![The Beagley-Gibson (1980) grading of cutaneous microtopographs. (Source: [31] Beagley J and Gibson IM. Changes in skin condition in relation to degree of exposure to ultraviolet light. School of Biology, Western Australia Institute of Technology, Perth, 1980).](https://www.researchgate.net/profile/Antigone-Kouris-Blazos/publication/12041521/figure/fig1/AS:276940616421384@1443039196970/The-Beagley-Gibson-1980-grading-of-cutaneous-microtopographs-Source-31-Beagley-J_Q320.jpg)
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Original Research
Skin Wrinkling: Can Food Make a Difference?
Martalena br Purba, BSc, MCN, Antigone Kouris-Blazos, PhD, Naiyana Wattanapenpaiboon, PhD,
Widjaja Lukito, MD, PhD, Elizabet M Rothenberg, PhD, Bertil C. Steen, MD, PhD, and Mark L. Wahlqvist, MD, FACN
International Health and Development Unit, Faculty of Medicine Nursing and Health Sciences and Asia Pacific Health and
Nutrition Centre, Monash University, Melbourne, Victoria, AUSTRALIA (M.b.P., A.K.-B., N.W., M.L.W.), SEAMEO-TROPMED
Regional Center for Community Nutrition, University of Indonesia, Jakarta, INDONESIA (W.L.), Department of Geriatric
Medicine, Vasa Hospital, Goteborg University, SWEDEN (E.M.R., B.C.S.)
Key words: food intake, nutrients, Caucasian elderly, actinic skin wrinkling, photoaging
Objectives: This study addressed whether food and nutrient intakes were correlated with skin wrinkling in
a sun-exposed site.
Methods: 177 Greek-born subjects living in Melbourne (GRM), 69 Greek subjects living in rural Greece
(GRG), 48 Anglo-Celtic Australian (ACA) elderly living in Melbourne and 159 Swedish subjects living in
Sweden (SWE) participating in the International Union of Nutritional Sciences IUNS “Food Habits in Later
Life” study had their dietary intakes measured and their skin assessed. Food and nutrient intakes were assessed
using a validated semi-quantitative food frequency questionnaire (FFQ). Skin wrinkling was measured using a
cutaneous microtopographic method.
Results: SWE elderly had the least skin wrinkling in a sun-exposed site, followed by GRM, GRG and ACA.
Correlation analyses on the pooled data and using the major food groups suggested that there may be less actinic
skin damage with a higher intake of vegetables (r
s
⫽⫺0.31, p⬍0.0001), olive oil (r
s
⫽⫺0.29, p⬍0.0001), fish
(r
s
⫽⫺0.24, p⬍0.0001) and legumes (r
s
⫽⫺0.16, p⬍0.0001), and lower intakes of butter (r
s
⫽0.46, p⬍0.0001)
and margarine (r
s
⫽0.24, p⬍0.001), milk products (r
s
⫽0.16, p⬍0.01) and sugar products (r
s
⫽0.12, p⬍0.01).
Similar findings were obtained using regression analyses, except fish was no longer significant; 32% of the
variance for actinic skin damage was predicted by six out of the ten major food groups. In particular, a high
intake of vegetables, legumes and olive oil appeared to be protective against cutaneous actinic damage
(collectively explaining 20% of the variance); a high intake of meat, dairy and butter appeared to be adverse
(explaining ⬍5% of the variance). Prunes, apples and tea explained 34% of variance amongst ACA.
Conclusion: This study illustrates that skin wrinkling in a sun-exposed site in older people of various ethnic
backgrounds may be influenced by the types of foods consumed.
INTRODUCTION
The skin is at relatively high risk of damage from reactive
oxygen species (ROS) for at least two reasons. Firstly, it is
exposed to oxygen by virtue of its rich blood flow and the even
higher oxygen tension that occurs in the air at its surface. Sec-
ondly, the skin is a light sensitive organ in relation to a number of
physiological phenomena including cellular metabolism and dif-
ferentiation [1], and while it requires light to function appropri-
ately through compounds capable of absorbing light and acting as
photosensitizers, it is a rich source of ROS generated by ultraviolet
wave length. Peroxidative damage to epidermal cells [2–4] and
underlying connective tissue is recognized cosmetically as skin
aging. The question is whether food components can modulate this
actinic damage. Indeed, it is a proposition of fundamental health
significance that, for skin to be an effectively functional organ, it
may need to be nourished in a protective way which allows light
exposure without damage.
Candidate nutrients that might offset the extent of actinic
damage include those which are found in sufficient quantity in
skin and are either oxidizable or antioxidant or indirectly in-
fluence these activities. The fatty acid composition of the
epidermis is 25% unsaturated [5], relatively chemically unsta-
ble and susceptible to ROS. Oxidative stress, particularly in
Address correspondence to: Prof. Mark Wahlqvist, International Health and Development Unit, P.O. Box 11A, Monash University, Victoria 3800, AUSTRALIA. E-mail:
mark.wahlqvist@med.monash.edu.au.
