Experimental Dermatology - 2019 - Polak Witka - The Role of The Microbiome in Scalp Hair Follicle Biology and Disease

Received: 1 October 2018 | Revised: 2 March 2019 | Accepted: 18 March 2019
DOI: 10.1111/exd.13935
REVIEW
The role of the microbiome in scalp hair follicle biology and

disease
Katarzyna Polak‐Witka1,2 | Lidia Rudnicka2 | Ulrike Blume‐Peytavi1 | Annika Vogt1

1
Clinical Research Center for Hair and Skin
Science, Department of Dermatology and Abstract
Allergy, Charité‐Universitaetsmedizin Berlin, The skin surface microbiome and its role in skin diseases have received increasing
corporate member of Freie Universitaet
Berlin, Humboldt-Universitaet zu Berlin, and attention over the past years. Beyond, there is evidence for a continuous exchange
Berlin Institute of Health, Germany with the cutaneous immune system in healthy skin, where hair follicles (HFs) provide
2
Department of Dermatology, Medical
unique anatomical niches. Especially, scalp HFs form large tubular invaginations,
University of Warsaw, Warsaw, Poland
which extend deeply into the skin and harbour a variety of microorganisms. The dis‐
Correspondence
tinct immunology of HFs with enhanced immune cell trafficking in superficial com‐
Annika Vogt, Clinical Research Center
for Hair and Skin Science, Department partments in juxtaposition to immune‐privileged sites crucial for hair follicle cycling
of Dermatology and Allergy, Charité‐
and regeneration makes this organ a highly susceptible structure. Depending on com‐
Universitaetsmedizin Berlin, Chariteplatz 1,
10117 Berlin, Germany. position and penetration depth, microbiota may cause typical infections, but may
Email: [email protected]
also contribute to pro‐inflammatory environment in chronic inflammatory scalp dis‐
eases. Involvement in hair cycle regulation and immune cell maturation has been pos‐
tulated. Herein, we review recent insights in hair follicle microbiome, immunology
and penetration research and discuss clinical implications for scalp health and
disease.
KEYWORDS
alopecia, bacteria, immune system, inflammation, nanoparticles
1 | I NTRO D U C TI O N within the follicular opening and upper part of the HF (the infundib‐
ulum), only single studies have reported on microbes located deeply
A single square centimetre of human skin, along with adnexal struc‐ in the follicle.[9‒12]
tures, can be inhabited by up to one billion of microorganisms includ‐ From the clinical perspective, inflammatory processes along
ing bacteria, fungi and viruses, forming a complex community known the hair follicle occur in multiple hair diseases. While bacterial
as the skin microbiome.[1,2] Its composition varies distinctly across folliculitis, furuncle and abscess formation represent classical in‐
different skin regions depending on pH, temperature, moisture and fectious diseases, various chronic skin diseases are characterized
sebum content of the same individual.[3,4] A vast range of external by an abnormal immune response to shifts in the skin flora in a
factors connected with for example, vaginal or caesarean delivery, susceptible host. The latter is probably observed in acne vulgaris
living environment (sunlight exposure, air temperature and humid‐ and hidradenitis suppurativa, but the exact mechanisms underly‐
ity), lifestyle habits or used cosmetics, along with probable genetic ing the microbial contribution to the disease and targeted effective
predispositions to particular microbiotas, shape the skin microbiome treatment remain to be determined.[1] Moreover, disturbance of
[5‒7]
and result in high interpersonal variabilities. Hair follicles (HFs) immune‐privileged sites and autoimmune reactions are key events
extending from the skin surface to the dermis or subcutaneous tis‐ in chronic hair follicle diseases such as alopecia areata (AA) and
sue with direct connection to the sebaceous gland (“pilosebaceous lichen planopilaris, in which immunosuppressive and immunomod‐
unit”) create a unique lipid‐rich hydrophobic niche.[8] Whereas many ulatory agents are widely used but not always with satisfactory
studies have confirmed the presence of numerous bacteria and fungi results.[13,14]
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POLAK‐WITKA et al. | 287
2 | S C A LP H A I R FO LLI C LE A S A D I S TI N C T In contrast to the massive exposure to microbial material in its

A N D CO M PLE X O RG A N upper part, immune‐privileged sites are found around the stem cell‐
bearing bulge as well as around the anagen bulb. Here, immune cells
100 000‐150 000 HFs of a total number of five million human HFs are significantly reduced and gradients of mediators with immuno‐
