Diet and Microbiome Influence on Alopecia Areata: Experience from Case Reports

Abstract

Alopecia areata (AA) is a potentially reversible auto-immune
non-scarring baldness on the scalp, which can be extended
to the entire body. There are many scientific evidence as
regards the impact of diet on scalp diseases related to hair
growth. Diet is also able to strongly influence gut microbiome. On the contrary, few evidence reports as regards the
link between microbiome, especially scalp microbiome and
hair diseases. Here we reported a two case-reports study
on patients affected by AA, with and without lactose intolerance, respectively, with the aim to underline how diet could
emphasize microbiome changing related to scalp disease.
Subjects were asked to fill out a 7-day dietary survey and
scalp and oral swabs were collected. Data from the dietary
survey, qRT-PCR on main bacterial strains inhabiting the
scalp and 16S sequencing of the scalp and oral microbiome
were matched and compared each other and with healthy
and general AA population. Beyond diet well-known impact
on general human health, our results highlighted the role of
diet in modifying oral and scalp microbiome, which in turn
seems to have an impact on AA evolution. The findings of
the present works suggested a kind of intercorrelation between microbial dysbiosis on the scalp of patients with AA
and dietary habits.

Full text

Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
Volume 5 | Issue 1
DOI: 10.23937/2572-3278.1510037
ISSN: 2572-3278
Open Access
Journal of
Nutritional Medicine and Diet Care
Citaon: Rinaldi F, Pinto D, Giuliani G, Sorbellini E (2019) Diet and Microbiome Inuence on Alopecia
Areata: Experience from Case Reports. J Nutri Med Diet Care 5:037. doi.org/10.23937/2572-
3278.1510037
Accepted: July 20, 2019: Published: July 22, 2019
Copyright: © 2019 Rinaldi F, et al. This is an open-access arcle distributed under the terms of the
Creave Commons Aribuon License, which permits unrestricted use, distribuon, and reproducon
in any medium, provided the original author and source are credited.
• Page 1 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
Diet and Microbiome Inuence on Alopecia Areata: Experience
from Case Reports
Fabio Rinaldi, MD1,2,3*, Daniela Pinto1,2,3, Giammaria Giuliani1,22,3
1Giuliani S.p.A., Italy
2Human Advanced Microbiome Project-HMAP, Italy
3Internaonal Hair Research Foundaon (IHRF), Italy
*Corresponding author: Rinaldi Fabio, MD, Internaonal Hair Research Foundaon (IHRF), Milan, Italy, Tel: +39-2-
76006089
Abstract
Alopecia areata (AA) is a potentially reversible auto-immune
non-scarring baldness on the scalp, which can be extended
to the entire body. There are many scientic evidence as
regards the impact of diet on scalp diseases related to hair
growth. Diet is also able to strongly inuence gut microbi-
ome. On the contrary, few evidence reports as regards the
link between microbiome, especially scalp microbiome and
hair diseases. Here we reported a two case-reports study
on patients affected by AA, with and without lactose intoler-
ance, respectively, with the aim to underline how diet could
emphasize microbiome changing related to scalp disease.
Subjects were asked to ll out a 7-day dietary survey and
scalp and oral swabs were collected. Data from the dietary
survey, qRT-PCR on main bacterial strains inhabiting the
scalp and 16S sequencing of the scalp and oral microbiome
were matched and compared each other and with healthy
and general AA population. Beyond diet well-known impact
on general human health, our results highlighted the role of
diet in modifying oral and scalp microbiome, which in turn
seems to have an impact on AA evolution. The ndings of
the present works suggested a kind of intercorrelation be-
tween microbial dysbiosis on the scalp of patients with AA
and dietary habits.
Keywords
Alopecia areata, Hair disorders, Dietary therapy, Microbi-
ome, Dysbiosis

Check for
updates
nutrient’s intake. Even though the role of macro and
micronutrients in normal hair follicle development has
not been completely claried [2], the impact of diet and
nutrional deciencies on hair growth diseases is well
documented [3,4].
Diet is also reported to have ability of shaping the gut
microbiome [5,6] but also skin microbiome in relaons
to some dermatological condions [7,8] especially acne
and psoriasis. Poor knowledge is currently available as
regards dermatological condions aecng the scalp
and hair growth.
