You are on page 1of 7

ORIGINAL ARTICLE

Association between Diet and Seborrheic


Dermatitis: A Cross-Sectional Study
Martijn G.H. Sanders1, Luba M. Pardo1, Rebecca S. Ginger2, Jessica C. Kiefte-de Jong3,4 and
Tamar Nijsten1

Current treatments for seborrheic dermatitis provide only temporary relief. Therefore, identifying modifiable
lifestyle factors may help reduce disease burden. The objective of this study was to determine whether specific
dietary patterns or total antioxidant capacity are associated with seborrheic dermatitis. Participants of the
Rotterdam Study with a skin examination and a food frequency questionnaire were included. Total antioxidant
capacity was assessed on the basis of ferric reducing antioxidant potential of each food item. Dietary patterns
were identified with principal component analysis (PCA). Multivariable logistic regression analyses were used
to assess the association between total antioxidant capacity, dietary pattern-derived PCA factors, and sebor-
rheic dermatitis adjusted for confounders. In total, 4,379 participants were included, of whom 636 (14.5%) had
seborrheic dermatitis. The PCA identified vegetable, Western, fat-rich and fruit dietary patterns. The fruit
pattern was associated with a 25% lower risk (quartile 1 vs. quartile 4: adjusted odds ratio ¼ 0.76, 95% confi-
dence interval ¼ 0.58e0.97, P ¼ 0.03), and the Western pattern with a 47% increased risk (quartile 1 vs. quartile 4:
adjusted odds ratio ¼ 1.47; 95% confidence interval ¼ 0.98e2.20, P ¼ 0.03), but only for females. Other factors
were not associated with seborrheic dermatitis. In conclusion, a high fruit intake was associated with less
seborrheic dermatitis, whereas high adherence to a “Western” dietary pattern in females was associated with
more seborrheic dermatitis.
Journal of Investigative Dermatology (2019) 139, 108e114; doi:10.1016/j.jid.2018.07.027

INTRODUCTION vegetables, may be beneficial for inflammatory skin diseases


Seborrheic dermatitis is a common chronic relapsing skin (Bickers and Athar, 2006; Carlsen et al., 2010). Other dietary
disease (Gupta and Bluhm, 2004). Although there is no components that might affect skin diseases include vitamin A
known cause for seborrheic dermatitis, evidence does sug- (i.e., involved in keratinization, immunomodulation, and the
gest that certain risk factors may predispose people to seb- regulation of sebaceous gland activity), omega-3 fatty acids
orrheic dermatitis. As well as a genetic predisposition, these (i.e., anti-inflammatory properties), and psoralen in citrus
factors include male sex, light skin color, winter season, and fruits (i.e., photocarcinogenic properties) (Beckenbach et al.,
high abundance of Malassezia yeasts on the skin (Sanders 2015; Dugrand et al., 2013; Millsop et al., 2014). The effect
et al., 2018a; Sanders et al., 2018b). Because treatment of a single dietary component on a disease is often too small
options for seborrheic dermatitis such as topical or oral to detect in individuals, and the single components are part of
antifungals and topical corticosteroids provide at most tem- an overall dietary pattern. Therefore, assessing dietary pat-
porary relief, it is essential to identify modifiable lifestyle terns and the overall antioxidant capacity may be more
factors that may reduce the burden of this condition. suitable for identifying potential nutritional risk factors for
Several studies suggested that nutrition may influence in- seborrheic dermatitis (Hu, 2002).
flammatory skin diseases such as acne vulgaris and, to a In a recent observational study in the Rotterdam Study (RS),
lesser extent, psoriasis (Kwon et al., 2012; Millsop et al., we showed that seborrheic dermatitis occurrence was asso-
2014). However, there are no studies investigating the ciated with male sex, light skin color, dry skin, and winter
effect of diet on seborrheic dermatitis. Numerous compo- season (Sanders et al., 2018a). In this cross-sectional study of
nents in our diet may affect skin health in vitro. For instance, a middle-aged and elderly population, we aimed to deter-
antioxidants, which are commonly found in fruits and mine whether the total dietary antioxidant intake or a specific
a posteriori defined dietary pattern is associated with sebor-
rheic dermatitis.
1
Department of Dermatology, Erasmus MC, Rotterdam, The Netherlands;
2
Unilever Research and Development, Colworth Science Park, Sharnbrook,
UK; 3Department of Epidemiology, Erasmus MC, Rotterdam, The RESULTS
Netherlands; and 4Leiden University College, The Hague, The Netherlands Study population
Correspondence: Tamar Nijsten, Burg. s’ Jacobplein 51, 3015 CA Rotterdam, In total, 5,498 participants underwent a full-body skin exam-
The Netherlands. E-mail: t.nijsten@erasmusmc.nl ination (FBSE), and 4,379 of them (RS-1: 801, RS-II: 1,441,
Abbreviations: FBSE, full body skin examination; FFQ, food frequency RS-III: 2,137) had complete nutrition data. Of the 4,379
questionnaire; FRAP, ferric-reducing ability of plasma; PCA, principal
component analysis; Q, quartile; RS, Rotterdam Study
eligible participants, 636 had seborrheic dermatitis lesions
found during the FBSE (point prevalence ¼ 14.5%). The
Received 14 March 2018; revised 11 July 2018; accepted 18 July 2018;
accepted manuscript published online 18 August 2018; corrected proof median age of all participants was 68.9 years (interquartile
published online 16 October 2018 range ¼ 62.6e77.4), and the proportion of woman was 57.6%.