which are formed during embryogenesis and ensure cyclic hair suppressive properties could be identified. A collapse of the immune
[15]
growth throughout our life time are located on the scalp. Their privilege is a key element in the pathogenesis of chronic scalp dis‐
openings contribute to a significant increase of skin surface area and, eases. The question as to whether the bulb or the bulge immune
more importantly with regard to colonization, form pockets along privilege is disturbed determines if the hair follicle itself is preserved
the infundibulum, which extend into deeper scalp skin layers.[16] of long time periods, as observed in AA, or if a hair follicle is perma‐
The infundibulum is typically filled with sebum, debris and mi‐ nently lost as observed in cicatricial alopecia.[13,14]
croorganisms ranging from viruses to bacteria, but also yeasts/
fungi and even mites.[1,16] Its epithelium is characterized by a rich
network of antigen‐presenting cells and active immune cell traffick‐ 3 | H OW C A N M I C RO B E S G E T ACC E S S TO
ing (Figure 1). The reservoir function and the shift of differentiation K E R ATI N O C Y TE S A N D TH E CU TA N EO U S
towards deeper parts make it a site of intensive communication with I M M U N E S YS TE M?
the external environment. While the general architecture among the
different hair follicle types is rather similar, it needs to be noted with To understand where, how and to which extent microbial material
regard to reservoir function and microbiome, that HF size and the gets in contact with viable cells, different aspects have to be consid‐
proportions of permanent to cycling parts differ substantially be‐ ered. Given that the general size of bacteria is in the low micrometre
tween large terminal HFs whose anagen bulbs extend deep into the range, penetration into the infundibular area should be largely re‐
subcutaneous tissue, compared to vellus HFs. Also the relation of stricted to the deeper infundibulum and sebaceous gland. Yet, while
sebaceous gland size and activity within the pilosebaceous unit are the upper compartments of the infundibulum are covered with thick
different across the body regions.[15] stratum corneum, the deeper infundibulum is widely considered as
area of higher permeability.[17]
Furthermore, epithelial surfaces can be colonized by bacteria
forming biofilm communities. Staphylococcus epidermidis (S. epider-
midis) forms biofilms between squamous cells of the outer three
to ten layers of the stratified epithelium of normal dry skin.[18]
Cutibacterium acnes (C. acnes) macrocolony/biofilm penetrates deep
in the sebaceous follicle, attached to the hair shaft, in the facial skin
of healthy controls and more often in patients with acne.[9] The for‐
mation of a biofilm provides bacteria with a protective shield against
innate immune cells and against the regular shedding process.[18]
Moreover, in contrast to engineered particles, certain bacteria are
equipped with enzymes which help promote penetration and tis‐
sue invasion.[3] As for dermatophytes in tinea capitis, deep invasion
along root sheaths (ectothrix) and even into hair shaft (endothrix) has
been observed.[19]
Larger studies on the penetration of micro‐ and nanoparticles
have demonstrated that microparticles largely remain on the skin
F I G U R E 1 Morphology and immunology of the pilosebaceous
unit. While the superficial parts of the pilosebaceous unit including surface, but also reach the deeper infundibulum of scalp HFs. Even
infundibulum, isthmus, bulge region and sebaceous gland remain nanoparticles only penetrate at very limited rates depending on
stable (permanent part), the deeper parts of the hair follicle their physicochemical properties.[20‒22] Mild disturbance of the skin
with the suprabulbar region and the bulb proliferate and regress barrier can be associated with particle translocation into the viable
throughout the hair cycle (non‐permanent). Dense infiltration
tissue, cellular particle uptake and subsequent immune reactions.[23]
of dendritic cells and CD4+ cells is observed at the level of the
infundibulum. Macrophages and mast cells are located along the Despite the fact that the barrier function of the skin is usually robust
hair follicle, outside the outer root sheath, within the adjacent enough to limit penetration of large molecules and particulate com‐
connective tissue sheath. Less abundant CD8+ cells reach the pounds to single events, such interactions occur on a regular basis,
maximal density in the infundibulum and below decline markedly. most pronounced in niches and pockets such as HFs and furrows.