Journal of the American College of Nutrition, Vol. 20, No. 1, 71–80 (2001)
Published by the American College of Nutrition
71
skin, is induced by photo-damage, inflammation and ischemia-
reperfusion. Under these circumstances, many skin antioxi-
dants undergo depletion [6–12] and must be replaced contin-
uously in order to delay the otherwise inevitable deterioration
which would lead to skin aging. There is considerable interest
in the use of natural compounds in skin protection. Topical
application of antioxidants, experimentally, indicates that they
may usefully decrease photo-damage and associated inflamma-
tion [13–17]. The use of various antioxidants such as vitamin C
[13,14], vitamin E (
␣
-tocopherol) [18,19] and their combina-
tions [20,21] as topical photo-protectants has been the subject
of various investigations. However, the role of daily food
intake in actinic skin damage has not been studied so far.
The work reported here addresses this issue by focussing on
older individuals where actinic damage is more manifest and
where the differential between individuals is greater. By exam-
ining food and nutrient intakes in relation to actinic damage,
within and between food cultures, the opportunity to recognize
such relationships is increased. We have studied Caucasians of
Anglo-Celtic, Greek and Swedish ancestry, living in Australia,
Greece and Sweden where actinic exposures differ. Our find-
ings are of interest in relation to the role of food in cutaneous
aging, inflammatory skin disorders and skin cancer [22] and to
the underlying mechanisms.
SUBJECTS AND METHODS
Subject Selection
The International Union on Nutritional Sciences “Food Habits
in Later Life (FHILL) Study” investigated the food habits of
approximately 2000 people aged 70 and older in Australia,
Greece, China, Japan, Sweden. Study design and subject selection
criteria details have been published elsewhere [23,24]. The present
report presents findings on skin measurements and food intake on
Greek-born subjects living in Melbourne (GRM) (n⫽177), Greeks
living in rural Greece (GRG) (n⫽69), Anglo-Celtic Australians
(ACA) living in Melbourne (n⫽48) and Swedes living in Gote-
borg, Sweden (SWE) (n⫽159).
Food Frequency Questionnaire (FFQ)
Data were collected through interviewer-administered ques-
tionnaires, clinical, history and physical examination. Informa-
tion on the dietary habits of each subject during the previous
year was obtained from a validated semi-quantitative food
frequency questionnaire (FFQ) [25]. A core FFQ was devel-
oped by the principal investigators which was then adapted by
co-investigators in different countries and made more culturally
sensitive by including culture-specific foods and dishes.
In brief, participants were asked to estimate the average
frequency of consumption of each food over the past year in
terms of a standard portion size. Portion sizes were specified in
units thought to be the most appropriate for the given food.
There are three frequency categories, ranging from daily to
weekly and monthly. From the average daily intakes of differ-
ent food items, nutrient intakes were derived using food com-
position tables. The Australian nutrient analyses program
(NUTTAB 1995) was used which is based on Australian food
composition tables [26]. This program was modified to include
additional Greek dishes [27] and Swedish foods [28]. The food
items were treated individually: 254 food items for GRM, 72
foods for GRG, 370 foods for ACA and 210 foods for SWE.
The food items were then grouped into minor food groups (55
food groups for GRM or GRG, 77 food groups for ACA and 43
food groups for SWE). Finally, the foods were grouped into 10
major food groups: milk/milk products, meat, fish, legume,
cereal, vegetables, fruits, oils/fats, sugar/sugar products and
alcohol. Swedish data did not have a separate oil/fats food
group because they were included in various recipes/dishes. We
were unable to identify the quantity of oil/fat used in dishes in
order to generate this food group and thus excluded the Swed-
ish data when analyzing fat intake and skin wrinkling.
Skin Microtopographic Method
A non-invasive skin test was performed on the back of the
hand using a cutaneous microtopographic method to assess actinic
damage. The back of the hand was chosen as a site for measuring
sun-exposure because the method at this site has been developed
and validated by Holman and colleagues [29,30]. Furthermore,
microtopographic measurements at other convenient sites, such as
the face, may be less reliable due to the popular use of facial
cosmetics to prevent wrinkling and UV damage.
The silicon rubber impression material (Optosil Flussig, Bayer,
Leverkusen, Germany), a viscous white liquid which sets in three
to five minutes after addition of a catalyst, was spread on the skin.
When the rubber was set, it was stripped slowly and steadily from
the skin. This caused no pain to the subjects. So that the assess-
ment was blinded, the microtopographs were assigned random
numbers. They were graded according to a six-step scale using a
binocular microscope (⫻10 magnification). The method used was
that described by Beagley and Gibson (Fig. 1) [31] to grade
cutaneous microtopograph differences which ranged from 1 to 6.
A high grade indicates extensive wrinkling and is regarded as an
index of severe actinic damage, but this may be influenced by
other factors.
Data Analyses
Non parametric Spearman correlation coefficients (r
s
) were
calculated to consider associations between actinic skin wrin-
kling and either 10 food major food groups or 43 to 77 minor
food groups or 72 to 370 food items or nutrient intakes for each
ethnic group and for the pooled data. Multiple regression anal-
yses were also performed to determine the importance of age,
gender, smoking and foods (major food groups used in pooled
data and food items used with individual ethnic groups) in
explaining the variance of actinic skin damage. Throughout the
analyses, the SAS statistical package [32] was used.
Skin Wrinkling: Can Food Make a Difference?
72 VOL. 20, NO. 1
RESULTS
Table 1 shows the distribution of the 453 study subjects by
ethnic origin, gender, age and degree of skin wrinkling. SWE
elderly had the least skin wrinkling in a sun-exposed site,
followed by GRM, GRG and ACA. Table 2 shows the mean
daily intake of the 10 major food groups.