108 Journal of Investigative Dermatology (2019), Volume 139 ª 2018 The Authors. Published by Elsevier, Inc. on behalf of the Society for Investigative Dermatology.
MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

The distribution of the demographic characteristics and The consumption of fruits might reduce the likelihood of
possible confounding factors between people with and having seborrheic dermatitis via consumption of a wide va-
without seborrheic dermatitis at time of FBSE are presented in riety of vitamins and other compounds (e.g., flavonoids,
Table 1. antioxidant) that have been shown to reduce inflammation in
several diseases (Cepeda et al., 2015; He et al., 2006). Also,
Total antioxidant capacity
fruits contain several nutrients that can serve as methyl do-
The median ferric-reducing ability of plasma (FRAP) score at
nors, which can prevent the expression of inflammatory
an intake of 2,000 kcal was 24.3 mmol/day (interquartile
genes (Perdigoto et al., 2014). Another possible hypothesis by
range ¼ 17.3e30.5). The crude and multivariable logistic
which fruits affect skin health involves psoralen. Psoralen is
regression between the FRAP score of the diet and seborrheic
highly present in citrus fruits and increases the sensitivity of
dermatitis is shown in Table 2. We did not find evidence for
the skin to UVR (Wu et al., 2015). This increased sensitivity to
an association between antioxidant intake and seborrheic
UVR could have a positive effect on seborrheic dermatitis
dermatitis (FRAP score, quartile 1 vs quartile 4: adjusted odds
because this dermatosis is less frequently present in summer
ratio ¼ 0.94; 95% confidence interval ¼ 0.73e1.19, P ¼
months (Pirkhammer et al., 2000; Sanders et al., 2018a).
0.88).
Western diets and diets high in meat and processed food
Dietary patterns consumption have often been associated with markers of
The principal component analysis (PCA) yielded four inde- inflammation (Giugliano et al., 2006; Ozawa et al., 2017).
pendent components of interest, explaining 26.2% of the Omega-6 fatty acids are one of the markers that can signifi-
total variation of the diet patterns. The first component was cantly change because of a diet and have been suggested to
characterized as a vegetables dietary pattern; the second as a induce chronic inflammation. However, intervention studies
Western pattern, characterized by meat, potato, and alcohol with omega-6 supplementation did not substantiate this (Innes
consumption; the third as a fruit pattern; and the fourth as a and Calder, 2018). The stratified analysis of our data showed
fat pattern, which most correlated with consuming olive oil that females with a high adherence to the Western pattern
and with other healthy and unhealthy fats (Table 3). seem to have higher odds of having seborrheic dermatitis.
Table 4 shows the effect of adherence to the diet patterns However, higher adherence to the Western pattern was not
on the risk of having seborrheic dermatitis. In the crude associated with seborrheic dermatitis in males. Previous di-
model, there seems to be a negative effect of the Western etary intervention studies showed that there are differences in
pattern, a positive effect of fruit consumption (borderline response to diet between males and females. For example, a
significant), and no effect of vegetable or fat consumption. In healthy diet improved insulin homeostasis in males but not in
the adjusted model, adherence to the Western pattern seems females; sex differences in body fat distribution might be one
to be associated with a higher risk for seborrheic dermatitis, explanation for this (Bedard et al., 2012). Also, it is known that
but this was significant only for the highest quartile (quartile 1 immune response in females differs from that in males and that
vs. quartile 4: adjusted odds ratio ¼ 1.34, 95% confidence females are more susceptible to autoimmune and inflamma-
interval ¼ 1.03e1.75, P ¼ 0.07). Adherence to the fruit tory diseases (Klein and Flanagan, 2016). This study underlines
pattern was associated with a lower risk for seborrheic the importance of possible interactions between sex and
dermatitis (quartile 1 vs. quartile 4: adjusted odds ratio ¼ nutrition, in which adding sex as a confounder in the final
0.75, 95% confidence interval ¼ 0.58e0.97, P ¼ 0.03), and model is not sufficient.
adherence to the other patterns did not influence seborrheic Because seborrheic dermatitis is a chronic inflammatory
dermatitis risk. disease, and because reactive oxygen species may promote
In the additional analysis, we tested for interaction be- chronic inflammation or aggravate inflammatory skin dis-
tween the dietary outcomes and all other variables. A sig- eases (Trouba et al., 2002), we expected individuals with a
nificant interaction was found between the Western dietary high total antioxidant intake to have a lower prevalence of
pattern and sex (P ¼ 0.013). Therefore, we decided to stratify skin disease. Moreover, two previous studies, one of the total
this dietary pattern. For males, there was no significant as- antioxidant level in serum and one of the antioxidant levels of
sociation between the Western pattern and seborrheic scalp scrapes, suggested that oxidative stress might be higher
dermatitis. However, for females, a higher adherence to this in seborrheic dermatitis patients (Emre et al., 2012; Ozturk
pattern was associated with an increased risk of seborrheic et al., 2013). In contrast to these studies and the hypothe-
dermatitis (Table 5). sis, participants with a higher overall dietary antioxidant ca-
pacity did not have a decreased odds of having seborrheic
DISCUSSION dermatitis. This observation suggests that the effect of oral
In the study, we found that participants with a dietary pattern antioxidants in the treatment of seborrheic dermatitis might
characterized by high fruit intake had lower odds of having be limited. However, it has been questioned if methods
seborrheic dermatitis after adjustment for confounders. assessing the overall antioxidant capacity should be used to
Furthermore, we found that a Western dietary pattern was make claims concerning the antioxidant defense system
associated with higher odds of having seborrheic dermatitis, (Turck et al., 2018). In addition, we also did not find a
but only for females. We did not find an association between consistent association between dietary antioxidant capacity
the presence of seborrheic dermatitis and dietary patterns and inflammatory markers in The RS (Stringa et al., 2017).
characterized by vegetables or fat, nor did we find an asso- Therefore, other biomarkers of antioxidant capacity or
ciation between seborrheic dermatitis and total dietary anti- oxidative stress may provide additional insights in the role of
oxidant capacity. antioxidants in seborrheic dermatitis.