Compared to the dense infiltration around the infundibulum, the
It has been hypothesized that the density of antigen‐presenting
part which hosts rich microbial flora, the areas of the bulb and
cells around infundibula with enhanced dendricity may reflect the
bulge feature a significant lower number of immune cells and
are considered to be immune‐privileged sites. HS, hair shaft; SG, central role of those structures.[24] Interesting insights have been
sebaceous gland; B, bulge gained from transcutaneous vaccination studies suggesting that
288 | POLAK‐WITKA et al.
mild inflammatory stimuli which put antigen‐presenting cells in an in the released cytokine profile. Thus, the composition of microbial
activated state increase uptake capacities for large molecules across communities may influence the immunological status of the skin.[1,29]
[25]
the skin barrier. As outlined in the following, microbe‐host inter‐ Commensals are considered essential to maintain skin homoeo‐
actions at this interface may even have a regulatory role on skin ho‐ stasis. They protect the skin from its colonization by pathogens, stim‐
moeostasis and hair cycling. ulate production of the complement system and cytokines involved
in the initiation and maintenance of an immune response.[8,29,30]
Furthermore, microbiota helps to decrease the magnitude of inflam‐
4 | I M M U N O LO G Y C ROS S ‐TA LK— mation and promotes tissue repair.[31]
M I C RO B E S I N FLU E N C E I M M U N O LO G I C A L Gene expression analysis of mice reared in the presence of
S TAT U S O F TH E S K I N A N D H A I R FO LLI C LE S microbiota compared to those devoid of microbes showed upreg‐
ulation of innate immune response genes (encoding eg Toll‐like re‐
Numerous immune cells are deployed in the skin and around its ap‐ ceptors [TLRs], antimicrobial peptides [AMPs]) and genes involved
pendages in close proximity to microbiota (Figure 2).[26] Langerhans in cytokine activity (eg in cutaneous IL‐1 signalling) in mice colonized
cells (LCs), which are predominantly concentrated in the epidermis with normal flora. Furthermore, differential expression of genes en‐
and outer root sheath (ORS) of the upper portion of the HF, have coding proteins involved in the differentiation and cornification of
the capacity to extend their dendrites between keratinocytes and keratinocytes was observed in a microbial‐dependent manner.[32]
[27]
capture microbial antigens. LCs interact with skin‐resident mem‐ Keratinocytes, including follicular keratinocytes and sebocytes,
ory T cells, probably featuring the memory to antigens encountered protect the host and simultaneously control the shape of microbiome
through epithelium. At steady state, LCs induce activation and pro‐ by producing different AMPs of a broad‐spectrum activity against
liferation of skin‐resident memory T regulatory cells involved in bacteria, fungi, viruses and parasites. Some AMPs are constitutively
peripheral tolerance induction. In the presence of a pathogen, how‐ expressed, whereas the production of others is stimulated by skin
ever, they also stimulate the proliferation of skin pathogen‐specific microbiota such as Cutibacterium (formerly Propionibacterium).[33,34]
[28]
resident effector memory T cells. Microbe‐derived products can Pattern recognition receptors on keratinocytes, such as TLRs, rec‐
also be actively engulfed by other antigen‐presenting cells, adjacent ognize pathogen‐associated molecular patterns such as lipopoly‐
keratinocytes, or can passively diffuse through the epithelial bar‐ saccharide (LPS) of Gram‐negative bacteria. The activation of these
rier, particularly within the lower part of the infundibulum, where receptors either initiates the immune response and secretion of
the epidermal differentiation shifts towards a tricholemmal differ‐ AMPs, cytokines and chemokines, or quite the opposite, inhibits the
entiation.[26] Skin‐resident CD103+ dendritic cells may sense altera‐ inflammation.[30]
tions in microbial communities and, in the absence of inflammation, Diverse AMPs have been identified within different structures
+ +
stimulate influx of IL‐17A CD8 T cells into the epidermis. The strong‐ of the scalp HF in steady‐state conditions, and some of them were
est stimulation of these cells has been reported in a murine model found to be elevated during inflammation. Under physiological con‐
during the colonization with S. epidermidis.[29] However, presence of ditions, all suprabasal layers of the epidermis, the distal and central
different commensal species is associated with distinct differences (including the bulge) part of the ORS, along with the sebaceous gland,
release human β‐defensin 1 and 2. A weaker expression of these
AMPs was also identified in the proximal region of the ORS and in the
inner root sheath (IRS).[35] Psoriasin was present in the epidermis and
distal ORS of the human scalp HF, whereas RNase7 was expressed
throughout the entire ORS. Both proteins were also found in the
sebaceous gland, and both could be induced by selective classical
microbial products.[36] In the scalp HFs, the stimulation of TLR4 with
LPS resulted in the release of RNase7 and psoriasin, whereas the
stimulation of TLR5 with flagellin (a component of Gram‐negative
bacteria), in the production of RNase7 only.[36] Furthermore, bacte‐
ricidal\permeability‐increasing protein was identified in the IRS.[37]
The strongest expression of AMPs within the upper part of the HF is
F I G U R E 2 The infundibulum hosts rich microbiome. The figure in line with the fact that this region holds the largest concentration
presents the capacity of the infundibulum extending from the skin of microbiota. The peptides are released to prevent microorganisms,
surface to the level of sebaceous duct opening, forming a pocket especially pathogens, from the penetration into the HF and probably
filled with numerous microorganisms: bacteria, yeasts, mites and to modulate the composition of follicle microbiome.[36]
viruses. While multiple studies have been conducted using skin
Microbes also have the capability to produce AMPs themselves.
