concentration
was significantly lower than the mean of the Korean res-
idents (p< 0.001) but not significantly higher than the
German mean.
Our hypothesis was additionally confirmed by the
findings within the immigrant Korean community in
Germany, which we divided into two age groups. The first
generation of Korean immigrants to Germany had come
during the 1960–1980s as foreign guest workers
[38] .
These first immigrants over the age of 50 showed a sig-
nificantly higher carotenoid mean concentration of
5.43± 0.21 (p< 0.001) than the younger generations un-
der the age of 50 at 4.39 ± 0.23, who were mostly born in
Germany ( fig.2 ).
Influence of Diet on the Antioxidant Status of the
Volu nt ee rs
In South Korea, Western dishes as well as Korean dish-
es are likewise available in supermarkets and restaurants.
These Western dishes are influenced by the American
and European culture including among others, bakery
products, cheese, jam, pizza, spaghetti and hamburgers,
which are becoming more and more popular, particular-
ly among the younger Koreans. Our survey showed that
69% of the Korean volunteers in South Korea consume
mainly traditional Korean dishes, 27% a mixture of both
Western and Korean cuisine and 3% mainly Western
dishes, while 100% stated to consume vegetables daily
( table1 ). Therefore, it can be assumed that the higher an-
tioxidant status in this group is due to a higher intake of
crude vegetables.
Regarding the Korean community in Germany,
where the access to Western dishes is easier, while tra-
ditional Korean ingredients are available in Asian su-
permarkets, the number of those who cook mainly
Korean dishes was considerably reduced to 25% ( ta-
ble1 ).
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Another striking fact is that among the volunteers in
South Korea the traditional Korean dietary habits are as-
sociated with higher antioxidant concentrations, while
the mixed and Western dietary habits lead to a decline in
measured antioxidants. The average age of the volunteers
stating to consume a mainly Korean diet was 38 years, the
average of those eating mainly a mixture of both Western
and Korean dishes was 23 years and an average age of
15 years was found in volunteers consuming a mainly
Western diet.
Korean-German immigrants showed a decreased an-
tioxidant concentration in the volunteers consuming a
mixture of Korean and Western food compared to those
consuming only traditional Korean food.
Table 1. Total numbers, percentages and adjusted p values of the parameters of the questionnaire for German volunteers, Korean vol-
unteers in South Korea and immigrant Korean volunteers in Germany
p value Population group
G erman volunteers Korean volunteers
in South Korea
Korean immigrants
in Germany
number percent number percent number percent
Gender
Male 236 71.1 103 36.9 41 39.8
Female 96 28.9 176 63.1 62 60.2
Age group, years 0.0071
7–13 10 3.0 71 25.4 4 3.9
14–17 90 27.1 25 9.0 4 3.9
18–30 101 30.4 47 16.8 20 19.4
31–49 74 22.3 57 20.4 19 18.4
50–59 42 12.7 37 13.3 17 16.5
60–83 15 4.5 42 15.1 39 37.9
Diet type <0.0012
Traditional Korean diet only 0 0 187 69.3 25 25.3
Both traditional Korean and Western diet 0 0 74 27.4 69 69.7
Western diet only 332 100.0 9 3.3 5 5.1
Vegetable and fruit consumption 0.0092
Once a week or less frequently 98 30.1 0 0 1 1.0
Several times a week 125 38.3 0 0 2 1.9
Daily 103 31.6 279 100.0 100 97.1
BMI group
Underweight 8 2.5 15 6.3 2 2.1
Normal weight 214 65.8 184 77.6 72 76.6
Overweight 91 28.0 31 13.1 18 19.1
Obese 12 3.7 7 3.0 2 2.1
Stress
No stress 73 22.0 54 19.4 23 22.3
Little stress 102 30.7 91 32.6 28 27.2
Moderate stress 38 11.4 59 21.1 40 38.8
Much stress 112 33.7 50 17.9 7 6.8
Very much stress 7 2.1 25 9.0 5 4.9
Smoking
Nonsmoker 292 88.0 258 92.5 92 89.3
Smoker<10 cigarettes per day 40 12.0 10 3.6 10 9.7
Smoker >10 cigarettes per day 0 0 11 3.9 1 1.0
The mean difference is significant at the p< 0.05 level. p values from χ2 test, t test, ANOVA and ANCOVA. BMI groups were formed
using the age-adjusted classification by Kromeyer-Hauschild et al. [54].
