Content uploaded by Daniela Pinto
Author content
All content in this area was uploaded by Daniela Pinto on Aug 28, 2019
Content may be subject to copyright.
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Short Communication Open Access
International Journal of Experimental Biology
ISSN 2643-699X
Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Areata
Pinto Daniela1,2,3, Giammaria Giuliani1,2, Sorbellini Elisabetta2,3 and Rinaldi Fabio1,2,3*
1 Giuliani S.p.A., Milan, Italy
2 Human Advanced Microbiome Project-HMAP, Milan, Italy
3 International Hair Research Foundation (IHRF), Milan, Italy
*Corresponding Author: Rinaldi Fabio, Giuliani S.p.A, Human Advanced Microbiome Project-HMAP,
Human Advanced Microbiome Project-HMAP, Milan, Italy E-mail: fabio.rinaldi@studiorinaldi.com; Tel.: ++39-
2-76006089
Citation: Microbiome and Diet Impact in Scalp Disorder: the Example of Alopecia Areata. Inte J
Expe Bio. 2019; 2(1): 001-009.
Submitted: 05 July 2019; Approved: 08 July 2019; Published: 09 July 2019
Abstract
Introduction:
the gut microbiome. Poor information is still available as regards the link between microbiome, especially
scalp microbiome and hair diseases.
Aim: In the present work, we reported data on patients affected by Alopecia areata with the aim to
study the impact of the diet on microbiome changing related to scalp disease.
Methodology: Data from the dietary survey, qRT-PCR on main bacterial strains inhabiting the scalp
were matched and compared each other and with healthy population.
Results: Beyond the diet’s well-known impact on general human health, our results highlighted the
role of one’s diet in modifying scalp microbiome, which in turn seems to have an impact on AA evolution.
Conclusions: -
osis on the scalp of patients with AA and dietary habits.
Keywords: Alopecia Areata; Hair Disorders; Dietary Therapy; Microbiome; Dysbiosis
Alopecia Areata (AA) is a potentially reversi-
ble auto-immune disease affecting the scalp (Syed
& Sandeep, 2013; D’Ovidio, 2014). Its typical man-
ifestations occur in the form of non-scarring bald-
ness on the scalp, which can be possibly extended
to the entire body (Odom et al., 2006). When affect-
ed by non-scarring alopecia, a kind of disorder in
hair follicle cycling has been observed (Paus, 1996),
leading to the arrest of anagen phase, hair loss and,
consequently, annular or patchy bald lesions (Tan et
al., 2002; Camacho, 1997). In AA, in particular, this
disorder has been reported to be strictly linked to
Hordinsky et al., 2004; Trink et al., 2013). As the
second most common type of hair loss disorder (in-
cidence higher than 2%) (Dawber, 1989), AA has
been extensively studied as regards causes (Syed &
Sandeep, 2013) and clinical management options
(Messenger et al., 2012). A novel innovative ap-
proach also includes the use of Platelet-rich plasma
& Katta, 2017).
Hair follicle cells have a high turnover and a very
active metabolism so they require a good intake of
nutrients and energy from the diet. The impact of
diet on hair growth disorder is well established, es-
on shaping the gut microbiome and its implications
for human health has been largely studied (Scott et
al., 2013; Vaughn et al., 2017). Changing in diet reg-
imen can induce large, reversible microbial altera-
tions in less than one day (Scott et al., 2013). This is
especially true when we speak about the gut but it is
also true, for example, when talking about the skin
(Bowe et al., 2010).
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Poor information is still available as regards the
link between microbiome and diseases and they are
mostly related to gut microbiome (Rebello et al.,
2017; Borde & Astrand, 2018). But poor knowledge
is currently available about the impact of changing
in scalp microbial communities in hair disorders
(Clavaud et al., 2013; Xu et al., 2016). In a recently
published work (Rinaldi et al., 2018) we reported,
in hair loss disorder, such as Alopecia androgeneti-
ca, AA and Lichen planopilaris. In the present work,
we reported data on patients affected by Alopecia
areata, with the aim to study the impact of the diet
on microbiome changing related to scalp disease
Thirty subjects affected by Alopecia Areata (20–60
years old; 30% male) were included in the study.
We enrolled all subjects under dermatological con-
trol. Subjects have been previously diagnosed by
-
ing to the Severity of Alopecia Tool (SALT) (Olsen et
al., 2004). The following exclusion criteria were used
for both groups: a) pregnancy or lactation; b) affect-
ed by other dermatological diseases; c) anti-tumor,
immunosuppressant or radiation therapy in the last
3 months; d) no topical or hormonal therapy on the
scalp in the last 3 months; e) use of antibiotics in the
last 30 days; f) probiotics in the last 15 days. There-
fore, for scalp swab sampling, the last shampoo had
to be performed at least 48h before.