Among hair growth disorders, Alopecia areata (AA)
is reported as the second most common disorder
aecng the scalp [9]. AA is a type of non-scarring
baldness aecng the scalp and, eventually the enre
body [10] which causes have been strictly associated
with immunity and inammaon [9,11,12].
In the past two years researchers focused their at-
tenon also on the role of microbial community inhab-
ing the scalp and hair growth disorders, including AA
[13-17]. More recently Nair and collaborator reported
evidence as regards the role for the gut microbiome
in the pathogenesis of AA [18]. Taking together these
ndings pose the need of a more deeply invesgaon
as regards the link between diet, microbiome and hair
growth disorders.
In the present work, we reported a two case-reports
study on paents aected by Alopecia areata, with and
Introducon
Hair follicle is a dynamic mini-organ [1] with an high
cellular turnover. As a consequence, hair follicle is char-
acterized by a very acve metabolism requiring a good

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• Page 2 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
me of inclusion. The clinical evaluaon reported 100%
hair loss of the scalp based on the Severity of Alopecia
Tool (SALT) Score [19] with no signs of erythema or
scaling. Eyebrows, eyelashes, and body hair were also
completely absent. The paent demographics include
being Caucasian, weight 72 kg, height 1.80 m, and BMI
22.2 kg/m2.
Case report 2
A 36-year-old female (Figure 3) came to the clinic
reporng a history of strong hair loss since one month.
Other reported symptoms are severe itching, psoriasis
on the scalp, birch and pauliary allergy, insomnia and
high sensaon of fague. The paent is also intolerant
without lactose intolerance, respecvely, with the aim
to underline how diet could emphasize microbiome
changing related to scalp disease (Figure 1).
Case Presentaon
Case report 1
A 17-year-old male (Milan, Italy), aected by Alopecia
universalis (Figure 2). The paent presented to the
dermatology clinic with a history of rapidly progressing
total body hair loss. There was no history of similar
illness in family members and also no history of drug
intake and trauma. Previously treatment includes stem
cell therapy. No therapy for at least 3 months at the
Figure 1: Diet importance in microbiome changing related to scalp disease.
Figure 2: Alopecia universalis affected male.

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• Page 3 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
to lactose. Clinical evaluaon showed strong hair loss
but no signal of miniaturizaon. Alopecia areata was
conrmed by histological examinaon. No therapy for
at least 3 months at the me of inclusion. The paent
demographics include being Caucasian, weight 48 kg,
height 1.62 m, and BMI 18.3 kg/m2.
Nutrient intake
Both subjects were asked to ll out a 7-day dietary
survey at the me of enrollment, following being
instructed by a diecian on how to record the food and
beverages consumed. The Winfood soware (Winfood
2.7 Medimaca Srl, Colonnella, Italy) was used for
analysis of surveys by esmang the energy intake and
the percentage of macronutrients and micronutrients.
Data collected were compared to the tables of food
consumpon and recommended dietary intakes of
the Italian Naonal Instute of Nutrion and Food
Composion Database in Italy.
Samples collecon
Before sampling paents had to avoid the use of
anbiocs in the last 30 days no probiocs, the use
of probiocs in the last 15 days, to perform the last
shampoo 48 h before sampling. They also did not have
to undergo to an-tumor, immunosuppressant or
radiaon therapy in the last 3 months and also topical
or hormonal therapy on the scalp. The study was under
the approval of the Ethical Independent Commiee for
Clinical, not pharmacological invesgaon in Genoa
(Italy) and in accordance with the ethical standards of
the 1964 Declaraon of Helsinki. All of the volunteers
signed the informed consent.
Microbiome samples were collected from the scalp
(minimum area sampled of 16 cm2) and oral mucosa with
a sterile coon swab, previously soaked in ST soluon
(NaCl 0.15 M and 0.1% Tween 20) for at least 30s
[20,21]. Samples from the same subjects were collected
together and stored at 4°C unl DNA extracon. Sterile
coon swabs placed in ST soluon have been used as
negave controls.
DNA extracon and 16s amplicon generaon and
sequencing: Genomic DNA from scalp swabs was ex-
tracted by mean of QIAamp UCP Pathogen Mini Kit
(Qiagen) according to manufacturer protocol, with mi-
nor modicaons [22]. Aer extracon, bacterial DNA
was suspended in DNAse free water and quaned by
the QIAexpert system (Qiagen) before sequencing and
qRT-PCR.