www.jidonline.org 109
MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

Table 1. Characteristics of participants by having or not having seborrheic dermatitis1


Characteristic SD No SD P-value

Participants, n (%) 636 (14.5) 3,743 (85.5) —


Male sex, n (%) 378 (59.4) 1,477 (39.5) <0.01
Age in years, median (IQR) 69.9 (63.9e77.5) 68.8 (62.4e77.4) 0.14
BMI in kg/m2, n (%) 0.23
<25 179 (28.1) 1,176 (31.4)
25e30 310 (48.7) 1,714 (45.8)
>30 147 (23.1) 845 (22.6)
Missing 0 (0.0) 8 (0.2)
Skin color, n (%) <0.01
Very whiteewhite 567 (89.2) 3,103 (82.9)
Whiteeolive 61 (9.6) 524 (14.0)
Light browneblack 8 (1.3) 116 (3.3)
Education, n (%) 0.45
Low 54 (8.5) 357 (9.5)
Average 378 (59.4) 2,267 (60.6)
High 195 (30.7) 1,068 (28.5)
Missing 9 (1.4) 51 (1.4)
Xerosis cutis, n (%) 0.07
No 214 (33.6) 1,421 (38.0)
Extensor-side extremities 325 (51.1) 1,850 (49.4)
Generalized 93 (14.6) 440 (11.8)
Other 4 (0.6) 31 (0.8)
Missing 0 (0.0) 1 (0.03)
Physical activity in METhours/week, median (IQR) 40.1 (15.0e75.8) 43.0 (17.5e81.6) 0.04
Missing, n (%) 24 (3.8) 191 (5.1)
Season, n (%) <0.01
Winter 187 (29.4) 861 (23.0)
Spring 137 (21.5) 800 (21.4)
Summer 77 (12.1) 605 (16.2)
Autumn 235 (36.9) 1,477 (39.5)
Current smoker, n (%) 546 (85.8) 3,262 (87.1) 0.37
Alcohol in glasses/week, median (IQR) 8.3 (1.4e21.0) 6.8 (0.9e17.3) 0.04
Energy intake in kcal/day, median (IQR) 2,118.1 (1,721.3e2,626.2) 2,077.2 (1,670.9e2,542.3) 0.07
Weekly use of supplements, n (%) 296 (46.5) 1,686 (45.0) 0.48
Abbreviations: IQR, interquartile range; MET, metabolic equivalent; SD, seborrheic dermatitis.
1
The chi-square test was used for categorical variables and the t test for continuous variables.