Characteristics of the population studied are
reported in Table 1.
Table 1 Characteristics of the population studied
AA
Age (mean±SD)
BMI
SALT score
S0
S1
S2
S3
S4
S5
41.66±13.04
23.20±2.38
0%
0%
30%
40%
20%
7%
Scalp surface has been sampled by mean of swab
procedure according to previously reported meth-
ods (Grice et al., 2009; Gao et al., 2010), with minor
extracted by mean of QIAamp UCP Pathogen Mini
Kit (Qiagen) according to manufacturer protocol,
Main bacterial species (Propionibacterium ac-
nes, Staphylococcus epidermidis and Staphylo-
-
al-time quantitative PCR (RT qPCR), using Microbial
PCR assay kit (Qiagen). Samples were mixed with
-
-
included. Pan-bacteria assays are also included as
as human GAPDH and HBB1 for the determination
of proper sample collection. The following ther-
mal cycling conditions were used: 95°C for 10 min,
40 cycles of 95°C for 15 sec, 60°C for 2 min. Each
PCR reaction was performed in duplicate using an
MX3000p PCR machine (Stratagene, La Jolla, CA).
Relative abundance in the expression of each strain
t method (Vigetti et
al., 2008), normalizing fold-change against PanBac-
teria, using MX3000p software (v.3; Stratagene).
dietary survey at the time of enrollment, following
being instructed by a dietician on how to record the
food and beverages consumed. The food surveys
were analyzed by Winford software (Winfood 2.7
Medimatica Srl, Colonnella, Italy) in order to esti-
mate the energy intake and the percentage of ma-
cronutrients and micronutrients. The data collected
was compared to the tables of food consumption
-
Database in Italy. The data is expressed as Relative
abundance % ± SEM for qRT-PCR analysis. The re-
sults were checked for normal distribution using
the D’Agostino & Pearson normality test before fur-
the bacterial community were determined by Stu-
dent’s t with Welch’s correction. The analysis was
performed with GraphPad Prism 7.0 (GraphPad
Software, Inc., San Diego, CA). P–values equal to or
Recent evidence suggests a strong correlation
between skin microbiome, including that of the
scalp, and many dermatological conditions (Cogen
et al., 2009; Zeeuwen et al., 2013; Belkaid & Hand,
2014). Poor information is currently available as re-
gards the microbial community inhabiting the scalp
and hair growth disorders. In a previous work we
-
terial unbalance in subjects affected by Alopecia (Ri-
naldi et al., 2018).
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Figure 1 reports the % of the distribu-
tion of main bacterial strains on the scalp in
analyzed subjects, grouped as regard SALT
score. Data are expressed as % of fold induc-
tion versus healthy subjects in our database.
All analyzed groups showed an increase in the P.
-
ferences were reported between groups. All groups
epidermidis species compared to baseline (healthy
-
ences were found as regard S. aureus species in
group S2, S3 and S4 (Fig. 1). On the contrary, a sig-
group (Fig. 1).
Figure 1:
of main bacterial species (P. acnes, S. epidermidis,
and S.aureus) inhabiting the scalp in subjects affect-
hair loss; S3: 50%-74% hair loss; S4: 75%-99% hair
Figure 3 show the intake of macronutrients
and micronutrients in the analyzed group, com-
Figure: 3a
Figure: 3b
Figure: 3c
Figure: 3d
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Figure: 3e
Figure: 3f
Figure: 3g
Figure: 3h
Figure: 3i
Figure: 3j
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Figure: 3k
Figure: 3l
Figure: 3m
Figure: 3n
Figure 3. Daily reported micronutrients intake in
-
trition and Energy Reference Assuming Levels.
(a) Calcium; (b) Iron; (c) Zinc; (d) Folic acid; (e)
(i) Vitamin B6; (j) Vitamin C (k) Vitamin D; (l) Bio-
tin; (m) Vitamin E; (n) Vitamin B12. S2: 25%-49%
hair loss; S3: 50%-74% hair loss; S4: 75%-99% hair
-
vey also highlighted a lower intake of lipids for S3
and S4 also showed lower and comparable intake of
(Fig. 2c). All analyzed groups also reported a very
-
ol (Fig. 2f) and saturated fatty acids (Fig. 2g) intake
-
(Fig. 2h) was reported in all groups. On the other
side, all groups showed a higher intake of monoun-
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Figure: 2a
Figure: 2b
Figure: 2c
Figure: 2d
Figure: 2e
Figure: 2f
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Figure: 2g
Figure: 2h
Figure: 2i
Figure 2: Daily reported macronutrients intake in
-
-
trition and Energy Reference Assuming Levels.