For sequencing, variable region V3-V4 was ampli-
ed by mean of the following universal primers: 341 F
CTGNCAGCMGCCGCGGTAA [23,24] and 806bR GGAC-
TACNVGGGTWTCTAAT [25-27]. Library preparaon and
Illumina MiSeq V3-V4 sequencing were carried out at
StarSEQ GmbH, Mainz, Germany, according to Capora-
so, et al. [28] and Kozich, et al. [29] methods, with mi-
nor modicaons. Real-Time Analysis soware (RTA) v.
1.16.18 and 1.17.22, MiSeq Control Soware (MCS) v.
2.0.5 and 2.1.13 were using.
qRT-PCR of main bacterial species: Main bacterial
species (Propionibacterium acnes, Staphylococcus epi-
dermidis and Staphylococcus aureus) on the scalp were
quaned by real-me quantave PCR (RT qPCR),
using Microbial PCR assay kit (Qiagen). Samples were
mixed with 12.5 μL of Microbial qPCR Mastermix, 1 μL
of Microbial DNA qPCR Assay, 5 ng of genomic DNA
sample and Microbial-DNA-free water up to a nal
volume of 25 μL. Posive PCR Control, No Template
Control, and Microbial DNA Posive Control were also
included. Pan-bacteria assays are also included as pos-
ive controls for the presence of bacterial DNA, as hu-
man GAPDH and HBB1 for the determinaon of proper
sample collecon. Following thermal cycling condions
were used: 95 °C for 10 min, 40 cycles of 95 °С for 15
sec, 60 °C for 2 min. Each PCR reacon was performed in
duplicate using an MX3000p PCR machine (Stratagene,
La Jolla, CA). Relave abundance in the expression of
each strain was calculated using the ΔΔCt method [30],
normalizing fold-change against Pan Bacteria, using
MX3000p soware (v.3; Stratagene).
Stascal analysis
Data are expressed as Relave abundance % ± SEM
for qRT-PCR analysis. Results were checked for normal
distribuon using the D'Agosno & Pearson normality
test before further analyses. Stascally signicant
dierences in the bacterial community were determined
by Student's t with Welch's correcon. Analyses
were performed with GraphPad Prism 7.0 (GraphPad
Soware, Inc., San Diego, CA). P-values equal to or less
than 0.05 were considered signicant.
Results and Discussion
In the present work, we invesgated diet impact
on microbial dysbiosis caused by the presence of AA
which in turn could impact on disorder evoluon and
manifestaons.
The preliminary analysis of macronutrients % in-
take (data not shown) suggested a Mediterranean diet
framework [31] for both case reports included in the
present study. Case report 1 diet included processed
food, red meat and low intake of fruits and vegetables.
Case report 2 diet included vegetables, fruit, peas, and
beans (legumes) and grains. When analyzed more deep-
ly as regards the type of proteins, lipids and carbohy-
drates ingested, diet from case-report 1 is beer classi-
ed as High fat-diet (more processed food, sugars, and
few bers). The second case reports can be considered,
instead, as following the Mediterranean like diet (lower
fruits intake compared to normal Mediterranean regi-
men).
Tables 1 and Table 2 show the intake of macronutri-

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• Page 4 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
The daily amount of total calories was signicantly
dierent among case reports (p < 0.01) (1,331.58 ±
ents and micronutrients in both case reports, compared
to Recommended (LARN) values in Italy.
Table 1: Daily reported energy and nutrient intake of studied case reports, assessed by a 7-day weighed food record. LARN:
Nutrition and Energy Reference Assuming Levels. a-cValues with different superscript letters, in the same row, differ signicantly
(P < 0.05).