surface swabs, the level of organization and interaction within
S. epidermidis and S. hominis release lantibiotics inhibiting the coloni‐
compartment is poorly understood. LC, Langerhans cell. *Diameter
of the infundibulum at skin surface level. **Diameter of the zation of S. aureus.[33] Serine protease glutamyl endopeptidase (Esp)
infundibulum at sebaceous duct opening level expressed by a subset of S. epidermidis strains can dissolve proteins
indispensable for formation of biofilm by S. aureus. However, it has oxygen tension, little is known regarding the environmental condi‐
also been reported that commensals can act exactly the opposite tions below the infundibulum.[30]
and contribute to skin colonization with pathogens. Depending on So far, scalp swabs have served as the most common material
dose, growth phase and pH, some Cutibacterium species manage to for scalp microbiome analyses. The most abundant bacteria found
induce aggregation of S. aureus.[3] in scalp swabs of healthy individuals are Cutibacterium spp. (with
Both HF morphogenesis and skin colonization with microbes in the vast majority of C. acnes) and Staphylococcus spp. (with the
mice during neonatal period are crucial for the migration of T reg‐ predominance of S. epidermidis), comprising approximately 90%
ulatory cells (Tregs) into HFs, and thereby for the development of of the total gene sequences. Corynebacterium spp., Streptococcus
immunological tolerance to skin commensal bacteria. This unique spp., Acinetobacter spp., and Prevotella spp. are listed among
+
subset of CD4 T cells plays a significant role in suppressing autoim‐ other significantly less numerous species.[42‒44] Some discrep‐
mune responses and maintaining immune homoeostasis in periph‐ ancies between studies have also been presented; for example,
eral tissues. Scharschmidt et al. showed in a neonatal murine model Perez‐Perez et al.[45] found a putatively lower representation of
and human skin explants, that the presence of cutaneous microbes Cutibacterium spp. in the scalp colonization. Changes in the com‐
stimulates the expression of chemokine Ccl20 within the infundib‐ position of the scalp residential bacteria with ageing were studied
ulum of developing HF. The receptor for Ccl20 (Ccr6) was identified in women by Shibagaki et al. Their results revealed, that the older
on Tregs in neonatal skin and thymus gland. This Ccl20‐Ccr6 path‐ group (60‐76 years) featured higher species richness and marked
way proved to be responsible for the inflow of the thymic subset of increase in the number of minor species than the younger group
[38,39]
Tregs into HFs. A transient inhibition of Treg migration during (21‐37 years). Moreover, the ageing‐related shifts in the scalp
this neonatal period or postponing of skin colonization with com‐ microbiome were correlated with changes of the oral bacterial
mensal bacteria to adult life resulted in histologic evidence of skin flora.[43]
inflammation and failure to establish the tolerance to residential Studies on the microbiome of the deeper portions of the scalp
[39]
bacteria. If the process of establishment of tolerance to commen‐ HF are scarce. Gram‐positive bacteria located deep within the in‐
sal bacteria also takes place in a limited period of time in humans, fundibulum were detected in biopsy samples by light and electron
its disruption might result in an inflammatory response to antigens microscopy.[10,12] Images of Matard et al. captured by field emission
[1]
introduced in later life. scanning electron microscopy and confocal laser scanning micros‐
Aside from the determination of tolerance towards commensal copy showed structures compatible with bacterial biofilm located
skin bacteria, Tregs seem to have direct effects on hair cycle regula‐ below the infundibular part, above the matrix zone of plucked hairs
tion. According to a recent study, these cells promote regeneration in two of three healthy individuals. The biofilms comprised bacilli
of the HF. Ali et al. found that Tregs accumulate in close proximity and morphologically corresponded to C. acnes.[11]
to the bulge of telogen HF and stimulate proliferation and differ‐ The vast majority of studies on the composition of fungi on
entiation of stem cells, and therefore transition to anagen phase. the human scalp (scalp mycobiome) is based on the analysis of
Lack of this subset of T cells led to impairment of follicle entry into swab samples. Among Malassezia spp., which largely predomi‐
the growth phase both after depilation and during the natural HF nate on the scalp, Malassezia globosa (M. globosa) and M. restricta
