ARTICLE
Auteur(s) : Jae Yoon Jung1,2,
Mi Young Yoon1,2, Seong Uk Min1,2,
Jong Soo Hong1,2, Yu Sung
Choi1,2,3, Dae Hun Suh1,2
1Department of Dermatology, Seoul National
University College of Medicine, 28 Yongon-dong, Chongno-gu,
Seoul 110-744, Korea
2Acne Research Laboratory, Seoul National University
Hospital, Seoul, Korea
3Department of Dermatology, University
of Ulsan College of Medicine, Ulsan, Korea
accepté le 30 Juin 2010
The association between acne and food has been evaluated with
inconsistent results. Many previous reports have shown no
relationship between food and acne [1-5]. However, in other
reports, diet-induced hyperinsulinemia was suggested to cause an
endocrine response that affected the development of acne [6, 7]. In
addition, some patients report that certain foods make their acne
worse. The effects of diet on acne have been explained by different
mechanisms [7-9]. The diet may be an important source of the
substrate needed for the synthesis of sebaceous lipids and it may
influence androgen-mediated increases in sebum production. In
addition, diet-induced hyperinsulinemia elevates the insulin-like
growth factor-1 (IGF-1), while reducing insulin-like growth factor
binding protein-3 (IGFBP-3) [10-12]. Hence, these alterations may
stimulate follicular epithelial growth and keratinization.
Traditional Korean foods consist of a low glycemic load and low
fat content. However, adoption of Western dietary habits over the
past few decades has been associated with an increase in acne [13].
Previous studies on diet and acne have been mostly Western based
research. The dietary patterns and food of Korea are different from
those of Western countries. Therefore, the association of diet with
acne may be different in Korea.
The aim of the present study was to investigate the effect of
dietary patterns on acne vulgaris, and to evaluate the endocrine
differences in acne patients divided into subgroups influenced and
not influenced by food.
Methods
A total of 1,285 subjects were recruited for this study. Seven
hundred and eighty three acne patients and 502 controls
without acne were surveyed with a questionnaire about the
association of acne and food. The controls were age-matched healthy
people. They had no acne and did not receive any acne treatment. We
recruited them using bulletin boards in high schools, universities
and companies. The study was approved by the Institutional Review
Board at Seoul National University Hospital, and informed consent
was obtained from all subjects.
The subject's age, gender, weight, height, and severity of acne
were recorded. The body mass index (BMI) was calculated by dividing
the weight (kilograms) by the square of the height (meters). All
participants in the acne group had blood tests for insulin,
insulin-like growth factor-1 (IGF-1), insulin-like growth factor
binding protein-3 (IGFBP-3), post prandial 2 hours blood
glucose (PP2), and dehydroepiandrosterone sulphate (DHEAS) at the
initial visit.
Clinical assessment of the acne severity, including inflammatory
and non-inflammatory acne counts and acne severity evaluations,
were performed by two independent dermatologists, using Dr.
Cunliffe's grading system [14]. The dietary data was collected by a
self-completed questionnaire. The questionnaire used was based on
the questionnaire used in the diabetes clinic of our hospital; it
was modified for this study by the study investigators. The
questionnaire was verified for accuracy, reproducibility and
validity by specialists in nutrition and statistics. Many
representative Korean foods were included in the questionnaire and
they were specified by the methods of cooking. All participants
were provided with a questionnaire and instructions on how to fill
it out. The participants were required to indicate the type of food
and amount of foods eaten during a week, including snacks and a
midnight meal. We collected the questionnaire after one week. After
evaluating the results from the questionnaire, we asked the
subjects to confirm their answers.
In addition to the questions on food intake over one week, the
questionnaire also contained questions about the foods that
aggravated their acne. In addition, questions about aggravating
events were included, such as stress, food intake, menstruation,
fatigue, and lack of sleep. All the questions were multiple-choice.