Daily Intake Recommended
(LARN)
Case report 1 Case report 2
Total calories
(kcal/day)
M: 2000-2400a
F: 1800-2300
1,331.58 ± 189.61b693.09 ± 143.48c
Total proteins
(g/day)
75a60.93 ± 15.19a37.11 ± 16.01b
Animal proteins
(% of total proteins)
40a72.44 ± 10.14b47.33 ± 2.01a
Vegetal proteins
(% of total proteins)
60a27.56 ± 11.22b52.67 ± 4.05a
Total lipids
(g/day)
65a50.58 ± 18.81a29.11 ± 4.64b
Total carbohydrates
(g/day)
290a165.80 ± 22.15b75.54 ± 18.88c
Amide
(g/day)
220a95.15 ± 35.35b27.72 ± 28.77b
Fiber
(g/day)
23a16.59 ± 13.23a7.44 ± 1.33b
Cholesterol
(mg/day)
255a126.50 ± 81.79a51.76 ± 39.61b
Saturated fatty acids
(% of total)
7a10.06 ± 6.31a3.12 ± 1.00b
Polyunsaturated fatty acids
(% of total)
18a6.45 ± 1.31b6.36 ± 1.82b
Monounsaturated fatty acids
(% of total)
4a11.74 ± 5.01b15.06 ± 5.24b
Table 2: Daily reported micronutrient intake of studied case reports, assessed by a 7-day weighed food record. LARN: Nutrition
and Energy Reference Assuming Levels. a-cValues with different superscript letters, in the same row, differ signicantly (P < 0.05).
Daily Intake Recommended
(LARN)
Case report 1 Case report 2
Calcium (mg) M: 1200a
F: 1500
419.06 ± 406.77b141.05 ± 47.31c
Iron (mg) 18a5.50 ± 1.66b4.26 ± 1.91b
Zinc (mg) 7a7.33 ± 2.59a4.03 ± 1.30a
Folic acid (µg) 200a149.25 ± 43.89a67.33 ± 24.08b
Niacin (mg) 14a7.79 ± 3.45b9.05 ± 4.22b
Riboavin (mg) 1.2a0.45 ± 0.11b0.46 ± 0.25b
Thiamine (mg) 0.9a0.65 ± 0.16a0.48 ± 0.30a
Vitamin A (µg) 600a1,147.00 ± 141.88b499.68 ± 351.71c
Vitamin B6 (mg) 1.1a0.99 ± 0.38a0.70 ± 0.29a
Vitamin C (mg) 70a42.33 ± 25.41a19.57 ± 29.15a
Vitamin D (µg) 10a0.78 ± 1.48b4.58 ± 6.55a
Vitamin E (mg) 8a3.21 ± 2.57b10.25 ± 3.81b

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• Page 5 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
report 1 and case report 2, respecvely. Case report 1
also has a signicant (p < 0.01) lower intake of niacin
(7.79 ± 3.45) and vitamin E (3.21 ± 2.57) and higher (p <
0.001) intake of vitamin A.
Unbalancing in nutrients intakes is reported to have
an inuence both on hair follicle structure and hair
growth diseases such as telogen euvium, androgenet-
ic alopecia, AA and cicatricial alopecia [4,32-35].
Indeed, many of the above cited micronutrients are
reported to aect the hair follicle as regards restoraon
of hair growth, cell division, cycling [3]. Therefore, Singh
and collaborators [5] also highlighted diet eect on gut
microbiome. The same eect has been reported on oral
microbiome [36].
189.61 and 3.09 ± 143.48, respecvely) (Table 1).
Food diary from both subjects also reported a very
small intake of ber (16.59 ± 13.23 and 7.44 ± 1.33,
respecvely) and polyunsaturated fay acids (6.45 ±
1.31 and 6.36 ± 1.82, respecvely). Therefore, a lower
percentage of saturated fay acid intake was reported
for case report 2 (3.12 ± 1.00).
As regards micronutrients intake (Table 2) we
noced signicant lower intake of iron (5.50 ± 1.66 and
4.26 ± 1.91 vs. recommended) (p < 0.001) and folic acid
(149.25 ± 43.89 and 67.33 ± 24.08 vs. recommended)
(p < 0.01), riboavin (0.45 ± 0.11 and 0.46 ± 0.25 vs.
recommended) (p < 0.01) and vitamin D (0.78 ± 1.48
and 4.58 ± 6.55 vs. recommended) (p < 0.01) for case
Figure 4: Distribution of main bacterial strains in healthy subjects and AA subjects.
Figure 3: Women with initial stages of Alopecia areata.