In this study we investigated the role of diet in seborrheic measurement errors and to limit the influence of outliers, we
dermatitis. The strengths of our study are the large sample adjusted our analyses for total energy intake and categorized
size, the population-based setting, the physician-based the dietary data into quartiles. Although self-reported dietary
diagnosis, and the availability of different epidemiological intake is subject to measurements error when it concerns
factors that allowed us to control for potential confounders. absolute intake, it has been shown that the FFQ is able to
There are several limitations to the study. The cross-sectional adequately rank the intake of individuals according to their
design does not allow us to make causal inferences, and food group (Goldbohm et al., 1994). To account for potential
because this study covers a middle-aged and elderly popu- confounding by food supplementation, we adjusted the an-
lation, the generalizability to younger patients might be alyses for any dietary supplement use. For RS-I and RS-II, the
limited. Unfortunately, the disease severity and distribution of FFQ was conducted in the same period as the FBSE. For RS-
seborrheic dermatitis was not specifically documented during III, the FFQ data were registered 5 years earlier than the FBSE.
the FBSE. Therefore, we cannot elaborate further on the However, we previously showed that dietary patterns are
relationship between location or severity of the disease and relatively stable in this population (in the same quartile of
the associations with the diet components. Also, because we intake), in particular for components such as vegetables
did not investigate individual dietary components, this study (73%), fruits (93%), dietary fiber (91%), saturated fat (92%)
cannot be used to select possible supplements that might and alcohol (79%) (Schoufour et al., 2018). There might al-
reduce seborrheic dermatitis risk. Furthermore, the use of a ways be residual confounding of variables that were not
food frequency questionnaire (FFQ) to assess dietary intake is documented in this cohort. Self-reported stress, for example,
prone to measurement error. To account for systematic could be such a variable that might have influenced both

110 Journal of Investigative Dermatology (2019), Volume 139


MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

Table 2. Multivariable logistic regression between the total antioxidant capacity of the diet and the risk of having
seborrheic dermatitis
FRAP Crude OR1 95% CI Lower 95% CI Upper P-Value Adjusted OR2 95% CI Lower 95% CI Upper P-Value

Q1 (ref)
Q2 0.81 0.63 1.03 0.09 0.80 0.63 1.03 0.08
Q3 1.08 0.86 1.37 0.51 1.04 0.82 1.32 0.75
Q4 0.96 0.75 1.22 0.74 0.93 0.73 1.19 0.57
P for trend 0.68 0.91
Abbreviations: CI, confidence interval; FRAP, ferric-reducing ability of plasma; OR, odds ratio; Q, quartile.
1
Crude OR: odds ratio adjusted for age and sex.
2
Adjusted OR: odds ratio adjusted for age, sex, total energy intake, skin color, smoking, alcohol, body mass index, season, physical activity education, and
supplement use.