If the aggravating factor was food, the aggravating foods were
specifically requested. The regularity of meals was also
investigated by questions about the inter-meal intervals and the
frequency of skipping meals (skipping each meal more than
3 times a week was considered irregular meal habits).
The data collected was analyzed by multiplying the frequency of
consumption of each unit of food, and the differences among the
three groups (control group, AF and NAF) were compared. In
addition, the glycemic index (GI) and the glycemic load (GL) were
investigated. Statistical analysis was performed using the
Statistical Package for the Social Sciences (SPSS) version 13. The
significant differences among the three groups (AF, NAF and control
group) were determined using the t-test, the Chi-Square test and
one way ANOVA. The Chi-square test was used to determine the
statistical significance of the qualitative variables, and the
t-test, and one way ANOVA were used to determine the significance
of the quantitative variables. P-values of less than 0.05 were
considered to be statistically significant.
Results
Among 1,285 patients included in this study, 783 (61%)
patients were acne patients and 502 (39%) were controls. We divided
them into a group aggravated by food (AF) and a group
not-aggravated by food (NAF) according to the participants’ answers
to the questionnaire about the effect of food on the aggravation of
the acne. The aggravation of acne was defined as an increase of
more than 25% in acne lesions compared to before taking a specific
food. Among the acne patients, 420 (54%) patients were in the AF
subgroup and 363 (46%) patients in the NAF subgroup. The mean age
of the subjects was 24.0 years, and the mean BMI was 21.3
kg/m2. There were 565 men (44%) and 720 women
(56%). There was no significant difference among the three groups
with respect to age, gender or body mass index
(P > .05). Mean baseline acne grades were 1.60 in the
AF and 1.75 in the NAF groups (figure 1). Overall,
the severity of acne was mild and there was no significant
difference between the two groups.
The events that aggravated the acne are shown in figure 2. Male acne
patients answered that food intake (49.5%) was the most important
factor for aggravating their acne; female acne patients answered
that menstruation (60.1%) was the most important aggravating factor
and food the second most important (56.3%). Among the foods, fatty
food (71.5%) was found to be the food most significantly associated
with the aggravation of acne compared to salty (22.1%), sugary
(8.0%), and spicy (11.0%). Regularity of meal habits was
significantly greater in the control group (71.3%) than in the acne
patients (AF: 44.4%, NAF: 39.0%) (P < .001). In particular, a
regular breakfast intake (figure 3, P < .001)
was significantly greater in the control group than in the acne
patients; however, there was no significant difference between the
AF and NAF subgroups.
Lists of the preferred foods for the acne and control groups are
summarized in table 1. The
frequency of vegetables (yellow, green leaf, cruciferous) (P =
.001), fish (white flesh and green fish, blue tuna) (P = .03) and
green peas (P < .001) was significantly higher in the control
group than in the acne patients. The intake of instant noodles (P =
.01), junk food (hamburger, doughnuts, croissants) (P = .002),
carbonated drinks (cola, fanta, soda pop) (P = .005), snacks (rice
cake, cracker, waffles) (P = .001), processed cheeses (P = .04),
pork (braised) (P = .02), pork (roast) (P < .001), chicken
(fried) (P = .001), chicken (stewed) (P = .001), seaweed (toasted
laver, boiled sea mustard) (P = .003), and nuts (almond, peanuts,
walnuts) (P = .002) were significantly higher in the acne patients
compared to the controls. When comparing the preferred foods
between the AF and NAF subgroups, intakes of roast pork (P = .02),
fried chicken (P < .02), and nuts (P = .03) were significantly
higher in the AF. In addition, the GL, total calorie and
nutritional composition of the preferred foods of the patients with
acne (AF, NAF) and the controls are summarized in table 1.
The IGF-1, IGFBP-3, insulin, PP2, and DHEAS levels of the acne
group are summarized in table 2.