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• Page 6 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
sults found in another autoimmune disease [42]. In both
case reports, an increase of Proteobacteria (33.28% and
27.71%, respecvely) has been reported. Most interest-
ing, analysis of sequences from case report 1 bacterial
oral DNA showed a decrease in Bidobacteria. A link
between a high-fat diet and this phylum decrease was
previously reported [43] thus conrming the role of diet
in inuencing oral bacterial composion. A signicant
reducon of Bacteroidetes has been found in case re-
port 2 compared to healthy control subjects. Since the
high intake of n-6 PUFA by case report 2, a link between
diet and this microbial unbalance could be hypothesized
as also suggested by some authors [44].
Results on bacterial composion of scalp microbi-
ome conrm our previous ndings on microbial shi
on the scalp in paents aected by AA [14,15]. In the
present work, we invesgated if dierent dietary habits
can re-modulate this microbial dysbiosis with the aim
to highlight the strict intercorrelaon between diet and
oral but especially scalp microbiome of these subjects.
The case reports of the present work represent just an
example of a larger clinical invesgaon we are leading
on this topic. For example, our clinical observaons sug-
gest that, in some paents aected by non-celiac gluten
sensivity (NCGS), AA manifestaons systemacally re-
curred following a non-gluten free diet. An explicave
photographic example was reported in Figure 6. Most
interesng this modulaon reects also in the microbi-
al composion of scalp microbiome (data not shown)
enhancing the existence of a link between diet and skin
bacterial communies scalp microbiome.
Data from the present study add to knowledge to
this evidence also highlighng that not only gut but
Evidence on the inuence of diet and microbiome
dysbiosis on skin disorders are mainly linked to topic
dermas [37], acne vulgaris [8,38-40], and psoriasis
[41]. In our previous works [14,15] on scalp microbial
community in hair growth disorders we showed, for the
very rst me, the presence of scalp bacterial shi in
such kind of disorders.
Figure 4 reports the % of the distribuon of main
bacterial strains in case report 1 and case report 2
compared with data from 15 healthy subjects and 15 AA
subjects in our database.
Data from case report 1 showed an increase in
P. acnes populaon and parallel decrease both of S.
epidermidis and S. aureus species. These data are in
line with data from the panel of AA subjects and clearly
evidence the presence of bacterial dysbiosis compared
to healthy control.
On the contrary, the percentage of distribuon of
main bacterial species in case report 2 resulted more
similar to the healthy populaon (Figure 4). Even if an
interindividual dierence has to be considered, the
analysis of food diary of the panel of een AA subjects
and case report 1 and 2 strongly suggested the impact
of diet in shaping scalp microbiome.
Data from oral bacterial DNA sequencing corrobo-
rated these ndings (Figure 5). Also, in this case, data
from case report 1 and 2 were compared to data from
our internal database of healthy and AA subjects, previ-
ously collected. The analysis of sequence at the phylum
level highlighted a slow decrease of Firmicutes both for
case report 1 and 1 (Figure 6) and these results are in
line with our previous ndings in AA subjects and re-
Figure 5: Data from oral bacterial DNA sequencing corroborated these ndings.

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• Page 7 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
6. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan
SH (2013) The inuence of diet on the gut microbiota.
Pharmacol Res 69: 52-60.
7. Vaughn AR, Notay M, Clark AK, Sivamani RK (2017) Skin-
gut axis: The relationship between intestinal bacteria and
skin health. World J Dermatol 6: 52-58.
8. Bowe WP, Joshi SS, Shalita AR (2010) Diet and acne. J
Am Acad Dermatol 63: 124-141.
9. Dawber R (1989) Alopecia areata. Monogr Dermatol 2: 89-
102.
10. Odom RB, Davidsohn IJ, William D, Henry JB, Berger
TG (2006) Clinical diagnosis by laboratory methods. In:
Elston Dirk M, Andrews’ Diseases of the Skin: Clinical
Dermatology. Saunders Elsevier.
11. Brenner W, Diem E, Gschnait F (1979) Coincidence
of vitiligo, alopecia areata, onychodystrophy, localized
scleroderma and lichen planus. Dermatologica 159: 356-
360.
12. Trink A, Sorbellini E, Bezzola P, Rodella L, Rezzani R,
et al. (2013) A randomized, double-blind, placebo- and
active-controlled, half-head study to evaluate the effects of
platelet-rich plasma on alopecia areata. Br J Dermatol 169:
690-694.