1p values adjusted to gender and population group.
2p values adjusted to gender, age and population group.
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DOI: 10.1159/000361053
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Influence of Age-Related Stress on the Antioxidant
Status
Above all, as in previous studies, we found stress con-
ditions to influence the individual antioxidant status no-
tably
[17, 39] . The individual variety of stress exposition
and stress management can explain the broad variance
found in all three ethnic groups despite the relatively uni-
form dietary habits regarding high vegetable intake in
South Korea. Higher antioxidants in Korean natives had
been anticipated, but the antioxidant concentrations in
Korean volunteers were found at notably lower levels
than expected regarding the healthy traditional Korean
0
2
4
6
8
10
12
German
volunteers
Korean
volunteers in
South Korea
Korean
immigrants in
Germany
Carotenoid concentration (AU)
p < 0.001 p < 0.001
0
2
4
6
8
10
<50 >50
Carotenoid concentration (AU)
p < 0.001
Age (years)
Fig. 1. Boxplot of carotenoid concentrations measured in German,
Korean and immigrant Korean volunteers in Germany. Whiskers
represent the minimum and maximum concentrations within the
1.5-fold interquartile range. Dots represent outliers beyond the
1.5-fold interquartile range. The differences in carotenoid
concentration between the resident Korean volunteers and both
the German and Korean-German volunteers are significant at the
p< 0.001 level.
Fig. 2. Boxplot of the carotenoid concentrations of Korean volunteers
living in Germany divided into volunteers<50 years of age for the
younger generation and >50 years of age for the elderly native Korean
generation of immigrated Koreans. Whiskers demonstrate the mini-
mum and maximum concentrations within the 1.5-fold interquartile
range. Dots represent outliers beyond the 1.5-fold interquartile range.
The difference in carotenoid concentration between the first genera-
tion of Korean immigrants >50 years of age and the younger Korean-
German generations<50 are significant at the p< 0.001 level.
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food ingredients, which are high in antioxidants. Age-re-
lated stress could be a reason for this. Therefore, conduct-
ing a gender-adjusted multi-factor ANCOVA, the effects
of population group, age group and stress on antioxidant
concentrations were determined. Previous studies showed
that the antioxidant status is independent of age
[39] .
However, evaluating the questionnaires of all volunteers
in our study, we found a significant effect of age group on
the carotenoid concentration at the p< 0.05 level for the
three conditions (F= 7.376, p= 0.007 ).
Several factors that differ with age could be confound-
ing factors for the effect of age groups.
The variables gender, diet type and fruit and vegeta-
ble consumption were investigated as possible con-
founders of the effect of age groups, but showed no sig-
nificant evidence of confounding. Furthermore, stress as
a result of occupational and social conditions could be a
possible influencing factor that differs with age. Here-
upon conducting a gender-adjusted ANCOVA of the ef-
fect of population group and age on stress as dependent
variable we found a significant dependency of stress on
age (F= 14.1, p< 0.001 ). In addition to that, the mean
stress level of different age groups shows axially approx-
imate symmetrical concentrations to the mean carot-
enoid concentrations in both Asian groups ( fig. 3 , 4 ).
These findings can be seen as the influence of age-relat-
ed stress on the individual antioxidant status of the vol-
unteers.
Gender Differences in the Antioxidant Status in the
Various Ethnic Groups
Korean men living both in Germany and in South
Korea showed a lower concentration of antioxidants than
Korean women. In the German group, men showed high-
er levels of antioxidants than German women.
Influence of the BMI on the Antioxidant Status
In both Korean groups the antioxidant concentration
showed a tendency to decrease with overweight and obe-
sity, as shown in previous studies
[39] .
Influence of Smoking on the Antioxidant Status of the
Volu nt ee rs
In our study, the number of smokers was notably low-
er than official percentages for Korean
[40] and German
[41] smokers of 25–26%, and smoking showed no corre-
lation with a low carotenoid concentration.
The assessed data of the questionnaire for the three
population groups are summarized in table1 .