dietary choices and disease risk (Misery et al., 2007). How- NTR6831. All participants provided written informed consent to
ever, we previously showed that measurements of anxiety participate in the study and to have their information obtained from
and depression (proxies of stress) were not associated with treating physicians. The study started in 1990 and now comprises
seborrheic dermatitis in this cohort (Sanders et al., 2018a). three cohorts (RS-1, RS-II, and RS-III) with a total of 14,926
Also, including these variables in the multivariable logistic
regression of this study did not influence the associations
between the dietary patterns and seborrheic dermatitis (data Table 3. Principal component analysis of 34 food
not shown). groups1
In conclusion, a high intake of fruit was associated with Food Group Vegetables Western Fruit Fat
lower odds of seborrheic dermatitis, and a high adherence to
the Western dietary pattern seems to be associated with a Greenleaf vegetables 0.846 0.039 0.040 0.047
higher risk of seborrheic dermatitis in females. These findings Vegetables, other 0.825 0.110 0.013 0.030
were not driven by the overall dietary antioxidant capacity. Yellow leaf vegetables 0.760 e0.086 0.152 0.000
Meat unprocessed 0.048 0.727 0.006 0.021
Although the results of this study cannot be used to provide
Meat processed e0.045 0.670 e0.042 0.070
exact recommendations, it seems advisable for seborrheic
Potatoes 0.164 0.478 0.012 0.096
dermatitis patients to follow national diet guidelines
Alcoholic drinks (not wine) e0.062 0.366 e0.067 0.040
regarding fruit, which recommends at least 200 g/day of fruit
Citrus fruits 0.050 e0.013 0.903 0.002
in The Netherlands (Brink et al., 2016). Furthermore, Fruits (non-citrus) 0.134 e0.021 0.883 e0.011
although a high adherence to the Western dietary pattern Olive oil 0.111 e0.099 0.075 0.758
was associated with an increased disease risk only for fe- Unhealthy fats e0.061 0.086 e0.079 0.692
males, it might be beneficial for both sexes to reduce meat Healthy fats e0.013 0.144 e0.009 0.596
consumption, considering recent literature linking meat Soups and sauces 0.135 0.273 0.028 0.330
intake with an increased risk of mortality (Etemadi et al., Sweets e0.065 0.056 0.123 0.112
2017). Dietary pattern studies seem appropriate, because Savory snacks 0.018 0.152 e0.117 0.027
initial dietary association study and might be meaningful in Refined grains 0.143 0.113 e0.163 0.105
other skin diseases as well. Replication of our findings in an Nuts and seeds 0.110 e0.061 0.063 0.013
independent cohort, or conducting an interventional study, Fatty fish 0.145 e0.005 0.039 0.010
would be necessary to substantiate these claims. A pro- Lean fish 0.113 e0.008 0.007 0.029
spective study measuring relapse rate in seborrheic derma- Shellfish e0.012 0.142 0.029 e0.010
titis patients with a high or low fruit intake would be of high Whole grains 0.075 0.032 e0.084 0.222
value. Yogurt 0.110 e0.044 0.175 e0.192
Mineral water 0.088 e0.006 0.060 e0.006
Poultry 0.197 0.185 0.025 e0.029
METHODS Black tea 0.021 0.123 0.079 e0.017
Study design Coffee 0.087 0.148 e0.007 e0.045
The RS is an ongoing prospective population-based cohort study of Soy 0.127 e0.113 0.033 e0.004
chronic diseases in a middle aged and elderly population in the Pulses 0.028 0.178 e0.037 e0.054
Ommoord district of Rotterdam, The Netherlands (Ikram et al., Herb tea 0.140 e0.161 0.110 0.042
2017). The Rotterdam Study has been approved by the Medical Wine 0.073 e0.022 e0.027 e0.026
Cheese 0.051 0.160 0.070 0.023
Ethics Committee of the Erasmus MC (registration number MEC
Soft drinks e0.030 0.130 e0.031 e0.081
02.1015) and by the Dutch Ministry of Health, Welfare and Sport
Milk 0.063 e0.080 0.088 0.010
(Population Screening Act WBO, license number 1071272-159521-
Eggs e0.066 0.295 e0.018 0.076
PG). The RS has been entered into the Netherlands National Trial 1
Extraction method: principal component analysis. Rotation method:
Register (NTR; www.trialregister.nl) and into the World Health Or-
varimax with Kaiser normalization. Factor loadings with a low predictive
ganization International Clinical Trials Registry Platform (www.who. value (e0.2  x  0.2) are presented in regular type. Factor loadings with
int/ictrp/network/primary/en/) under shared catalog number a high predictive value (>0.35) are presented in boldface type.

www.jidonline.org 111
MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

Table 4. Multivariable logistic regression between adherence to the dietary patterns and the risk of having
seborrheic dermatitis
Pattern Crude OR1 95% CI Lower 95% CI Upper P-Value2 Adjusted OR3 95% CI Lower 95% CI Upper P-Value2

Vegetables
Q1 (ref)
Q2 1.04 0.82 1.33 0.75 1.028 0.81 1.31 0.82
Q3 1.13 0.89 1.44 0.31 1.134 0.89 1.45 0.31
Q4 1.12 0.87 1.43 0.37 1.122 0.87 1.45 0.38
P for trend 0.28 0.28
Western
Q1 (ref)
Q2 1.29 1.00 1.66 0.05 1.27 1.11 1.44 0.07
Q3 1.19 0.92 1.54 0.18 1.16 0.89 1.50 0.27
Q4 1.35 1.05 1.73 0.02 1.34 1.03 1.75 0.03
P for trend 0.05 0.07
Fruit
Q1 (ref)
Q2 0.87 0.69 1.09 0.22 0.83 0.74 0.93 0.12
Q3 0.80 0.63 1.02 0.07 0.77 0.60 0.99 0.04
Q4 0.80 0.63 1.03 0.08 0.75 0.58 0.97 0.03
P for trend 0.06 0.03
Fat
Q1 (ref)
Q2 1.26 0.99 1.61 0.06 1.28 1.00 1.63 0.05
Q3 0.96 0.75 1.24 0.76 0.98 0.77 1.24 0.85
Q4 1.20 0.94 1.53 0.14 1.22 .945 1.58 0.14
P for trend 0.47 0.47
Abbreviations: CI, confidence interval; OR, odds ratio; Q, quartile; ref, reference.
1
Crude OR: odds ratio adjusted for age and sex.
2
Boldface indicates P-values < 0.05.
3
Adjusted OR: odds ratio adjusted for age, sex, skin color, smoking, body mass index, season, total energy intake, physical activity, education, and sup-
plement use.