13. Clavaud C, Jourdain R, Bar-Hen A, Magali Tichit,
Christiane Bouchier, et al. (2013) Dandruff is associated
with disequilibrium in the proportion of the major bacterial
and fungal populations colonizing the scalp. PLoS One 8:
e58203.
14. Rinaldi F, Pinto D, Marzani B, Rucco M, Giuliani G, et al.
(2018) Human microbiome: What's new in scalp diseases.
J Transl Sci 4: 1-4.
15. Pinto D, Sorbellini E, Marzani B, Rucco M, Giuliani G, et al.
(2019) Scalp bacterial shift in Alopecia areata. PLoS One
14: e0215206.
16. Ho BS, Ho EXP, Chu CW, Ramasamy S, Bigliardi-Qi M,
et al. (2019) Microbiome in the hair follicle of androgenetic
alopecia patients. PLoS One 14: e0216330.
17. Polak-Witka K, Rudnicka L, Blume-Peytavi U, Vogt A (2019)
The role of the microbiome in scalp hair follicle biology and
disease. Exp Dermatol.
18. L Nair, Z Dai, AM Christiano (2017) 649 Gut microbiota
also oral and scalp microbiome could be modulated by
dietary habits.
Nowadays, the study of human microbiome rep-
resents a novel diagnosc and therapeuc approach to
treat many human condions, also including that strict-
ly related to skin and scalp. Beyond diet well-known im-
pact on general human health, our results highlighted
the role of diet in modifying oral and scalp microbiome,
which in turn seems to have an impact on Alopecia
areata evoluon.
According to our ndings and previous reported
evidence cited above, the modulaon of the gut
microbiome by mean of diet could represents a valid
approach in the managing of hair growth disorders,
especially AA, in which also the permeability of the gut
can be compromised [44].
Acknowledgment
This study was supported by Giuliani SpA.
Conict of Interest
R.F. and S.E. serve as a consultant for Giuliani S.p.A.
P.D. is employed by Giuliani S.p.A.
References
1. Schneider MR, Schmidt-Ullrich R, Paus R (2009) The hair
follicle as a dynamic miniorgan. Curr Biol 19: R132-R142.
2. Almohanna HM, Ahmed AA, Tsatalis JP, Tosti A (2019)
The Role of Vitamins and Minerals in Hair Loss: A Review.
Dermatol Ther (Heidelb) 9: 51-70.
3. Guo EL, Katta R (2017) Diet and hair loss: Effects of nutrient
deciency and supplement use. Dermatol Pract Concept 7:
1-10.
4. Finner AM (2013) Nutrition and hair: Deciencies and
supplements. Dermatol Clin 31: 167-172.
5. Singh RK, Chang HW, Yan D, Lee KM, Ucmak D, et
al. (2017) Inuence of diet on the gut microbiome and
implications for human health. J Transl Med 15: 73.
A B
Figure 6: A slow decrease of Firmicutes.

ISSN: 2572-3278DOI: 10.23937/2572-3278.1510037
• Page 8 of 8 •Rinaldi et al. J Nutri Med Diet Care 2019, 5:037
smooth muscle cell motility during aging. J Biol Chem 283:
4448-4458.
31. Castro-Quezada I, Román-Viñas B, Serra-Majem L (2014)
The mediterranean diet and nutritional adequacy: A review.
Nutrients 6: 231-248.
32. Rushton DH (2002) Nutritional factors and hair loss. Clin
Exp Dermatol 27: 396-404.
33. Mubki T, Rudnicka L, Olszewska M, Shapiro J (2014)
Evaluation and diagnosis of the hair loss patient: Part I.
History and clinical examination. J Am Acad Dermatol 71:
415.
34. Spivak JL, Jackson DL (1997) Pellagra: An analysis of 18
patients and a review of the literature. Johns Hopkins Med
J 140: 295-309.
35. Goldberg LJ, Lenzy Y (2010) Nutrition and hair. Clin
Dermatol 28: 412-419.
36. Kato I, Vasquez A, Moyerbrailean G, Land S, Djuric Z, et al.
(2017) Nutritional correlates of human oral microbiome. J
Am Coll Nutr 36: 88-98.