D i s c u s s i o n
Health Aspect of Traditional Korean Cuisine
The elevated antioxidant concentration of Korean vol-
unteers in South Korea and of volunteers who consume
mainly traditional Korean food in comparison to the
0
1
2
3
4
5
6
7
7–13 14–17 18–30
Age (years)
31–49 50–59 60–83
Subjective stress scale
4
3
2
1
0
Concentration of carotenoids (AU)
Subjective stress
Carotenoid concentration
Fig. 3. Antioxidant concentration and
mean stress level (0= no stress, 1= little
stress, 2= medium stress, 3= much stress,
4 = very much stress) in different age
groups of native Korean volunteers in
Korea. The linear graphs of the carotenoid
concentration and subjective stress level
show an axially approximate symmetrical
alignment.
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A Comparative Study between South
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Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/000361053
299
German volunteers and volunteers with a more Western-
ized dietary behaviour confirms our expected hypothesis
about the health aspects of a Korean diet that is rich in
antioxidants.
Of particular interest is the fact that the members of the
Korean community living in Germany who were aged
over 50 showed values almost as high as volunteers
in Korea. While the Korean-born generations who immi-
grated from the 1960s to the 1980s to Germany
[42]
showed a tendency towards the carotenoid concentration
of the Korean volunteers in South Korea, the younger
German-born generations of Korean origin under the age
of 50 showed a low mean concentration even below the
Germanmean value of 4.5 in the same age group. This re-
sult is not surprising considering the answers to the ques-
tionnaires. These indicate that the nutritional behaviour
of the elderly Korean volunteers in Germany is similar to
the volunteers living in Korea, although most of them have
been living for several years or decades in Germany,
whereas the younger generations are more adapted to the
European eating habits and lifestyle, which is reflected in
a lower carotenoid concentration in the skin.
We observed that, in general, the German-Korean
generations over 50 years of age showed more social par-
ticipation and integration within the Korean community
than the younger participants. Most of these older volun-
teers in our study not only preferred Korean food but
spoke the Korean language more frequently than German
and felt more strongly associated with Korean values and
traditions than the younger generations. According to
this, the first generation of immigrants has been keeping
traditional food habits and preferences, while the young-
er generations tend to consume more Western dishes.
This could be seen as a result of stronger acculturation
to the Western lifestyle and Western nutritional habits
among the younger generations. Similar observations
were found in studies about Korean-American immi-
grants
[22, 23, 43] .
Stress in Korean Society
The quantitative determination of individual stress is
complex and difficult. Therefore, not only the subjective
stress data, but also more objective stress factors within
each cultural environment were investigated. The per-
ception of stress already shows differences between
Korean and European societies. In Korean society a
strong emphasis is put on education and academic suc-
cess, since a successful career is linked to high apprecia-
tion and honour for the family
[44] . Thus, being stressed
because of hard work represents activity, deployment,
high motivation and dedication at work and is linked to
high social appreciation. This view of stress differs nota-
bly from the negative and avoidant attitude towards stress
in the European culture.
Social [45] and economic pressure is high in Korean
society. According to the Organization of Economic Co-
0
1
2
3
4
5
6
7
7–13 14–17 18–30
Age (years)
31–49 50–59 60–83
Subjective stress scale
4
3
2
1
0
Concentration of carotenoids (AU)
Subjective stress
Carotenoid concentration
Fig. 4. Antioxidant concentration and
mean stress level (0= no stress, 1= little
stress, 2= medium stress, 3= much stress,
4 = very much stress) in different age
groups of Korean volunteers in Germany.
The linear graphs of the carotenoid con-
centration and subjective stress level show
an axially approximate symmetrical align-
ment.
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operation and Development (OECD) Koreans worked
44.6 h a week on average in 2011, which is the second
highest rate among the OECD member states (Germany:
35.5 h per week on average) with unemployment rates of
3.5% of the South Korean labour force and 6% of the
German labour force
[46] . The suicide rate in South Korea
is the highest among countries of the OECD
[47, 48] and
suicide is one of the leading causes of death in Korea
[48,
49] .
Above all, the Korean tradition and culture are char-
acterized by authoritarianism, hierarchy and collectivism
[50, 51] . Such a working environment differs notably
from the organization of Western countries, which is
rather horizontal in comparison. According to this, we
found that the antioxidant concentration of Korean supe-
riors was often higher than the concentrations measured
in employees of the same company. Therefore, the social
and occupational stress exposure of the volunteers in
Korea can objectively be seen as higher than the exposure
of the volunteers in Germany in our study.