participants aged 45 years or older. Dermatological examinations rich in sebaceous glands. Participants without seborrheic dermatitis
were introduced in 2010, and since then, 5,498 participants have were considered as controls.
had a skin examination. The current study is a cross-sectional study
containing all participants with a skin examination and available Nutritional data
nutrition data. Dietary intake was assessed by means of an FFQ, which included
389 questions regarding the consumption of food over the last
Case definition month. The Dutch Food Composition Table of 2006 and 2011 was
Seborrheic dermatitis was diagnosed by a dermatology-trained then used to transform the data into daily macronutrient intake and
physician during a scheduled FBSE. The diagnoses were based on total energy intake (kcal/day) (Dutch Food Composition Table,
greasy scaling, erythema, and a characteristic distribution in areas 2011). This FFQ was based on a validated FFQ for Dutch adults

Table 5. Multivariable logistic regression between the Western dietary pattern and seborrheic dermatitis, stratified
for sex1
Male Female
2 2
Quartile OR 95% CI Lower 95% CI Upper P-Value OR 95% CI Lower 95% CI Upper P-Value3

Q1 (ref)
Q2 1.19 0.99 1.44 0.35 1.26 0.88 1.81 0.21
Q3 0.87 0.60 1.27 0.47 1.50 1.04 2.18 0.03
Q4 1.18 0.83 1.67 0.37 1.47 0.98 2.20 0.06
P for trend 0.67 0.03
Abbreviations: CI, confidence interval; OR, odds ratio; Q, quartile; ref, reference.
1
This stratified multivariable logistic regression was conducted because of the significant interaction between the Western dietary pattern and sex
(P ¼ 0.013).
2
Odds ratio adjusted for age, sex, skin color, smoking, body mass index, season, total energy intake, physical activity, education and supplement use.
3
Boldface indicates P-values < 0.05.

112 Journal of Investigative Dermatology (2019), Volume 139


MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

(Feunekes et al., 1993; Goldbohm et al., 1994). This FFQ was vali- The threshold for significance was set at a P-value of 0.05. All
dated against 3-day food records, 4e5 months apart, and showed an analyses were conducted in IBM SPSS Statistics for Windows,
energy- and sex-adjusted correlation for macronutrients between version 21.0 (IBM, Armonk, NY).
0.47 (fat) to 0.79 (polysaccharides).
CONFLICT OF INTEREST
RG is an employee of Unilever with a shareholding in this company. TN
Total antioxidant capacity received research grants from Unilever. The other authors state no conflict of
The total antioxidant capacity was calculated as described earlier interest.
(Pantavos et al., 2015). In short, an Antioxidant Food Table (Carlsen
et al., 2010) was used to assess the antioxidant capacity of each ACKNOWLEDGMENTS
dietary item. This Antioxidant Food Table contains the antioxidant The Rotterdam Study is funded by Erasmus Medical Center and Erasmus
capacity of food items determined assessed on the basis of an University Rotterdam; Netherlands Organization for the Health Research and
Development (ZonMw); the Research Institute for Diseases in the Elderly
existing table that evaluated the FRAP for more than 3,000 food
(RIDE); the Ministry of Education, Culture and Science; the Ministry for
items (Carlsen et al., 2010). For every participant, the consumption Health, Welfare and Sports; the European Commission (DG XII); and the
frequency of each dietary item was multiplied by the FRAP value in Municipality of Rotterdam. MGHS is supported by Unilever, and RG is a
this table. The total antioxidant capacity was then adjusted for the Unilever employee.
total energy intake using the residual method and categorized into
quartiles (Willett et al., 1997). REFERENCES
Beckenbach L, Baron JM, Merk HF, Loffler H, Amann PM. Retinoid treatment
Dietary patterns of skin diseases. Eur J Dermatol 2015;25:384e91.
To define dietary patterns, we used the a posteriori dietary pattern Bedard A, Riverin M, Dodin S, Corneau L, Lemieux S. Sex differences in the
analysis described by Hu et al. (1999). The list of 389 food items impact of the Mediterranean diet on cardiovascular risk profile. Br J Nutr
from the FFQ was categorized into 34 main food groups. The groups 2012;108:1428e34.