(a) Proteins; (b) Lipids; (c) Carbohydrates; (d)
Amide; (e) Fiber; (f) Cholesterol; (g) Saturated fat-
ty acids; (h) Polyunsaturated fatty acids; (i) Mon-
ounsaturated fatty acids. S2: 25%-49% hair loss;
S3: 50%-74% hair loss; S4: 75%-99% hair loss; S5:
With regards to the micronutrients intake (Fig.
to the zinc intake between groups and compared to
of folic acid was reported only in S4 and S5 groups
differences were reported in vitamins intake (Fig.
3e-j) with the exception of Vitamin D (Fig. 3k) (S2:
-
E and vitamin B12 was also reported in S3 and S5
our previous data. Here we added more knowledge
as regards to bacterial dysbiosis and AA severi-
unique ecosystem in AA patch which leads to an un-
balance in P. acnes species at the expense of S. epi-
dermidis species. Even if an interindividual differ-
ence has to be considered, this unbalancing did not
seem to be correlated with the severity of AA, with
the exception of the more severe grade (S5, as SALT
-
cant decrease of S. aureus species reported.
The aim of the present work was to investigate if
different dietary habits can contribute to microbial
dysbiosis of the scalp of AA subjects.
Hypocaloric regimen or scarcity of proteins, min-
erals, amino acids, vitamins, and essential fatty acids
derived from an unbalanced diet can lead to struc-
tural changes in the hair follicle and, eventually, to
hair loss (Rushton, 2002). Therefore, micronutri-
ents have been implicating in affecting chronic telo-
pattern hair loss (FPHL), and AA (Spivak & Jackson,
1977;
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
Goldberg & Lenzy, 2010; Mubki et al., 2014). Indeed,
many of the above micronutrients are reported to
affect the hair follicle regarding restoration of hair
growth, cell division, cycling (Finner, 2013).
Even though recent evidence (Scott et al., 2013)
strongly highlighted the ability of diet to impact on
gut and oral (Kato et al., 2017) microbiome, poor
diet on microbial dysbiosis in skin disorders (Bowe
et al., 2010; Gallo et al., 2011). Evidence is mainly
linked to acne vulgaris (Borde & Astrand, 2018;
Zouboulis et al., 2014; Grossi et al., 2016), atop-
ic dermatitis (Manam et al., 2014) and psoriasis
(Zákostelská et al., 2016).
More and more evidence has been accumulated
with regards to the link between gut and hair disor-
ders (Rebello et al., 2017; Borde & Astrand, 2018).
In autoimmune disease, among which AA, immune
response leads to tissue damage and loss of function
of the intestinal barrier (Mu et al., 2017). Therefore,
the permeability of the epithelial lining may be
compromised; antigens, toxins, and bacteria migrat-
ed from the lumen to the bloodstream leading to a
syndrome known as “leaky gut” (Mu et al., 2017).
Modulating the gut microbiome also by mean of diet
represents a valid approach for regulating and re-
storing such damage, leading to an improvement of
the autoimmune disease.
Combining data from microbial dysbiosis of
the scalp and diet a clear link between dietary
food intake and the severity grade of AA could not
be hypothesized. On the other hand, the impact of
lower intake of some macronutrient and micronu-
trients lead to hypothesize an impact on microbial
dysbiosis on the scalp and suggests the possibility
to modulate microbial dysbiosis by targeted dietary
approaches.
For example, modulating the intake of mono-
unsaturated fatty acids by lowering them in favor of
some polyunsaturated fatty acids could help reduce
Similarly, improving the intake of some micro-
nutrients such as calcium, iron and folic acid could
lead to an improvement of hair follicle healthiness.
Most interestingly, all analyzed groups reported a
lower intake of vitamin D and biotin, two micronu-
trients strongly involved in hair follicle development
(Finner, 2013; Chiu et al., 2015; Patel et al., 2017).
limited to hair follicle development itself, but also
extended to the modulation of the microbial ecosys-
tem around the hair follicle. Thus, increasing dairy
intake of biotin and in general, vitamins leads to an
increase of nutrients for the hair follicle contribut-
ing to a healthier ecosystem for microbial commu-
nities of the scalp which can result in themselves be
stimulated into micronutrients biosynthesis.