[40]
cycle. It remains obscure, whether microbes have an impact on were the most abundant species according to different stud‐
the activity and maintenance of Tregs in the skin after the neonatal ies.[44,46‒48] Ascomycota (Acremonium spp., Didymella bryoniae),
[41]
period and whether they contribute to hair cycle regulation. other Basidiomycota (Cryptococcus liquefaciens and C. diffluens),
Coniochaeta spp., Rhodotorula spp., were also identified on healthy
scalp.[49] Mycobiome of children (age <14) was found to be more
5 | CO M P OS ITI O N O F TH E M I C RO B I O M E diverse with a relatively lower part of Malassezia spp. compared to
O N TH E S C A LP S U R FAC E A N D I N adults (age 20s‐30s). This is most likely due to the fact that seba‐
TE R M I N A L S C A LP H A I R FO LLI C LE S ceous glands exhibit lower activity and different sebum composition
before puberty.[47] Yeasts were also identified in the infundibulum
Scalp is rich in sebaceous glands, which produce sebum released by light and electron microscopy in biopsy samples and in vivo on the
via sebaceous ducts into the infundibula and to the skin surface. scalp by confocal laser scanning microscopy.[12,50]
Although sebum, a mixture of lipids and the debris of lipid‐produc‐ Not only bacteria and fungi but also other microorganisms such
ing cells, has antimicrobial properties, some microbes manage to as mites or viruses colonize the human scalp. Demodex folliculorum
thrive in this environment (Figure 2). Cutibacterium hydrolyses tri‐ is usually found in the follicular infundibulum, while Demodex bre-
glycerides and releases free fatty acids promoting its adherence. vis is located in sebaceous glands.[51] Dermatophagoides spp. and
Malassezia spp. and Corynebacterium spp. do not produce their own Euroglyphus spp. were identified by Naspitz et al. in a material col‐
lipids and may benefit from lipids of the sebum. Whereas the niche lected by vacuuming the scalp surface.[52] Among viruses, human
for microbes inhabiting the upper portion of the follicle is probably papilloma virus was detected in healthy volunteers in plucked hairs
mainly influenced by sebum properties and possibly variations in and in scales collected from the scalp.[53]
6 | C H A N G E S O F TH E H A I R FO LLI C LE patients with FD.[11,58] Although such structures were also found
M I C RO B I O M E I N S C A LP D I S E A S E S in plucked HFs from healthy individuals, the hypothesis about bio‐
film is quite convincing. The persistence of the disease despite a
The strongest evidence supporting correlations with microorgan‐ transiently effective antibiotic therapy, infiltration of polymorpho‐
isms colonizing the scalp has been found in seborrheic dermatitis/ nuclear neutrophils in histology, which destroy the follicle but are
dandruff and in a type of cicatricial alopecia named folliculitis decal‐ not able to destroy the biofilm, and normal immune background
vans (FD). An antimicrobial treatment administered in these diseases of patients, are enumerated among supporting arguments. As it is
brings a transient success in most cases. However, frequent recur‐ currently postulated, an initially non‐pathogenic biofilm may be‐
rences, lack of efficacy in some patients and the additional need of come more extensive and transform into a pathogenic form caus‐
anti‐inflammatory therapy in acute flare‐ups indicate the complexity ing an inflammation. Antibiotic treatment may kill the planktonic
of their ethiopathogenesis.[11,54] form of bacteria released from biofilms and even temporarily obvi‐
ate symptoms, but the remaining biofilm cells constitute the nidus
of chronic infection.[11,18]
6.1 | Seborrheic dermatitis of the scalp and dandruff
Seborrheic dermatitis is an inflammatory skin condition develop‐
6.3 | Androgenetic alopecia
ing within sebum‐rich areas. Dandruff is considered a mild type of
seborrheic dermatitis limited to the scalp. The ethiopathogenesis of Androgenetic alopecia (AGA) features shortening of the anagen
the disease is not fully understood and, for years, has been associ‐ phase and a slowly progressing miniaturization of the hair follicle over
ated with an inflammatory response to yeasts. [54] A potential patho‐ time. Infiltration of mononuclear cells and lymphocytes is detected
mechanism links free fatty acids released by lipases of Malassezia in about 50% of skin samples. This micro‐inflammation takes place in
with an inflammatory cascade and epidermal hyperproliferation.[54] the upper third of the HF, where a great number of microorganisms