Actinic Skin Wrinkling, Age, Gender and
Smoking Status
Age was positively correlated (r
s
⫽0.27, p⬍0.0001) with ac-
tinic skin damage; therefore, all analyses were age-adjusted. Even
though actinic skin wrinkling was not significantly correlated with
gender or smoking by ethnic group or in the pooled data, all
analyses controlled for smoking status because smoking has been
reported in other studies to increase skin wrinkling [33].
Actinic Skin Wrinkling and Food Intake
Correlation analyses on the pooled data and using the
major food groups suggested that there may be less actinic
skin damage with a higher intake of vegetables (r
s
⫽⫺0.31,
p⬍0.0001), olive oil (r
s
⫽⫺0.29, p⬍0.0001), fish
(r
s
⫽⫺0.24, p⬍0.0001) and legumes (r
s
⫽⫺0.16, p⬍0.0001)
after controlling for age and smoking. More actinic skin
damage was seen with higher intakes of dairy foods
(r
s
⫽0.16, p⬍0.01), butter (r
s
⫽0.46, p⬍0.0001), margarine
(r
s
⫽0.24, p⬍0.001) and sugar products (r
s
⫽0.12, p⬍0.01)
(Table 3).
Correlation analyses on the individual ethnic groups were
as follows: Greek-born Australians with a low intake of milk
and coffee, but a high intake of legumes, mousaka, eggplant
dip, garlic, low fat yogurt and polyunsaturated oil had the
least skin wrinkling (Table 4). Greek elderly living in rural
Greece with a low intake of milk, processed meat, pudding
and dessert, fat spread (mainly butter), but a high intake of
green leafy vegetables, broad beans and cheese had the least
skin damage. Certain foods were negatively associated (pro-
tective) with skin wrinkling amongst Anglo-Celtic Austra-
lians: sardines, cheese, asparagus, celery, vegetable juice,
cherries, grapes, melon, apple, fruit salad, jam, multigrain
bread, prunes and tea. Swedish elderly with a low intake of
roast beef, meat soup, fried potato, canteloup, grapes,
canned fruit, ice cream, cakes and pastries, jam and soft
drink, but a high intake of egg, skimmed milk, yogurt, lima
bean and spinach pie had better skin.
Fig. 1. The Beagley-Gibson (1980) grading of cutaneous microtopo-
graphs. (Source: [31] Beagley J and Gibson IM. Changes in skin
condition in relation to degree of exposure to ultraviolet light. School
of Biology, Western Australia Institute of Technology, Perth, 1980).
Table 1. Demographic Characteristic of the Study Population
GRM
n⫽177)
GRG
n⫽69
ACA
n⫽48
SWE
n⫽159
Gender (%)
Men 49 42 50 67
Women 51 58 50 33
Age (years)
Mean
b
77.57⫾0.33 77.56⫾0.55 74.11⫾0.47 78.15⫾0.48
Median (min-max) 77 (70–104) 76.5 (70–94) 73 (70–92) 78 (69–96)
Age ⱖ80 y, n (%) 64 (33.9) 41 (39.4) 16 (11.3) 85 (28.7)
Skin Hand
a
Mean
b
4.87⫾0.05 5.06⫾0.10 5.14⫾0.12 4.74⫾0.08
Median (min-max) 5.0 (2.7–6.0) 5.3 (3.7–6.0) 5.4 (3.5–6.0) 5.0 (3–6)
a
Age adjusted.
b
Data are in mean ⫾ (SE).
GRM⫽Greek-born Australians living in Melbourne.
GRG⫽Greeks living in Greece.
ACA⫽Anglo-Celtic Australians living in Melbourne.
SWE⫽Swedes living in Sweden.
Skin Wrinkling: Can Food Make a Difference?
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 73
Actinic Skin Wrinkling and Nutrient Intake
Total fat intake was negatively correlated with actinic skin
damage (r
s
⫽⫺0.10, p⬍0.05) (Table 5). However, the only
fatty acid which was significantly associated with actinic dam-
age was monounsaturated fatty acid in a protective way
(r
s
⫽⫺0.15, p ⬍0.01). Vitamin C, retinol and intake of minerals
such as calcium, phosphorus, magnesium, iron and zinc also
appeared to be protective against cutaneous actinic damage
(age and smoking adjusted).
Food and Nutrient Predictors of Actinic Skin
Damage (Multiple Regression Analyses)
Multiple regression analyses on the pooled data indicated
that about 32% of the variance for actinic skin damage was
Table 2. Mean Intake of Major Food Groups (gram/day) by Ethnicity and Total Sample
Food Groups GRM GRG ACA SWED TOTAL
Dairy 232⫾187 184⫾129 312⫾163 431⫾241 284⫾209
Meat 170⫾76 97⫾56 162⫾91 126⫾64 136⫾77
Fish 69⫾52 60⫾44 20⫾19 84⫾55 61⫾50
Legumes 86⫾61 51⫾36 15⫾45 23⫾28 46⫾52
Cereal 244⫾97 270⫾129 243⫾127 232⫾137 248⫾123
Fruit 220⫾127 180⫾116 307⫾179 273⫾192 238⫾160
Vegetables 415⫾172 304⫾153 210⫾130 346⫾158 328⫾170
Oil and Fats
Olive 9.4⫾17.9 30.7⫾11.9 0.1⫾0.2 NA 13.3⫾18.2
Olive oil 18.1⫾13.3 30.8⫾12.2 0.0 NA 17.7⫾15.7
Other oil 3.7⫾8.0 0.0 0.0 NA 2.6⫾6.9
Butter 0.8⫾2.9 0.3⫾1.3 35.9⫾7.4 NA 10.2⫾16.5
Margarine 2.8⫾4.3 0.0 15.0⫾12.9 NA 4.8⫾8.8
Sugar and
Sugar
Products 89⫾119 66⫾88 165⫾175 227⫾211 132⫾166
Alcohol 84⫾136 104⫾161 168⫾319 NA 112⫾206
GRM⫽Greek-born Australians living in Melbourne.