The IGF-1 of the AF (543.9 ± 56.4 ng/mL) was significantly higher
than that of the NAF (391.3 ± 118.2 ng/mL) (P < 0.01). Although
not significantly different, the IGFBP-3 of the AF (3,876.9 ± 720.0
ng/mL) was lower than that of the NAF (4,458.0 ± 1,066.2 ng/mL).
The IGF-1 level was significantly higher in the males in the AF
(530 ng/mL) compared to the NAF (398 ng/mL) (P = .03),
and the IGFBP-3 was significantly lower in the females in the AF
(3,990.2 ng/mL) compared to the NAF (4,878.2 ng/mL) (P = .02).
Table 1 Lists of the food preferences
of the acne and control groups. Glycemic load (GL) and
nutritional components of the food
|
Control (%)
|
AF (%)
|
NAF (%)
|
GL
|
per 100 g
|
|
Energy (kcal)
|
Water (g)
|
Protein (g)
|
Fat (g)
|
Ash (g)
|
CHO (g)
|
|
Vegetables (green and light color)*
|
58.4
|
44.3
|
44.4
|
< 10
|
|
|
|
|
|
|
|
Green peas*
|
29.9
|
23.2
|
20.3
|
3
|
|
|
|
|
|
|
|
Hamburger, doughnuts, croissant†
|
12.4
|
21.1
|
21
|
> 20
|
|
|
|
|
|
|
|
Rice cake, cracker, waffles†
|
30.7
|
55.4
|
47.1
|
> 20
|
|
|
|
|
|
|
|
Instant noodle†
|
8.9
|
15.3
|
15.9
|
> 20
|
|
|
|
|
|
|
|
Carbonated drink (cola, fanta, soda pop)†
|
36.7
|
43.2
|
45.5
|
> 20
|
|
|
|
|
|
|
|
Processed cheese†
|
4.5
|
6.3
|
5.8
|
|
312
|
47.6
|
18.3
|
24.2
|
4.4
|
5.5
|
|
Pork (braised)†
|
8.6
|
10.5
|
11.3
|
|
307
|
49
|
24.9
|
25.7
|
0.4
|
0
|
|
Pork (roast)†,#
|
8.7
|
14.4
|
12.2
|
|
368
|
43.7
|
30.1
|
25.6
|
0.6
|
0
|
|
Chicken (fried)†,#
|
4
|
15
|
13.8
|
|
324
|
46.2
|
19.9
|
21.8
|
1.2
|
10.9
|
|
Chicken (stewed)†
|
8.1
|
44.6
|
40.6
|
|
243
|
62.3
|
20.8
|
16.5
|
0.4
|
0
|
|
Fish (white flesh fish & green fish, blue tuna)*
|
14
|
12.1
|
11.2
|
|
|
|
|
|
|
|
|
Alask pollack (broiled)
|
|
|
|
|
111
|
73
|
25.2
|
0.5
|
1.3
|
0
|
|
Hair tail (mild salted-cured and dried)
|
|
|
|
|
188
|
57.2
|
26.3
|
8.1
|
8.3
|
0.1
|
|
Yellow Croaker (salt)
|
|
|
|
|
332
|
32.6
|
44.4
|
15.2
|
7.4
|
0.4
|
|
Mackerel (broiled)
|
|
|
|
|
271
|
55.2
|
25.8
|
17.1
|
1.5
|
0.4
|
|
Seaweeds†
|
15.2
|
19.4
|
19.1
|
|
|
|
|
|
|
|
|
Toasted laver
|
|
|
|
|
128
|
4
|
43.3
|
0.9
|
10
|
41.7
|
|
Boiled sea mustard
|
|
|
|
|
15
|
84.9
|
1.1
|
0
|
8.2
|
5.5
|
|
Nuts†,#
|
3.3
|
6.4
|
4.3
|
|
|
|
|
|
|
|
|
Almonde (dried)
|
|
|
|
|
598
|
4.6
|
18.6
|
54.2
|
2.9
|
19.7
|
|
Peanuts (roasted)
|
|
|
|
|
567
|
2.2
|
25.6
|
48.2
|
2.4
|
21.6
|
|
Walnuts (dried)
|
|
|
|
|
652
|
3.5
|
15.4
|
66.7
|
1.8
|
12.6
|
Table 2 IGF-1, IGFBP-3, insulin, PP2, DHEAS levels
of AF and NAF
|
AF
|
NAF
|
|
Mean (SD)
|
Mean (SD)
|
|
IGF-1 (ng/mL)
|
543.9 (56.4)*
|
391.3 (118.2)*
|
|
IGFBP-3 (ng/mL)
|
3,876.9 (720.1)
|
4,458.0 (1,066.2)
|
|
Insulin (μU/mL)
|
12.7 (4.0)
|
12.5 (4.4)
|
|
PP2 (mg/dL)
|
93.8 (12.4)
|
91.4 (22.0)
|
|
DHEA-S (ng/mL)
|
2,382.3 (1,260.0)
|
2,016.2 (946.3)
|
Discussion
Hereditary factors have been shown to be important in the
development of acne as demonstrated by familial studies [15].