While the peak of subjective stress in immigrant
Korean and German volunteers was found at 31–49 years,
the peak within the Korean volunteers in Korea was
shown to be at 13–17 years of age. One possible explana-
tion for this can be found in the Korean educational sys-
tem, which is known to be very competitive and demand-
ing compared to the educational systems of Western
countries
[44] . These circumstances cause tremendous
social and psychological pressure, lack of sleep and high
competitiveness already for teenagers and young adoles-
cents
[52] . This is reflected by high stress levels and con-
sequently a reduced antioxidant status of the Korean vol-
unteers in the age group from 13 to 17 years, as seen in
figure 3 .
Within the Germans and immigrant Koreans the stress
level of the age group 13 to 17 years was reduced in com-
parison to the Korean volunteers in South Korea, as the
German educational system is less stressful ( fig. 3 , 4 ).
However, the antioxidant status is more strongly charac-
terized by the different nutritional habits of elderly and
younger Koreans in Germany as described above, which
explain the age-related differences in the antioxidant sta-
tus.
Regarding these conditions, the high impact of stress in
combination with a healthy nutrition leads to our results.
Further Observations
While conducting our study we found that in certain
social groups within the Korean population, that were
characterized by the same eating and stress habits, similar
concentrations of carotenoids in the skin were found.
One example is employees of a high-class sushi restaurant
in Seoul, who all showed remarkably high above-average
carotenoid concentrations. Their working environment
was described by them as demanding, but cooperative
and appreciating, and their employment situation as se-
cure. Their daily meals were eaten together and prepared
from the leftovers in the restaurant, consisting of fresh
fish and raw vegetables.
Five German students were measured during an in-
ternship in South Korea. All of them had been living in
Korea for at least 3 weeks and consumed traditional
Korean food daily. Notably, they all showed high levels of
carotenoids compared to the German volunteers in
Germany. Their mean concentration was measured at 5.4.
In general, we assume by our observations that posi-
tive thinking and equanimity can favour a high level of
antioxidants, as similarly described in a previous study by
Boehm et al.
[53] , who found an association between op-
timism and serum antioxidant levels.
Limitations of the Study
It has to be taken into consideration that the sun expo-
sure of Korean residents is lower compared to German
residents due to a different ideal of beauty. In general,
both Korean men and women avoid direct sun exposure.
During the summer months, it is common to see women
wearing visors, long sleeves and avoiding direct sun ex-
posure
[20] . This can influence the formation of sun-in-
duced free radicals in the Korean volunteers additionally
and, as a result, lead to the accumulation of antioxidants
in the skin.
Since all of our measurements were conducted on a
voluntary basis, it has to be taken into account that sub-
jects being conscious about an unfavourable lifestyle
might anticipate a negative feedback and therefore avoid
participating in our study.
C o n c l u s i o n
Our results indicate that healthy nutrition and a low
stress level are equally important for developing a high
antioxidant status in order to reduce premature skin ag-
ing and the negative effects of oxidative stress. While
many political and medical campaigns have popularized
the positive effects of a healthy nutrition, the impact of
stress has not been emphasized as strongly. Therefore,
more educational advertising about the negative influ-
ence of stress and more information about effective stress
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A Comparative Study between South
Korea and Germany
Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/000361053
301
management is needed in educational systems and the
general public. The results of our survey can also be useful
regarding dietetics and preventive health care.
Acknowledgements
We would like to thank Seong-Cheol Ha, Jae-Wang Kim, Ji-Il
Jung, Kook-Ja Jung, Young-Mi Lee, Youn-Gang Ro, Sang-Dae Lee,
Hyang-Suk Lee, Bok-Ja Jung, Dong-Chun Lee and the Korean As-
sociation of Berlin (Koreanischer Verein Berlin e.V.) for their
organizational and logistical support and helpful discussions.
Wethank Opsolution GmbH, Kassel, Germany for technical sup-
port.
Disclosure Statement
There was no funding institution or other funding source in-
volved in this study.
References
1 Valko M, Leibfritz D, Moncol J, Cronin MTD,
Mazur M, Telser J: Free radicals and antioxi-
dants in normal physiological functions and
human disease. Int J Biochem Cell Biol 2007;
39: 44–84.
2 Droge W: Free radicals in the physiological con-
trol of cell function. Physiol Rev 2002;
82: 47–95.
3 Barouki R: Ageing free radicals and cellular
stress. Med Sci (Paris) 2006;
22: 266–272.