GRG⫽Greeks living in Greece.
ACA⫽Anglo-Celtic Australians living in Melbourne.
SWE⫽Swedes living in Sweden.
NA⫽data not available; Swedish food was entered as recipes which included oil and fats.
Table 3. Correlation (r
s
) between Skin Wrinkling and Major Food Groups (Age and Smoking Adjusted)
Food Groups
GRM
N⫽177
GRG
N⫽69
ACA
N⫽48
SWED
N⫽153
TOTAL
N⫽453
Dairy 0.01 0.23* ⫺0.08 0.11 0.16**
Meat 0.13 ⫺0.18 ⫺0.03 0.05 0.06
Fish ⫺0.03 ⫺0.04 ⫺0.10 ⫺0.04 ⫺0.24****
Legumes ⫺0.12 ⫺0.12 ⫺0.16 0.10 ⫺0.16***
Cereal ⫺0.10 ⫺0.10 ⫺0.16 0.16 0.07
Fruit ⫺0.06 ⫺0.06 ⫺0.25 0.12 0.03
Vegetables ⫺0.04 ⫺0.08 ⫺0.07 0.01 ⫺0.31****
Oil & fats ⫺0.14 0.12 ⫺0.11 NA ⫺0.21***
Olive ⫺0.06 0.12 ⫺0.30 NA ⫺0.32****
Olive Oil ⫺0.02 0.13 0.00 NA ⫺0.29****
Other Oil 0.07 0.00 0.00 NA ⫺0.05
Butter ⫺0.04 0.31* ⫺0.06 NA 0.46****
Margarine ⫺0.04 0.00 ⫺0.11 NA 0.24***
Sugar Products 0.06 0.03 ⫺0.00 0.20* 0.12**
Alcohol ⫺0.04 ⫺0.12 0.15 NA ⫺0.00
Significant differences⫽* p⬍0.05, ** p⬍0.01, *** p⬍0.001, **** p⬍0.0001.
GRM⫽Greek-born Australians living in Melbourne.
GRG⫽Greeks living in Greece.
ACA⫽Anglo-Celtic Australians living in Melbourne.
SWE⫽Swedes living in Sweden.
NA⫽Swedish data on oils/fats not available; analyses of oils/fats for total sample does not include Swedish data.
Skin Wrinkling: Can Food Make a Difference?
74 VOL. 20, NO. 1
predicted or could be explained by eight out of the ten major
food groups. In particular, a high intake of oil (mainly olive
oil), legumes, fish, vegetables and cereal appeared to be pro-
tective against cutaneous actinic damage (collectively ex-
plained 20% of the variance) (Fig. 2). In contrast, a high intake
of meat, sugar and its products and dairy products appeared to
be adverse (explaining ⬍5% of the variance). In addition,
intakes of nutrients such as fat, carbohydrate, vitamin C, reti-
nol, iron, phosphorus and magnesium predicted 25% of the
variance for actinic damage (Table 6a). When the type of fats
(polyunsaturated, monounsaturated, saturated) was put into the
model, the variance increased to 39%; monounsaturated fats
and zinc appeared to be protective against photoaging (explain-
ing 10% of the variance) while saturated fats and vitamin C
appeared to be adverse (explaining 10% of the variance) (Table
6b). When multiple regression analyses were run with minor
food groups, the predictive power of food was 10% for GRM,
36% for GRG, 85% for ACA and 41% for SWE. GRM with
high intakes of nuts, olives, low fat spread and dips, but low
intakes of milk, crispbread and soups had the least actinic
damage (Table 7). GRG subjects with a high intake of green
leafy vegetables, garlic, rice and chicken, but a low intake of fat
spread (mainly butter), shellfish and processed meat had the
least cutaneous damage. Three food groups, namely dried
fruits, apples and tea, explained 34% of variance amongst ACA
(Table 8). SWE elderly with a high intake of vegetable dishes,
eggs, water, but a low intake cereal, bread and soft drinks had
the least skin damage (Table 7).
DISCUSSION
Foods Protective Against Skin Wrinkling
This was a cross-sectional study to investigate the associa-
tion between actinic skin damage and dietary intake. We found
that Swedish elderly had the least skin wrinkling, followed by
Greeks in Melbourne, Greeks in rural Greece and Anglo-Celt
Australians. Despite genetic differences, other factors such as
geographical area and life style differences might influence the
skin. Swedish people, for example, tend to seek sunlight due to
the short period of summer. Overall, our finding suggest that
subjects with a higher intake of vegetables, olive oil and mono-
unsaturated fat and legumes, but a lower intake of milk/milk
products, butter, margarine and sugar products had less skin
wrinkling in a sun-exposed site. There may be covariance
between food categories in which a cuisine may operate on skin
biology.