However, environmental factors are also thought to strongly
influence the development and aggravation of acne [16, 17], as acne
has not been observed in non-westernized populations, such as Ache
hunter-gatherers [6], Kitavan islanders [6] and Okinawa islanders
[18]. According to Korean national data, the major preferred source
of nutrients has shifted from carbohydrates to fat and meats; in
addition, the consumption of snacks, junk food and carbonated
drinks has significantly increased during the past several decades
[19]. Furthermore, the number of diabetic, obese and overweight
Koreans is increasing annually [20]. Along with these factors, the
acne incidence in Korea has been increasing over the past several
decades [13]. Dietary pattern changes are thought to be one of the
most important causes of such changes. The results of our study
confirm prior reports that food can affect acne; 54% of the
patients with acne had their condition aggravated by food (figure 2). In
retrospective studies, participants are required to remember what
they have eaten for a certain period of time; in such studies
recall bias could seriously influence the study results. Therefore,
this study used a prospective design to reduce such bias. Although
there are some validated food frequency questionnaires [21-23],
they could not be applied in the Korean setting. Hence we developed
our own questionnaire to fit Korean dietary habits. In addition,
our questionnaire also contained information on the regularity of
meal habits. The regularity of meal habits was significantly higher
in the control group than in the acne patients (figure 3). There are
no prior reports on the influence of irregular meal habits on acne.
These findings may be explained by the following. Irregular meal
habits may occur under stressful conditions. It is well-known that
stress can exacerbate acne. Moreover, irregular meal habits might
be associated with eating too fast and too much; which might result
in an increase of the GL.
Diet-induced hyperinsulinemia elevates IGF-1 and reduces IGFBP-3
[6]. IGF-1 stimulates basal keratinocyte proliferation and sebum
production. It also stimulates the synthesis of androgens in the
ovary and testis, and inhibits the synthesis of the sex hormone
binding globulin, hence increasing the effect of circulating
androgens which stimulate sebum production. IGFBP-3 prevents IGF-1
from binding to its receptor, and IGFBP-3 is a pro-apoptotic factor
in epithelial cells; hence a decreased level of IGFBP-3 stimulates
follicular epithelial growth and keratinization. In our study, the
AF patients showed significantly higher levels of IGF-1 than did
the NAF patients; in addition, the AF patients had a lower level of
IGFBP-3 than did the NAF patients (table 2). These findings support the
influence of a high glycemic diet on the aggravation of acne. A
significantly higher IGF-1 level was observed in the male AF
subgroup than in the male NAF subgroup, while a significantly lower
IGFBP-3 level was found in the female AF subgroup than in the
female NAF subgroup. The different response of IGF-1 and IGFBP-3,
according to gender, has not been previously reported.