A vast majority of studies on microbiome in dandruff and seborrheic are harboured. Moreover, porphyrins stimulating the production of
dermatitis searched for disturbances among yeast communities and complement and produced by Cutibacterium spp. were identified in
disease development, but not all of them found such correlations. the pilosebaceous duct of 58% of patients with AGA compared to
According to Park et al. and McGinley et al., the level of Malassezia 12% of the control group. These arguments together with observed
increases in dandruff 1.5 to 2 times the normal level, but Soares et al. improvement after application of antimicrobial agents may suggest
found no difference compared to the healthy scalp.[49,55,56] Findings a possible connection with scalp microflora.[59] Interestingly, many
of Xu et al. suggested that different strains of M. restricta can have patients presenting with acute episodes of AGA also exhibit features
either positive or negative relationship with dandruff.[44] In recent of seborrheic scalp dermatitis.[60]
studies, other fungal species such as Filobasidium spp. were found to
be potentially connected with this disease entity.[49,56]
6.4 | Scalp psoriasis
Alterations in bacterial microbiome have also been postulated to
play a significant role in dandruff formation. Underrepresentation of Psoriasis is a chronic T cell‐mediated disorder, probably develop‐
Cutibacterium spp. and higher abundance of Staphylococcus spp. are ing as a result of a combination of genetic background and external
considered to be strongly correlated with disease severity.[44,48,57] triggering factors, such as drugs, microorganisms and stress.[61] The
Moreover, bacteria such as Hymenobacter and Deinococcus may predominant species in scalp swabs taken from patients with pso‐
be responsible for symptoms, such as itching or burning, accom‐ riasis were M. globosa, M. furfur or M. restricta according to different
[57]
panying the course of dandruff and seborrheic dermatitis. studies.[61‒65] The rate of positive cultures of Malassezia species was
According to some researchers, not particular bacterial or fungal higher in psoriatic scalp lesions compared to healthy controls.[61,62,66]
species, but the imbalance between them contributes to disease Changes of the scalp microbiome were also found to depend on
development.[42,48,56,57] disease severity. Gomez‐Moyano et al. identified M. restricta as
the most frequent in mild scalp psoriasis, and M. globosa in moder‐
ate, and severe cases, and in patients with exacerbation in the last
6.2 | Folliculitis decalvans
month.[61] Cases of refractory scalp psoriasis successfully treated
Folliculitis decalvans is a type of primary cicatricial alopecia with with imidazole, followed by reduction of yeasts, were presented
unclear pathophysiology. The arguments for a connection of bac‐ and support the theory of a role of Malassezia as an exacerbating
terial communities with disease development are based on the factor in scalp psoriasis.[67] The release of cytokines through TLR2,
fact that S. aureus is often cultured from swabs taken from lesions, upregulation of transforming growth factor beta 1 in keratinocytes,
and there is a temporary good response to antimicrobial treatment complement activation and neutrophil recruitment are listed among
[11]
in most cases. Furthermore, biofilm‐like structures consisting immunological processes induced by yeasts, which may stimulate a
of C. acnes were identified within HFs in biopsy samples (species flare of psoriasis.[61]
confirmed by in situ hybridization), and within plucked HFs (spe‐ Microbiome of psoriatic lesions, including the scalp, also fea‐
cies of bacteria suspected based on their morphology) of some tures an increased bacterial diversity with a relative enrichment of
(A) (B) (C) and subsequent hair loss. Since the stem cells are spared, re‐entry
into the regular hair cycle and hair regrowth occurs after the in‐
flammation resolves. Factors triggering this autoimmune reaction
remain unknown.[14] Skinner et al.[71] found cytomegalovirus DNA
sequences in paraffin‐embedded sections taken from AA foci and
suggested a role of this virus in triggering the disease. Subsequent
(D) (E) (F)
studies did not confirm this finding.[72]
A possible connection between colonization of the scalp by
Alternaria spp. and AA development was postulated. Fungi of this
genus were cultured from epidermal scrapings in 20% of patients
compared to 13.3% of controls.[73,74] Not only skin but also gut mi‐
(G) (H) (I) crobiome has recently been considered to be associated with AA.