Smoking was not a significant predictor of skin wrinkling in
this cohort of elderly people. We suspect that the high vegeta-
ble intakes of the smokers (mean 308g/day) may have masked
or antagonized the effects of smoking on skin biology. Never-
theless, smoking has been found to influence skin wrinkling in
Table 4. Correlation between Actinic Skin and Food Item
Intake and Mean Intake of Food Items by Ethnicity
Ethnicity Food Items r
s
Mean⫾STD
(g or mL/day)
GRM Evaporated Milk 0.12* 135⫾157
Instant Coffee 0.19** 0.45⫾0.79
Legumes ⫺0.11 68⫾52
Mousaka ⫺0.17* 2.0⫾4.9
Eggplant Dip ⫺0.16* 0.22⫾1.10
Garlic ⫺0.20** 1.21⫾2.70
Yoghurt (low fat) ⫺0.14* 5.14⫾25.29
Polyunsaturated oil ⫺0.16* 1.16⫾4.82
GRG Milk 0.25* 100⫾107
Processed Meat 0.22 1.64⫾10.47
Pudding/Dessert 0.24* 6.92⫾14.61
Fat Spread 0.31* 0.27⫾1.34
Green Leafy Vegetables ⫺0.21 62.50⫾54.56
Broad Bean Boiled ⫺0.22 2.77⫾3.46
Cheese, (Kefalotiri) ⫺0.24* 3.46⫾7.40
ACA Sandwich Meat 0.43** 0.47⫾1.80
Mashed Potatoes 0.44** 27.03⫾57.11
Cocoa 0.35* 5.46⫾25.17
Salmon 0.35* 0.25⫾1.42
Low Alcohol Beer 0.39* 39.28⫾107.1
Tin Sardines ⫺0.34 1.20⫾2.38
Phila Cheese ⫺0.35* 0.11⫾0.61
Asparagus ⫺0.36* 1.73⫾4.05
Celery ⫺0.46** 7.56⫾10.12
Vegetables Juice ⫺0.35* 13.50⫾87.24
Cherries ⫺0.46** 0.57⫾1.69
Grapes ⫺0.34 5.46⫾9.94
Melon ⫺0.44** 5.46⫾14.01
Apple ⫺0.37* 0.44⫾1.60
Fruit Salad ⫺0.36* 7.63⫾17.62
Multi Grain Bread ⫺0.50** 19.17⫾47.92
Dried Prunes ⫺0.42** 1.64⫾5.96
Tea ⫺0.54*** 679⫾520
SWE Roast Beef 0.16* 34.5⫾24.4
Meat Soup 0.25* 10⫾15
Fried Potato 0.24* 9⫾18
Cantaloupe 0.19* 3⫾6
Grapes 0.20* 12⫾23
Canned Fruit 0.23* 6⫾13
Ice Cream 0.20* 8⫾14
Plain Cake 0.18* 14⫾23
Marmalade Jam 0.20* 12⫾15
Soft Drink 0.27* 60⫾151
Brown Meat 0.21* 3⫾8
Danish Pastry 0.17* 3⫾9
Sweet Pastry 0.16* 2⫾5
Egg ⫺0.17* 16⫾19
Skimmed Milk ⫺0.15 132⫾204
Yogurt ⫺0.14 5.6⫾33.2
Chicken Soup ⫺0.20** 0.4⫾2.8
Lima Bean Casserole ⫺0.21** 0.2⫾1.6
Spinach pie ⫺0.19* 0.2⫾1.5
Water ⫺0.17* 539⫾464
Significant differences⫽* p⬍0.05, ** p⬍0.01, *** p⬍0.001, **** p⬍0.0001.
GRM⫽Greek-born Australians living in Melbourne.
GRG⫽Greeks living in Greece.
ACA⫽Anglo-Celtic Australians living in Melbourne.
SWE⫽Swedes living in Sweden.
Skin Wrinkling: Can Food Make a Difference?
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 75
other studies [33]. We therefore proceeded to adjust for smok-
ing to enable us to consider the effect of vegetables on skin in
their own right.