4 Hamanaka RB, Glasauer A, Hoover P, YangS,
Blatt H, Mullen AR, Getsios S, Gottardi CJ,
DeBerardinis RJ, Lavker RM, Chandel NS:
Mitochondrial reactive oxygen species pro-
mote epidermal differentiation and hair fol-
licle development. Sci Signal 2013;
6:ra8.
5 Knight JA: The biochemistry of aging. Adv
Clin Chem 2000;
35: 1–62.
6 Schagen SK, Zampeli VA, Makrantonaki E,
Zouboulis CC: Discovering the link between
nutrition and skin aging. Dermatoendocrinol
2012;
4: 298–307.
7 Cui J, Le G, Yang R, Shi Y: Lipoic acid attenu-
ates high fat diet-induced chronic oxidative
stress and immunosuppression in mice jeju-
num: a microarray analysis. Cell Immunol
2009;
260: 44–50.
8 Sander CS, Chang H, Hamm F, Elsner P,
Thiele JJ: Role of oxidative stress and the an-
tioxidant network in cutaneous carcinogene-
sis. Int J Dermatol 2004;
43: 326–335.
9 Bohm F, Edge R, Truscott G: Interactions of
dietary carotenoids with activated (singlet)
oxygen and free radicals: potential effects for
human health. Mol Nutr Food Res 2012;
56:
205–216.
10 Torbergsen AC, Collins AR: Recovery of hu-
man lymphocytes from oxidative DNA dam-
age; the apparent enhancement of DNA re-
pair by carotenoids is probably simply an an-
tioxidant effect. Eur J Nutr 2000;
39: 80–85.
11 Cesari M, Pahor M, Bartali B, Cherubini A,
Penninx BW, Williams GR, Atkinson H,
Martin A, Guralnik JM, Ferrucci L: Antioxidants
and physical performance in elderly persons:
The Invecchiare in Chianti (InCHIANTI)
study. Am J Clin Nutr 2004;
79: 289–294.
12 Agudo A, Cabrera L, Amiano P, Ardanaz E,
Barricarte A, Berenguer T, Chirlaque MD,
Dorronsoro M, Jakszyn P, Larranaga N, Marti-
nez C, Navarro C, Quiros JR, Sanchez MJ, Tor-
mo MJ, Gonzalez CA: Fruit and vegetable in-
takes, dietary antioxidant nutrients, and total
mortality in Spanish adults: findings from the
Spanish cohort of the European Prospective In-
vestigation into Cancer and Nutrition (EPIC-
Spain). Am J Clin Nutr 2007;
85: 1634–1642.
13 Rao AV, Rao LG: Carotenoids and human
health. Pharmacol Res 2007;
55: 207–216.
14 Halvorsen BL, Carlsen MH, Phillips KM,
Bohn SK, Holte K, Jacobs DR Jr, Blomhoff R:
Content of redox-active compounds (i.e.
antioxidants) in foods consumed in the United
States. Am J Clin Nutr 2006;
84: 95–135.
15 Muller H, Bub A, Watzl B, Rechkemmer G:
Plasma concentrations of carotenoids in
healthy volunteers after intervention with ca-
rotenoid-rich foods. Eur J Nutr 1999;
38: 35–44.
16 Meinke MC, Darvin ME, Vollert H, Lade-
mann J: Bioavailability of natural carotenoids
in human skin compared to blood. Eur J
Pharm Biopharm 2010;
76: 269–274.
17 Lademann J, Meinke MC, Sterry W, Darvin
ME: Carotenoids in human skin. Exp Derma-
tol 2011;
20: 377–382.
18 Nouveau-Richard S, Yang Z, Mac-Mary S, Li
L, Bastien P, Tardy I, Bouillon C, Humbert P,
de Lacharrière O: Skin ageing: a comparison
between Chinese and European populations.
J Dermatol Sci 2005;
40: 187–193.
19 Roh K, Kim D, Ha S, Ro Y, Kim J, Lee H: Pig-
mentation in Koreans: study of the differences
from Caucasians in age, gender and seasonal
variations. Br J Dermatol 2001;
144: 94–99.
20 Chung JH: Photoaging in Asians. Photoder-
matol Photoimmunol Photomed 2003;
19:
109–121.
21 Luther N, Darvin ME, Sterry W, Lademann J,
Patzelt A: Ethnic differences in skin physiology,
hair follicle morphology and follicular penetra-
tion. Skin Pharmacol Physiol 2012;
25: 182–191.