The data from the present study is just a limit-
ed representation of a larger set of data we have ac-
cumulated in our clinical practice. Indeed, we have
noticed, for example, how a gluten-free diet could
strongly affect AA evolution in patients affected by
manifestations systematically recurred following
a non-gluten free diet. Therefore, even though not
conclusive, our data also opens to a new diet and
microbiome-based adjuvant approaches in the man-
agement of hair disorders such as AA. Larger studies
are still needed to better investigate the role of the
microbiome in scalp diseases and different drivers
involved in this process.
AUTHOR STATEMENTS
Conceptualization, Methodology, and Investi-
gations: DP and FR. Data curation and Formal Anal-
ysis: DP. Resources: ES and FR. Wrote the paper: DP,
BM, and FR. Funding acquisition: GG and FR. Super-
vision: ES and FR.
CONFLICT OF INTEREST
FR and ES serve as a consultant for Giuliani
S.p.A. DP are employed by Giuliani S.p.A.
FUNDING INFORMATION
This study was supported by the Giuliani SpA.
ETHICAL APPROVAL
The study was approved by the Ethical Inde-
pendent Committee for Clinical, not a pharmacolog-
ical investigation in Genoa (Italy) and in accordance
with the ethical standards of the 1964 Declaration
of Helsinki. Volunteers signed informed consent.
REFERENCES
1. Belkaid, Y, Hand, T (2014). Role of the microbiota in
2. Borde, A, Åstrand, A (2018). Alopecia areata and the
gut-the link opens up for novel therapeutic interventions. Ex-
pert Opin Ther Targets 22(6),503-511.
3. Bowe, WP, Joshi, SS, Shalita, AR (2010). Diet and acne.
J Am Acad Dermatol 63,124-41.
4. Brenner, W, Diem, E, Gschnait, F (1979) Coincidence of
vitiligo, alopecia areata, onychodystrophy, localized scleroder-
ma and lichen planus. Dermatologica 159(4),356-60.
5. Camacho, F (1997). Alopecia areata. Clinical char-
acteristics and dermatopathology. In: Trichology: Diseases of
the Pilosebaceous Follicle. Aula Medical Group S. A, Madrid pp.
440–471.
6. Chiu, CH, Huang, SH, Wang, HM (2015). A review: hair
health, concerns of shampoo ingredients and scalp nourishing
treatments. Curr Pharm Biotechnol 16, 1045–1052.
7. Clavaud, C, Jourdain, R, Bar-Hen, A, et al. (2013) Dan-
druff is associated with disequilibrium in the proportion of the
major bacterial and fungal populations colonizing the scalp.
PLoS One 8(3):e58203. Erratum in: PLoS One 8(10).
A source of disease or defence? Br J Dermatol 158,442-455.
9. Cordain, L, Lindeberg, S, Hurtado, M, Hill, K, Eaton, SB,
Brand-Miller, J (2002). Acne vulgaris: a disease of Western civi-
Cite this article: Microbiome and Diet Impact in Scalp Disorder: The Example of Alopecia Area-
ta. Inte J Expe Bio. 2019; 2(1): 001-009.
lization. Arch Dermatol 138,1584-1590.
10. Dawber, R (1989). Alopecia areata. Monogr Dermatol
2,89-102.
11. D’Ovidio R (2014). Alopecia Areata: news on diag-
nosis, pathogenesis, and treatment. G Ital Dermatol Venereol
149(1),25-45.
and supplements. Dermatol Clin 31(1),167-72.
with the innate immune defense system of the skin. J Invest
Dermatol 131,1974-1980.
14. Gao, Z, Perez-Perez, GI, Chen, Y, Blaser, MJ (2010).
Quantitation of Major Human Cutaneous Bacterial and Fungal
Populations . J ClinMicrobiol 48(10),3575-3581.
Dermatol 28(4),412-419.
16. Grice, EA, Kong, HH, Conlan, S, et al. (2009). Topo-
graphical and Temporal Diversity of the Human Skin Microbi-
17. Grossi, E, Cazzaniga, S, Crotti, S, et al. (2016). The con-
stellation of dietary factors in adolescent acne: a semantic con-
nectivity map approach. J Eur Acad Dermatol Venereol 30,96-
100.
18. Guo, EL, Katta, R (2017). Diet and hair loss: effects of
& Conceptual 7(1),1-10.
19. Hordinsky, M, Ericson, M (2004). Autoimmunity: alo-
pecia areata. J Investig Dermatol Symp Proc 9(1),73-8.