The former group of foods may have partly contributed to
the less skin wrinkling due to their high content of antioxidant
vitamins and phytochemicals. A protective effect of antioxi-
dants such as vitamin C, vitamin E, retinoic acid, co-enzyme
Q10 as a topical treatment and prevention of photoaging has
been documented [19,34,35]. It is generally accepted that,
being the largest surface area of the body, skin is a major target
of oxidative stress. Skin is very susceptible to oxidative damage
due to its high content of lipids, proteins and DNA, which are
extremely sensitive to the oxidation process [36]. However, by
consuming vegetables, legumes and olive oil, the oxidation of
the skin could be protected against. In the Greek cuisine,
vegetables and legumes are consumed with olive oil. This
combination of foods may provide further benefit in preventing
skin wrinkling if the oil assists in the absorption of fat-soluble
antioxidant vitamins and phytochemicals, such as vitamin E,
lycopene and isoflavones. Fish intake was significantly corre-
lated with less skin wrinkling, but this association was not
Table 5. Correlation between Actinic Skin Damage and Nutrients (Age and Smoking Adjustment)
Nutrients GRM GRG ACA SWED TOTAL
Protein 0.05 ⫺0.15 ⫺0.08 0.06 0.01
Fat ⫺0.04 0.11 ⫺0.03 0.12 ⫺0.10*
SFA 0.03 0.07 0.01 0.15 ⫺0.03
MUFA ⫺0.09 0.12 0.01 0.11 ⫺0.15**
PUFA ⫺0.07 0.07 ⫺0.18 0.05 ⫺0.08
Cholesterol 0.14 ⫺0.01 0.00 NA 0.00
Carbohydrate ⫺0.02 ⫺0.14 ⫺0.18 0.17* 0.09
Calcium ⫺0.03 ⫺0.02 0.10 0.07 ⫺0.25****
Phosphorus 0.00 ⫺0.10 ⫺0.01 0.06 ⫺0.28****
Magnesium ⫺0.11 ⫺0.17 0.11 0.12 ⫺0.35****
Iron ⫺0.09 0.02 0.15 0.12 ⫺0.25****
Zinc 0.03 ⫺0.10 0.13 0.11 ⫺0.25****
Retinol 0.10 0.01 ⫺0.35 0.16* ⫺0.16**
Vitamin C 0.01 ⫺0.07 0.13 0.08 ⫺0.30****
Alcohol ⫺0.03 ⫺0.12 0.07 ⫺0.00 ⫺0.04
Significant differences⫽* p⬍0.05, ** p⬍0.01, *** p⬍0.001, **** p⬍0.0001.
GRM⫽Greek-born Australians living in Melbourne.
GRG⫽Greeks living in Greece.
ACA⫽Anglo-Celtic Australians living in Melbourne.
SWE⫽Swedes living in Sweden.
NA⫽data not available.
SFA⫽saturated fatty acid.
MUFA⫽monounsaturated fatty acid.
PUFA⫽polyunsaturated fatty acid.
Fig. 2. Food predictors of skin wrinkling. Multiple regression analyses
shows 32% of the variance was predicted by food intake. Oils, legumes,
fish, vegetables and cereal appeared to be protective (collectively
explained 20% of the variance). In contrast, a high intake of meat, sugar
products and dairy appeared to be adverse (explaining 5% of the
variance). Age and smoking explained 7% of the variance.
Table 6a. Nutrient Predictors of Actinic Skin Damage
a
Variable Parameter Estimate Standard Error Partial R
2
Age ⫺0.0226 0.0117 0.0045§
Smoking ⫺0.4032 0.0795 0.1237****
Nutrients
Retinol ⫺0.0003 0.0001 0.0357****
Iron ⫺0.0151 0.0063 0.0297***
Vitamin C ⫺0.0021 0.0010 0.0210***
Carbohydrate 0.0029 0.0011 0.0093*
Fat ⫺0.0121 0.0038 0.0160*
Phosphorus 0.0011 0.0004 0.0308***
Magnesium ⫺0.0031 0.0014 0.0086*
% Variance explained by the model R
2
(⫻100)⫽25%
a
Variables included in the analysis were age, gender, smoking and nutrients (fat
as total fat).
Significant level was set at 0.15 for variables to be entered into the model.
Significant level for F-test at which values are different from zero⫽* p⬍0.05,
** p⬍0.01, *** p⬍0.001, **** p⬍0.0001, § p⬍0.13.
Smoking status was classified as 3⫽smoker, 2⫽ex-smoker, 1⫽non-smoker, so
negative sign means non-smokers are less likely to have wrinkled skin.
Skin Wrinkling: Can Food Make a Difference?
76 VOL. 20, NO. 1
observed in the multiple regression analyses. The fact that fish
is also a significant source of n-3 polyunsaturated fatty acids is
of interest. But whether fish is protective against actinic dam-
age may depend on what it is eaten with. If fish is eaten with
salad or cooked vegetables, then it may be the antioxidant
carotenoids and other compounds in the plant foods which are
offering protection. Fish itself can also contain a significant
amount of antioxidants including carotenoids contributing to
fish color, Co-Q10 (ubiquinone) and vitamin E along with
components like fish sterols which may influence skin biology.
n⫺3 F fatty acids have been found to be useful in the treatment
of psoriasis [37].
For each ethnic population, vegetables, legumes and fer-
mented milk products were negatively correlated or predictive
of photoaging. In particular, full-fat milk (as opposed to skim
milk, cheese and yogurt), red meat (especially processed meat),
potatoes, soft drinks/cordials and cakes/pastries were associ-
ated with extensive skin wrinkling. In contrast, eggs, yogurt,
legumes (especially broad and lima beans), vegetables (espe-
cially green leafy/spinach, eggplant, asparagus, celery, onions/
leeks and garlic), nuts, olives, cherries, grapes, melon, dried
fruits/prunes, apples/pears, multigrain bread, jam, tea and water
were associated with less photoaging. Three food groups,
namely dried fruits (prunes), apples and tea, explained 34% of
variance amongst ACA.
Fruits, vegetables, tea (as well as herbs) with diverse phar-
macological properties have been shown to be rich sources of
phythochemicals with potential for the prevention and treat-
ment of noncommunicable disease. Recent studies in vitro have
shown that procyanidins in grape seeds possess anti-inflamma-
tory and anti-arthritis properties and prevent heart disease and
skin aging [38,39]. In other studies, polyphenols, which are
also found in prunes, apples and tea, have been shown to exert
a much stronger oxygen free radical scavenging effect than
vitamins C and E [40,41], and to prevent ultraviolet-C-induced
peroxidation [42].