were categorized on the basis of the Nevo table (Dutch Food Bickers DR, Athar M. Oxidative stress in the pathogenesis of skin disease.
J Invest Dermatol 2006;126:2565e75.
Composition Table, 2011), while accounting for effects of specific
Brink L, Smeets AP-, Stafleu A, Wolvers D. The Netherlands Nutrition Centre.
subgroups (e.g., vegetables were split up because of the high vitamin Richtlijnen Schijf van Vijf. http://www.voedingscentrum.nl/professionals/
A content in green leafy vegetables, and fruits were split up because schijf-van-vijf/naslag-richtlijnen-schijf-van-vijf.aspx. 2016. Accessed 4
of the high vitamin C content in citrus fruits). These food groups were October 2018.
then analyzed with a PCA to identify dietary patterns that explained Carlsen MH, Halvorsen BL, Holte K, Bohn SK, Dragland S, Sampson L, et al.
the maximum variation of food intake. To minimize correlation The total antioxidant content of more than 3100 foods, beverages, spices,
herbs and supplements used worldwide. Nutr J 2010;9:3.
between the dietary patterns, a Varimax rotation was used. In
Cepeda AM, Del Giacco SR, Villalba S, Tapias E, Jaller R, Segura AM, et al.
determining the number of dietary patterns (factors) that should A traditional diet is associated with a reduced risk of eczema and wheeze
remain; we interpreted the scree test for factors with an Eigenvalue of in Colombian children. Nutrients 2015;7:5098e110.
1.0 or greater. The factors were then used to rank participants in low Dugrand A, Olry A, Duval T, Hehn A, Froelicher Y, Bourgaud F. Coumarin and
to high adherence for each of the dietary patterns. These ranks were furanocoumarin quantitation in citrus peel via ultraperformance liquid
used to create quartiles, which explain how good a participant fits in chromatography coupled with mass spectrometry (UPLC-MS). J Agric Food
Chem 2013;61:10677e84.
a specific pattern.
Dutch Food Composition Table. Nevo tabel 2006/2011. Voorlichtingsbureau
voor de Voeding. The Hague, The Netherlands, 2011. https://www.rivm.nl/
Covariates en/Topics/D/Dutch_Food_Composition_Database/Publications. Accessed
Age, sex, skin color (Jacobs et al., 2015), height, weight, and season 4 October 2018.
were documented during the visit to the research center. During the Emre S, Metin A, Demirseren DD, Akoglu G, Oztekin A, Neselioglu S, et al.
home interview, participants were asked about their education level The association of oxidative stress and disease activity in seborrheic
dermatitis. Arch Dermatol Res 2012;304:683e7.
(low ¼ primary education, medium ¼ lowereintermediate voca-
Etemadi A, Sinha R, Ward MH, Graubard BI, Inoue-Choi M, Dawsey SM,
tional education, high ¼ general secondary education and higher) et al. Mortality from different causes associated with meat, heme iron,
and tobacco use (never and former vs. current). Physical activity was nitrates, and nitrites in the NIH-AARP Diet and Health Study: population
assessed using the Longitudinal Aging Study Amsterdam Physical based cohort study. BMJ 2017;357:j1957.
Activity Questionnaire and expressed in metabolic equivalent hours/ Feunekes GI, Van Staveren WA, De Vries JH, Burema J, Hautvast JG. Relative
week (Stel et al., 2004). Participants were categorized as supplement and biomarker-based validity of a food-frequency questionnaire estimating
intake of fats and cholesterol. Am J Clin Nutr 1993;58:489e96.
users if they used supplements at least once a week.
Giugliano D, Ceriello A, Esposito K. The effects of diet on inflammation:
emphasis on the metabolic syndrome. J Am Coll Cardiol 2006;48:677e85.
Statistical analyses Goldbohm RA, van den Brandt PA, Brants HA, van ’t Veer P, Al M, Sturmans F,
Missing data on the covariates were imputed using the fully condi- et al. Validation of a dietary questionnaire used in a large-scale prospective
tional specification imputation method with 20 imputations (Sterne cohort study on diet and cancer. Eur J Clin Nutr 1994;48:253e65.
et al., 2009). Multivariable logistic regression was used to calcu- Gupta AK, Bluhm R. Seborrheic dermatitis. J Eur Acad Dermatol 2004;18:
late the strength of the association between total antioxidant ca- 13e26.
pacity and seborrheic dermatitis and the PCA-extracted dietary He FJ, Nowson CA, MacGregor GA. Fruit and vegetable consumption and
stroke: meta-analysis of cohort studies. Lancet 2006;367(9507):320e6.
patterns and seborrheic dermatitis, both adjusted for age, sex, skin
Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology.
color, smoking, total energy intake, body mass index, season,
Curr Opin Lipidol 2002;13:3e9.
physical activity, education, and supplement use. In addition, we
Hu FB, Rimm E, Smith-Warner SA, Feskanich D, Stampfer MJ, Ascherio A,
tested for interaction between the dietary outcomes and all other et al. Reproducibility and validity of dietary patterns assessed with a food-
variables. frequency questionnaire. Am J Clin Nutr 1999;69:243e9.

www.jidonline.org 113
MGH Sanders et al.
Association between Diet and Seborrheic Dermatitis