The GI of an individual food is defined as 100 times the
ratio of the glycemic response of a test food to the glycemic
response of an equal portion of a reference carbohydrate, usually
white bread or glucose [24]. The GL includes both the quantity and
quality of dietary carbohydrate per serving by the GI value of the
food divided by 100 [24]. Therefore, high GI and GL foods cause a
rapid increase in the blood glucose levels and subsequent insulin
levels. In our study, high GL foods (hamburgers, doughnuts,
croissant, rice cake, cracker, waffles, instant noodles, and
carbonated drinks) were significantly more common in the acne
patients compared to the controls, and low GL foods (green and
light colored vegetables and green peas) were significantly lower
in acne patients than in the control group (table 1). Smith et al. reported the
therapeutic effect of a low GL dietary intervention in patients
with acne [25]. Twelve weeks of a low GL diet could reduce weight,
acne severity and the free androgen index, and increase IGFBP-1.
Smith et al. reported that a low glycemic load diet increased
the ratio of saturated to monounsaturated fatty acids of the skin
surface triglycerides [26]. The increase in the saturated to
mono-unsaturated ratio was inversely correlated with the acne
lesion counts (r = –.03), and increased follicular sebum outflow
was also associated with an increase in the proportion of
mono-unsaturated fatty acids in the sebum.
Recently, studies have reported a relationship between milk and
acne [9, 21-23]. In these reports, dairy food intake, including
cottage cheese and cream cheese, caused the aggravation of acne. In
our study, processed cheese was consumed significantly more in the
acne patients compared to the controls. It has been suggested that
ingesting milk may stimulate endogenous IGF-1, mediate some of the
effects of comedogenic factors and increase the production of
sebum. In addition, milk also contains androgens, 5-alpha reduced
steroids and other non-steroidal growth factors that affect the
pilosebaceous unit. But there were no statistically significant
differences of milk consumption between control and acne group in
our study.
The acne patients in this study showed a significant preference
for a high fat diet (nuts, chicken, pork and processed cheese)
(table 1). The association between
a high fat diet and acne is controversial [2-4, 9, 27, 28]. Further
evaluation of the effect of fatty diets on acne is required. In
addition, the acne patients ingested significantly more seaweed,
which is high in iodine. It is well established that iodine intake
can exacerbate acne [29]. Therefore, seaweed may aggravate acne.
But it needs further evaluation.
Studies on diet and acne have usually compared control and acne
patients. In our study, in addition to the comparison between
control and acne patient groups, we also compared the dietary
patterns of the subgroups AF (acne patients aggravated by food) and
NAF (acne patients not-aggravated by food). Although the dietary
patterns between the acne and control groups showed significant
differences, the dietary patterns between the AF and NAF subgroups
did not show significant differences for most of the food intake,
except for roast pork (P = .02), fried chicken (P < .02) and
nuts (P = .03). In fact, the list of foods which are significantly
different between AF and NAF should have been longer. Because
people eat many kinds of food at each meal, they may not accurately
identify the foods which aggravate acne.
In this study we showed differences in the dietary patterns of
acne patients and controls, and between AF and NAF groups. We
analyzed the whole type of food and amount of foods eaten, with a
specified questionnaire, by the methods of cooking, during a week.
But we have not proved the effect of individual food on acne. And
the classification of AF and NAF was entirely based on the
patients’ answers to the questionnaire. Therefore the results might
be changed slightly if we really performed an intervention study in
all acne patients. Further study is needed in the future.
In conclusion, the results of our study suggest that a high
glycemic load diet, processed cheese, a high fat diet, and iodine
play a role in the exacerbation of acne in Koreans. In addition,
irregular dietary habits may also aggravate acne.
Disclosure
Acknowledgments: the authors greatly appreciate the advice given by
Mi-Sun Park, RD who is in charge of Department of Clinical
Nutrition in Seoul National University Hospital. Financial support:
this study was supported by a grant of the Korea Healthcare
Technology R&D Project, Ministry for Health, Welfare &
Family Affairs, Republic of Korea (A090411). Conflict of interest:
none.
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