Due to their antioxidant activity, polyphenols present in
plant food [43–47] such as tea, apples, onions, garlic and
eggplant appear to be partially responsible for many of the
protective effects against oxidative stress of the skin. Recent in
Table 6b. Nutrient Predictors of Actinic Skin Damage
a
Variable Parameter Estimate Standard Error Partial R
2
Smoking ⫺0.4032 0.0795 0.1843****
Nutrients
MUFA ⫺0.0422 0.0060 0.1002****
SFA 0.0553 0.0086 0.0917****
Zinc ⫺0.0346 0.0155 0.0072I
`
Vitamin C 0.0017 0.0009 0.0086*
% Variance explained by the model R
2
(⫻100)⫽39%
a
Variables included in the analysis were age, gender, smoking and nutrients (fat
as fatty acids).
Significant level was set at 0.15 for variables to be entered into the model.
Significant level for F-test at which values are different from zero⫽* p⬍0.05,
** p⬍0.01, *** p⬍0.001, **** p⬍0.0001, I
`
p⬍0.06.
Smoking status was classified as 3⫽smoker, 2⫽ex-smoker, 1⫽non-smoker, so
negative sign means non-smokers are less likely to have wrinkled skin.
MUFA⫽monounsaturated fatty acid.
PUFA⫽polyunsaturated fatty acid.
Table 7. Food Predictors of Actinic Skin Damage by
Ethnicity
Ethnicity Variables
Parameter
Estimate
Standard
Error
Partial R
2
GRM
Evaporated
Milk 0.0066 0.0034 0.0249**
Nuts ⫺0.0070 0.0039 0.0196*
Crispbread 0.0079 0.0039 0.0164*
Olives ⫺0.0052 0.0032 0.0158*
Low Fat Spread ⫺0.0758 0.0451 0.0108†
Dips ⫺0.0276 0.0169 0.0091§
Soups Broth
Type 0.0016 0.0011 0.0087§
% Variance explained by the model R
2
(⫻100)⫽10%
GRG Smoking 0.2067 0.0981 0.0347I
`
Fat Spread 0.1510 0.0482 0.0735*
Green Leafy
Vegetables ⫺0.0043 0.0015 0.0838**
Garlic ⫺0.164 0.0103 0.0444I
`
Shellfish 0.0354 0.0169 0.0325I
`
Processed Meat 0.0138 0.0059 0.0354I
`
Rice ⫺0.0081 0.0046 0.0254‡
Chicken/Turkey ⫺0.0055 0.0035 0.0270†
% Variance explained by the model R
2
(⫻100)⫽36%
SWE Age 0.0454 0.0152 0.0305†
Gender ⫺0.3666 0.1742 0.0387*
Smoking ⫺0.5154 0.2032 0.0234§
Vegetable Mix
Dish ⫺0.0044 0.0023 0.0453*
Eggs ⫺0.0124 0.0044 0.0391*
Soft Drinks &
Cordials 0.0010 0.0006 0.0397*
Flower
Vegetables 0.0062 0.0031 0.0271©
Fungi ⫺0.0426 0.0162 0.0267‡
Dessert and
Pudding 0.0029 0.0012 0.0373*
Water ⫺0.0005 0.0002 0.0317I
`
Bread 0.0028 0.0018 0.0221†
Tea 0.0718 0.0718 0.0298*
Green Leafy
Vegetables ⫺0.1238 0.0559 0.0168£
Chicken and
Turkey ⫺0.0165 0.0095 0.0228†
Root
Vegetables 0.0018 0.0011 0.0191©
% Variance explained by the model R
2
(⫻100)⫽41%
a
Variables included in the analyses were age, gender, smoking and minor food
groups.
b
Major food groups.
Significant level was set at 0.15 for variables to be entered into the model.
Significant level for F-test at which values are different from zero⫽* p⬍0.05,
** p⬍0.01, *** p⬍0.001, **** p⬍0.0001, ¥ p⬍0.1088, § p⬍0.1189, © p⬍0.09,
£ p⬍0.1475.
Smoking status was classified as 1⫽smoker, 2⫽ex-smoker, 3⫽non-smoker, so
negative sign means non-smokers are less likely to have wrinkled skin.
Skin Wrinkling: Can Food Make a Difference?
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 77
vitro evidence from Tufts University has identified prunes,
strawberries/berries, cherries, tea and the like to have the high-
est antioxidant activity compared to many other foods. Fla-
vonoids are among the most potent plant antioxidants because
of their involvement in antiradical activity [48]. In this study,
legume consumption also appeared to be protective against
actinic damage; this may be partly explained by their phy-
toestrogen content. Phytoestrogens have recently been identi-
fied to act as antioxidants [49,50].