Ikram MA, Brusselle GGO, Murad SD, van Duijn CM, Franco OH, Sanders MGH, Pardo LM, Franco OH, Ginger RS, Nijsten T. Prevalence
Goedegebure A, et al. The Rotterdam Study: 2018 update on objectives, and determinants of seborrhoeic dermatitis in a middle-aged and
design and main results. Eur J Epidemiol 2017;32:807e50. elderly population: the Rotterdam Study. Br J Dermatol 2018a;178:
Innes JK, Calder PC. Omega-6 fatty acids and inflammation. Prostaglandins 148e53.
Leukot Essent Fatty Acids 2018;132:41e8. Sanders MGH, Pardo LM, Uitterlinden AG, Smith AM, Ginger RS,
Nijsten T. The genetics of seborrheic dermatitis: a candidate gene
Jacobs LC, Hamer MA, Verkouteren JA, Pardo LM, Liu F, Nijsten T. Perceived
approach and pilot genome-wide association study. J Invest Dermatol
skin colour seems a swift, valid and reliable measurement. Br J Dermatol
2018b;138:991e3.
2015;173:1084e6.
Schoufour JD, de Jonge EAL, Kiefte-de Jong JC, van Lenthe FJ, Hofman A,
Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev
Nunn SPT, Franco OH. Socio-economic indicators and dietary quality in an
Immunol 2016;16:626e38.
elderly population. Maturitas 2018;107:71e7.
Kwon HH, Yoon JY, Hong JS, Jung J, Park MS, Suh DH. Clinical and histological
Stel VS, Smit JH, Pluijm SM, Visser M, Deeg DJ, Lips P. Comparison of the
effect of a low glycaemic load diet in treatment of acne vulgaris in Korean
LASA Physical Activity Questionnaire with a 7-day diary and pedometer.
patients: a randomized, controlled trial. Acta Derm Venereol 2012;92:241e6.
J Clin Epidemiol 2004;57:252e8.
Millsop JW, Bhatia BK, Debbaneh M, Koo J, Liao W. Diet and psoriasis, part
Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al.
III: role of nutritional supplements. J Am Acad Dermatol 2014;71:561e9.
Multiple imputation for missing data in epidemiological and clinical
Misery L, Touboul S, Vincot C, Dutray S, Rolland-Jacob G, Consoli SG, et al. research: potential and pitfalls. BMJ 2009;338:b2393.
Stress et dermatite séborrhéique [Stress and seborrheic dermatitis]. Ann
Stringa N, Brahimaj A, Zaciragic A, Dehghan A, Ikram MA, Hofman A, et al.
Dermatol Venereol 2007;134:833e7.
Relation of antioxidant capacity of diet and markers of oxidative status with
Ozawa M, Shipley M, Kivimaki M, Singh-Manoux A, Brunner EJ. Dietary C-reactive protein and adipocytokines: a prospective study. Metabolism
pattern, inflammation and cognitive decline: the Whitehall II prospective 2017;71:171e81.
cohort study. Clin Nutr 2017;36:506e12.
Trouba KJ, Hamadeh HK, Amin RP, Germolec DR. Oxidative stress and its
Ozturk P, Arican O, Belge Kurutas E, Karakas T, Kabakci B. Oxidative stress in role in skin disease. Antioxid Redox Signal 2002;4:665e73.
patients with scalp seborrheic dermatitis. Acta Dermatovenerol Croat
Turck D, Bresson JL, Burlingame B, Dean T, Fairweather-Tait S, Heinonen M,
2013;21:80e5.
et al. Guidance for the scientific requirements for health claims related to
Pantavos A, Ruiter R, Feskens EF, de Keyser CE, Hofman A, Stricker BH, et al. antioxidants, oxidative damage and cardiovascular health. EFSA J 2018;16:
Total dietary antioxidant capacity, individual antioxidant intake and breast 5136.
cancer risk: the Rotterdam Study. Int J Cancer 2015;136:2178e86. Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake
Perdigoto CN, Valdes VJ, Bardot ES, Ezhkova E. Epigenetic regulation of epidermal in epidemiologic studies. Am J Clin Nutr 1997;65(Suppl. 4):
differentiation. Cold Spring Harb Perspect Med 2014;4:a015263. 1220Se8S.
Pirkhammer D, Seeber A, Honigsmann H, Tanew A. Narrow-band ultraviolet Wu S, Han J, Feskanich D, Cho E, Stampfer MJ, Willett WC, et al. Citrus
B (ATL-01) phototherapy is an effective and safe treatment option for pa- consumption and risk of cutaneous malignant melanoma. J Clin Oncol
tients with severe seborrhoeic dermatitis. Br J Dermatol 2000;143:964e8. 2015;33:2500e8.

114 Journal of Investigative Dermatology (2019), Volume 139

You might also like