37. Manam S, Tsakok T, Till S, Flohr C (2014) The association
between atopic dermatitis and food allergy in adults. Curr
Opin Allergy Clin Immunol 14: 423-429.
38. Cordain L, Lindeberg S, Hurtado M, Hill K, Eaton SB, et
al. (2002) Acne vulgaris: A disease of Western civilization.
Arch Dermatol. 138: 1584-1590.
39. Grossi E, Cazzaniga S, Crotti S, Naldi L, Di Landro A, et
al. (2016) The constellation of dietary factors in adolescent
acne: A semantic connectivity map approach. J Eur Acad
Dermatol Venereol 30: 96-100.
40. Zouboulis CC, Jourdan E, Picardo M (2014) Acne is an
inammatory disease and alterations of sebum composition
initiate acne lesions. J Eur Acad Dermatol Venereol 28:
527-532.
41. Zákostelská Z, Málková J, Klimešová K, Pavel Rossmann,
Michaela Hornová, et al. (2016) Intestinal microbiota
promotes psoriasis-like skin inammation by enhancing
Th17 response. PLoS One 11: e0159539.
42. Zhang C, Zhang M, Wang S, Han R, Cao Y, et al. (2010)
Interactions between gut microbiota, host genetics and diet
relevant to development of metabolic syndromes in mice.
ISME J 4: 232-241.
43. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008)
Diet-induced obesity is linked to marked but reversible
alterations in the mouse distal gut microbiome. Cell Host
Microbe 3: 213-223.
44. Mu Q, Kirby J, Reilly CM, Luo XM, (2017) Leaky gut as a
danger signal for autoimmune diseases. Front Immunol 8:
598.
plays a role in the development of alopecia areata. Journal
of Investigative Dermatology 137: S112.
19. Olsen EA, Hordinsky MK, Price VH, Roberts JL, Shapiro
J, et al. (2004) Alopecia areata investigational assessment
guidelines--Part II. National Alopecia Areata Foundation. J
Am Acad Dermatol 51: 440-447.
20. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, et al.
(2010) Topographical and temporal diversity of the human
skin microbiome. Science 324: 1190-1192.
21. Paulino LC, Tseng CH, Strober BE, Blaser MJ (2006)
Molecular analysis of fungal microbiota in samples from
healthy human skin and psoriatic lesions. J Clin Microbiol
44: 2933-2941.
22. Gao Z, Perez-Perez GI, Chen Y, Blaser MJ (2010)
Quantitation of major human cutaneous bacterial and
fungal populations. J Clin Microbiol 48: 3575-3581.
23. Klindworth A, Pruesse E, Schweer T, Jörg Peplies, Christian
Quast, et al. (2013) Evaluation of general 16S ribosomal
RNA gene PCR primers for classical and next-generation
sequencing-based diversity studies. Nucleic Acids Res 41:
e1.
24. Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M
(2014) Development of a prokaryotic universal primer for
simultaneous analysis of bacteria and archaea using next-
generation sequencing. PLoS One 9: e105592.
25. Apprill A, McNally S, Parsons R, Weber L (2015) Minor
revision to V4 region SSU rRNA 806R gene primer greatly
increases detection of SAR11 bacterioplankton. Aquat
Microb Ecol 75: 129-137.
26. Parada AE, Needham DM, Fuhrman JA (2016) Every base
matters: assessing small subunit rRNA primers for marine
microbiomes with mock communities, time series and
global eld samples. Environ Microbiol 18: 1403-1414.
27. Walters W, Hyde ER, Berg-Lyons D, Ackermann G,
Humphrey G, et al. (2015) Improved bacterial 16S rRNA
Gene (V4 and V4-5) and fungal internal transcribed spacer
marker gene primers for microbial community surveys.
mSystems 1.
28. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D,
Lozupone CA, et al. (2011) Global patterns of 16S rRNA
diversity at a depth of millions of sequences per sample.
Proc Natl Acad Sci USA 108: 4516-4522.
29. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss
PD (2013) Development of a dual-index sequencing strategy
and curation pipeline for analyzing amplicon sequence data
on the MiSeq Illumina sequencing platform. Appl Environ
Microbiol 79: 5112-5120.
30. Vigetti D, Viola M, Karousou E, Rizzi M , Moretto P, et al.
(2008) Hyaluronan-CD44-ERK1/2 regulate human aortic