22 Yang EJ, Chung HK, Kim WY, Bianchi L,
Song WO: Chronic diseases and dietary
changes in relation to Korean Americans’
length of residence in the United States. J Am
Diet Assoc 2007;
107: 942–950.
23 Park SY, Murphy SP, Sharma S, Kolonel LN:
Dietary intakes and health-related behaviours
of Korean American women born in the USA
and Korea: the Multiethnic Cohort Study.
Public Health Nutr 2005;
8: 904–911.
24 Lutsey PL, Diez Roux AV, Jacobs DR Jr, Burke
GL, Harman J, Shea S, Folsom AR: Associa-
tions of acculturation and socioeconomic sta-
tus with subclinical cardiovascular disease in
the multi-ethnic study of atherosclerosis. Am
J Public Health 2008;
98: 1963–1970.
25 Lee Y, Choi J, Kwon M, Kim J, Suh H, Song Y:
Isolation and identification of active principle
in Chinese cabbage kimchi responsible for an-
tioxidant effect. Korean J Food Sci Technol
2004;
36: 129–133.
26 Choi IH, Noh JS, Han J-S, Kim HJ, Han E-S,
Song YO: Kimchi, a fermented vegetable, im-
proves serum lipid profiles in healthy young
adults: randomized clinical trial. J Med Food
2013;
16: 223–229.
27 Pugliese A, O’Callaghan Y, Tundis R, Galvin
K, Menichini F, O’Brien N, Loizzo MR: In vi-
tro investigation of the bioaccessibility of ca-
rotenoids from raw, frozen and boiled red
chili peppers ( Capsicum annuum ). Eur J Nutr
2014;
53: 501–510.
28 Lordan S, Ross RP, Stanton C: Marine bioac-
tives as functional food ingredients: potential
to reduce the incidence of chronic diseases.
Mar Drugs 2011;
9: 1056–1100.
29 Park EJ, Pezzuto JM: Antioxidant marine
products in cancer chemoprevention. Anti-
oxid Redox Signal 2013;
19: 115–138.
30 Kim S, Moon S, Popkin BM: The nutrition
transition in South Korea. Am J Clin Nutr
2000;
71: 44–53.
31 Lee MJ, Popkin BM, Kim S: The unique
aspects of the nutrition transition in South
Korea: the retention of healthful elements in
their traditional diet. Public Health Nutr
2002;
5: 197–203.
32 Kwak CS, Lee MS, Oh SI, Park SC: Discovery
of novel sources of vitamin B
12 in traditional
Korean foods from nutritional surveys of cen-
tenarians. Curr Gerontol Geriatr Res 2010;
2010: 374897.
33 Lee MS, Woo MK, Kwak CS, Oh SI, Park SC:
Analysis of traditional Korean food patterns
according to the healthy longevity diet based
on the database of favorite Korean foods. Ann
NY Acad Sci 2001;
928: 348.
Downloaded by:
Charité - Universitätsmedizin Berlin
193.175.73.207 - 6/26/2014 10:09:08 AM
Jung/Darvin/Chung/Jung/Lee/Lenz/
Chung/Yu/Patzelt/Lee/Sterry/Lademann
Skin Pharmacol Physiol 2014;27:293–302
DOI: 10.1159/000361053
302
34 Slimani N, Fahey M, Welch A, Wirfält E,
Stripp C, Bergström E, Linseisen J, Schulze
MB, Bamia C, Chloptsios Y, Veglia F, Panico
S, Bueno-de-Mesquita HB, Ocké MC, Brustad
M, Lund E, González CA, Barcos A, Berglund
G, Winkvist A, Mulligan A, Appleby P, Over-
vad K, Tjønneland A, Clavel-Chapelon F,
Kesse E, Ferrari P, Van Staveren WA, Riboli
E: Diversity of dietary patterns observed in
the European Prospective Investigation into
Cancer and Nutrition (EPIC) project. Public
Health Nutr 2007;
5: 1311.
35 Darvin ME, Sandhagen C, Koecher W, Sterry
W, Lademann J, Meinke MC: Comparison of
two methods for noninvasive determination
of carotenoids in human and animal skin: Ra-
man spectroscopy versus reflection spectros-
copy. J Biophotonics 2012;
5: 550–558.
36 Haag SF, Taskoparan B, Darvin ME, Groth N,
Lademann J, Sterry W, Meinke MC: Determi-
nation of the antioxidative capacity of the skin
in vivo using resonance Raman and electron
paramagnetic resonance spectroscopy. Exp
Dermatol 2011;
20: 483–487.