-
36(2),88-98.
21. Klindworth, A, Pruesse, E, Schweer, T, et al. (2013)
classical and next-generation sequencing-based diversity stud-
Microbiota and Salivary Diagnostics: The Mouth Is Salivating to
Tell Us Something. BioResearch Open Access 6(1),123-132.
23. Manam, S, Tsakok, T, Till, S, Flohr, C (2014). The associ-
ation between atopic dermatitis and food allergy in adults. Curr
Opin Allergy Clin Immunol 14,423-429.
24. Messenger, AG, McKillop, J, Farrant, P, McDonagh,
AJ, Sladden, M (2012). British Association of Dermatologists’
guidelines for the management of alopecia areata 2012. Br J
Dermatol 166(5),916-26.
25. Mu Q, Kirby J, Reilly CM, Luo XM (2017). Leaky Gut As
a Danger Signal for Autoimmune Diseases. Frontiers in Immu-
nology 8:598.
26. Mubki, T, Rudnicka, L, Olszewska, M, Shapiro, J (2014).
Evaluation and diagnosis of the hair loss patient: part I. Histo-
ry and clinical examination. J Am Acad Dermatol 71(3),415.e1-
e415.e15.
27. Odom, RB, Davidsohn, IJ, William, D, Henry, JB, Berger,
TG (2006). Clinical diagnosis by laboratory methods. In: Elston,
Dirk M. (Ed.), Andrews’ Diseases of the Skin: Clinical Dermatol-
ogy. Saunders Elsevier. 2006.
28. Olsen, EA, Hordinsky, MK, Price, VH (2004). Alopecia
Alopecia Areata Foundation. J Am Acad Dermatol 51,440–447.
29. Patel, DP, Swink, SM, Castelo-Soccio, L(2017). A review
of the use of biotin for hair loss. Skin Appendage Disord 3, 166–
169.
30. Paus, R (1996). Control of the hair cycle and hair dis-
eases as cycling disorders. Curr Opin Dermatol 3,248-258.
31. Rebello, D, Wang, E, Yen, E, Lio, PA, Kelly, CR (2017).
Hair Growth in Two Alopecia Patients after Fecal Microbiota
Transplant. ACG Case Rep J 4:e107.
32. Rinaldi, F, Pinto, D, Marzani, B, Rucco, M, Giuliani, G,
Sorbellini, E (2018). Human microbiome: What’s new in scalp
diseases. J Transl Sci 4(6), 1-4.
Clin Exp Dermatol 27(5),396–404.
34. Scott, KP, Gratz, SW, Sheridan, PO, Flint, HJ, Duncan, SH
-
Clavaud et al., 2013; Pharmacol Res 69(1),52-60.
diet on the gut microbiome and implications for human health. J
Transl Med 15(1),73.
36. Spivak, JL, Jackson, DL (1977). Pellagra: an analysis of
18 patients and a review of the literature. Johns Hopkins Med J
140(6),295- 309.
37. Syed, SA, Sandeep, S (2013). Alopecia areata: A review.
J Saudi Dermatol & Dermatol Surg Soc 17(2), 37-45.
38. Tan, E, Tay, YK, Goh, CL, Chin, Giam, Y (2002). The pat-
Asians. Int J Dermatol 41(11),748-53.
39. Trink, A, Sorbellini, E, Bezzola, P, et al. (2013). A rand-
omized, double-blind, placebo- and active-controlled, half-head
study to evaluate the effects of platelet-rich plasma on alopecia
areata. Br J Dermatol 169(3),690-4.
Skin-gut axis: The relationship between intestinal bacteria and
skin health. World J Dermatol 6(4),52-58
41. Vigetti, D, Viola, M, Karousou, E, et al. (2008). Hyalu-
ronan-CD44-ERK1/2 regulate human aortic smooth muscle cell
motility during aging. J Biol Chem 283,4448–58.
42. Xu, Z, Wang, Z, Yuan, C, et al. (2016). Dandruff is asso-
ciated with the conjoined interactions between host and micro-
43. Zákostelská, Z, Málková, J, Klimešová, K, et al. (2016).
-
tion by Enhancing Th17 Response. PLoS One 11:e0159539.
44. Zeeuwen, PL, Kleerebezem, M, Timmerman, HM,
Schalkwijk, J (2013). Microbiome and skin diseases. Curr Opin
Allergy Clin Immunol 13,514-20.
45. Zouboulis, CC, Jourdan, E, Picardo, M (2014). Acne is
initiate acne lesions. J Eur Acad Dermatol Venereol 28,527-532