Foods Associated with More Skin Wrinkling
A higher intake of full-fat milk, sweet milk desserts, ice-
cream, but not skim milk, yogurt or cheese, was associated with
a greater degree of photoaging. These foods explained only 5%
of the variance. This suggests that these foods may need to be
consumed with other protective foods, such as fruit, vegetables,
fish and legumes, to minimize any adverse effects on skin
health. Butter was also significantly correlated with more pho-
toaging and explained more than 50% of the variance for skin
wrinkling in the pooled data when the analysis only included
dietary fats and no other food groups. Even though saturated fat
is known to be resistant to oxidation, foods high in saturated fat
did not appear to protect against photoaging. There is evidence
that sugar and sugar products may contribute to a deterioration
in skin health via the glycosylation of proteins [51,52] in the
skin, which in turn may contribute to skin wrinkling and
photoaging.
Nutrients and Skin Wrinkling
In terms of nutrients, total dietary fat intake and a higher
intake of monounsaturated fatty acids were negatively associ-
ated with photoaging. About 25% of the fatty acid composition
of the epidermis consists of monounsaturated fatty acids [5].
The polyunsaturated fatty acids in the cell membranes are
prone to oxidation; in contrast, monounsaturated fats and sat-
urated fats resist oxidation [35]. A high intake of monounsat-
urated fat may increase the content of monounsaturated fatty
acids in the epidermis, which may in turn assist in reducing
oxidative damage. This may explain why a higher intake of
olive oil was associated with less photoaging and a higher
intake of polyunsaturated margarine was associated with more
photoaging. Intakes of micronutrients such as iron, zinc, cal-
cium, phosphorus, magnesium, retinol and vitamin C were
protective against actinic skin damage. Intakes of such nutrients
may partly increase the endogenous antioxidative capacity of
the skin. In the regression analyses, vitamin C was positively
associated with skin wrinkling (Table 6b). Vitamin C can act as
a pro-oxidant at levels above the recommended dietary intake
[53]. The vitamin C intakes of the subjects (127 mg/day) may
have reached the level where vitamin C acts as a pro-oxidant.
Pro-oxidants would theoretically increase the susceptibility to
photoaging. There is growing evidence that the important an-
tioxidants in human diets are much more than the vitamins C,
E or beta-carotene [54]; our finding supports this view.
CONCLUSION
This study illustrates that skin wrinkling in a sun-exposed
site in older people of various ethnic backgrounds may be
influenced by the types of foods consumed. Correlation and
regression analyses on the minor food groups and food items
for each ethnic group identified the following foods to be
positively associated with cutaneous actinic skin damage: full-
fat milk (as opposed to skim milk, cheese and yogurt), red meat
(especially processed meat), potatoes, soft drinks/cordials,
cakes/pastries. Negative associations were found with eggs,
yogurt, legumes (especially broad and lima beans), vegetables
(especially green leafy/spinach, eggplant, asparagus, celery,
onions/leeks, garlic), nuts, olives, cherries, melon, dried fruits/
prunes, apples/pears, multigrain bread, jam, tea and water.
Three food groups, namely dried fruits, apples and tea, ex-
plained 34% of variance amongst ACA. For nutrients, higher
intakes of total fat, especially monounsaturated fat, vitamin C,
calcium, phosphorus, magnesium, iron, zinc and retinol were
correlated with less actinic skin damage.
An intervention study is needed to investigate whether
cutaneous actinic damage could be prevented in part with
Table 8. Food Predictors of Actinic Skin Damage amongst
Anglo-Celtic Australian
Variables Parameter EstimateStandard Error Partial R
2
Smoking ⫺0.6747 0.0600 0.0379*
Food groups
b
Dried Fruits ⫺0.0481 0.0040 0.1672**
Apples & Pears ⫺0.0199 0.0011 0.0933*
Tea ⫺0.0005 0.0002 0.0826*
Salad Dressing 0.1233 0.0140 0.0572*
Leafy Green Vegetables ⫺0.0523 0.0064 0.0626*
Spirit and Liqueurs ⫺0.0371 0.0068 0.0472*
Nuts and Seeds 0.0579 0.0182 0.0518*
Ice Cream 0.0599 0.0042 0.0306I
`
Onion & Leeks ⫺0.0368 0.0099 0.0340*
Jam & Sweet Spread ⫺0.0160 0.0014 0.0280*
Other Confectionery ⫺0.1168 0.0118 0.0115§
Deli Meats ⫺0.2157 0.0762 0.0155©
Chocolate ⫺0.0438 0.0196 0.0167†
Bread & Rolls ⫺0.0030 0.0016 0.0100I
`
% Variance explained by the model R
2
(⫻100)⫽85%
a
Variables included in the analyses were age, gender, smoking and minor food
groups.
b
Minor food groups.
Significant level was set at 0.15 for variables to be entered into the model.
Significant level for F-test at which values are different from zero⫽* p⬍0.05,
** p⬍0.01, *** p⬍0.001, **** p⬍0.0001, I
`
p⬍0.06, † p⬍0.07, ‡ p⬍0.08;
© p⬍0.09, ¥ p⬍0.1088, £ p⬍0.1075, § p⬍0.1689.
Smoking status was classified as 1⫽smoker, 2⫽ex-smoker, 3⫽non-smoker, so
negative sign means non-smokers are less likely to have wrinkled skin.
Skin Wrinkling: Can Food Make a Difference?
78 VOL. 20, NO. 1
higher intakes of vegetables (especially green leafy, garlic/
onions, celery), legumes, olive oil, total fat (mainly monoun-
saturated), apples/pears, prunes, tea and possibly fish, cherries,
melons, minerals, vitamin C and retinol.
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