37 Stahl W, Heinrich U, Jungmann H, von Laar
J, Schietzel M, Sies H, Tronnier H: Increased
dermal carotenoid levels assessed by noninva-
sive reflection spectrophotometry correlate
with serum levels in women ingesting Be-
tatene. J Nutr 1998;
128: 903–907.
38 Schönwälder K: Why Germany’s guest work-
ers were largely Europeans: the selective prin-
ciples of post-war labour recruitment policy.
Ethn Racial Stud 2004;
27: 248–265.
39 Meinke MC, Lauer A, Taskoparan B, Gersonde
I, Lademann J, Darvin ME: Influence on the
carotenoid levels of skin arising from age, gen-
der, body mass index in smoking/non-smoking
individuals. Free Radic Antioxid 2011;
1: 15–20.
40 World Health Organization: WHO report on
the global tobacco epidemic, 2011: warning
about the dangers of tobacco. WHO Library
Cataloguing-in-Publication Data 2011:
130
(online). http://www.who.int/tobacco/global_
report/2011/en/.
41 Statistisches Bundesamt Zweigstelle Bonn
destinies BN: Mikrozensus – Fragen zur Ge-
sundheit. 2009.
42 Hähner-Rombach S, Schweikardt C: Quellen
zur Geschichte der Krankenpflege: mit Ein-
führungen und Kommentaren. Mabuse-Ver-
lag, 2008.
43 Kim E, Wolpin S: The Korean American fam-
ily: adolescents versus parents acculturation
to American culture. J Cult Divers 2008;
15:
108–116.
44 Yang CK: Age-related changes in sleep/wake
patterns among Korean teenagers. Pediatrics
2005;
115: 250–256.
45 Gelfand MJ, Raver JL, Nishii L, Leslie LM, Lun
J, Lim BC, Duan LL, Almaliach A, Ang S, Ar-
nadottir J, Aycan Z, Boehnke K, Boski P, Ca-
becinhas R, Chan D, Chhokar J, D’Amato A,
Ferrer M, Fischlmayr IC, Fischer R, Fulop M,
Georgas J, Kashima ES, Kashima Y, Kim K,
Lempereur A, Marquez P, Othman R, Over-
laet B, Panagiotopoulou P, Peltzer K, Perez-
Florizno LR, Ponomarenko L, Realo A, Schei
V, Schmitt M, Smith PB, Soomro N, Szabo E,
Taveesin N, Toyama M, Van de Vliert E,
Vohra N, Ward C, Yamaguchi S: Differences
between tight and loose cultures: a 33-nation
study. Science 2011;
332: 1100–1104.
46 OECD: OECD Labour Force Statistics. 2011.
47 OECD: Suicides. OECD Factbook 2013: Eco-
nomic, Environmental and Social Statistics.
OECD, 2013.
48 Kim S-W, Yoon J-S: Suicide, an urgent health
issue in Korea. J Korean Med Sci 2013; 28:
345–347.
49 Normile D: Public health. Korea tackles a
mushrooming problem. Science 2012;
338:
1026–1027.
50 Park S-G, Min K-B, Chang S-J, Kim H-C, Min
J-Y: Job stress and depressive symptoms
among Korean employees: the effects of cul-
ture on work. Int Arch Occup Environ Health
2008;
82: 397–405.
51 Choi S-M, Park YS, Yoo J-H, Kim G-Y: Oc-
cupational stress and physical symptoms
among family medicine residents. Korean J
Fam Med 2013;
34: 49.
52 KCDC Division of Health and Nutrition Ex-
amination Surveys MDoSHaS: 2011 online
survey on youth health status concerning
smoking, drinking and eating habits and sleep
patterns of adolescents. 2011.
53 Boehm JK, Williams DR, Rimm EB, Ryff C,
Kubzansky LD: Association between opti-
mism and serum antioxidants in the midlife
in the United States study. Psychosom Med
2012;
75: 2–10.
54 Kromeyer-Hauschild K, Glasser N, Zellner K:
Percentile curves for skinfold thickness in 7-
to 14-year-old children and adolescents from
Jena, Germany. Eur J Clin Nut 2012;66:613–
621.
Downloaded by:
Charité - Universitätsmedizin Berlin
193.175.73.207 - 6/26/2014 10:09:08 AM