An increased intestinal permeability due to dysbiosis and/or inflam‐
mation may be an underlying stressor of the immune system in ge‐
netically susceptible individuals. Low production of short chain fatty
acids by intestinal bacteria as a result of insufficient intake of fibres
in “Western diet” is likely to disadvantage the intestinal barrier and
F I G U R E 3 Collapse of the immune‐privileged status of the
function of colonic Tregs, which as mentioned above, is important
hair follicle results in the development of alopecia. HFs of the
healthy scalp (A: macrophotograpy; B: trichoscopy, Photofinder; regulators of the immune system.[75] Two cases of AA with long‐term
C: histopathology) display two immune‐privileged areas, the stem hair regrowth after faecal microbiota transplants support a role of
cell‐bearing bulge and bulb. Collapse of this status within the bulge the intestinal microbiome.[76]
results in its destruction (F: histopathology) and development of A higher prevalence of atopic dermatitis in patients with AA
scarring alopecias such as lichen planopilaris (D: macrophotograpy)
compared to population prevalence, and its association with more
with typical follicular casts, subsequent disappearence of hair
severe course of AA, encourage to seek common pathomechanisms
follicle openings and progressive permanent hair loss (scarring
alopecia) seen under trichoscopy (E: Photofinder). In contrast, of the diseases.[77] According to recent studies, dysbiosis with over‐
inflammation in AA (G: macrophotography) is predominantely growth of S. aureus and decreased quantity of commensals such as
located around the bulb (I: histopathology) and leaves the stem cell Cutibacterium, Corynebacterium or Streptococcus can influence the
niche intact. As a result, the capacity of the hair follicle to produce severity of atopic dermatitis. Superantigens, proteases and other
hair fibres remains reserved and hair growth is re‐established after
toxins produced by S. aureus, and direct interaction of bacteria with
stabilization of the disease (non‐scarring alopecia presenting yellow
dots under trichoscopy) (H: Photofinder) immune cells, contribute to inflammation and skin barrier dysfunc‐
tion.[78] We hypothesize that abnormal composition of skin microbi‐
ome, including microbiome of the HF, may also be present in patients
S. aureus compared to controls. It has been demonstrated in a mu‐ with AA and result in a local immune response disturbing the im‐
rine model that this type of bacteria triggers Th17 immune response, mune‐privileged area of the bulb. In addition, defective skin barrier
which is also overactive in patients with psoriasis. Therefore, a po‐ in atopic dermatitis may ease microbial penetration to deeper follic‐
tential capability of S. aureus to influence psoriasis development is ular compartments.
currently of interest.[68]
Furthermore, alterations in the composition of gut microbiome
have been observed in patients with psoriasis. A decrease in phy‐ 7 | S U M M A RY A N D CO N C LU S I O N S
lum of Actinobacteria, which includes Bifidobacterium species of a
known immunosuppressive activity, and perturbations in the bal‐ So far, very few studies have explored deeper parts of the termi‐
ance of Firmicutes and Bacteroidetes, along with recent findings of nal scalp HF. Only Matard et al. presented images of structures that
an increased intestinal permeability, supports a new concept of a might be bacilli biofilm located below the infundibular part.[10‒12] If
[5,69,70]
“gut‐skin axis” in psoriasis. bacteria colonize normal scalp structures of HF deeper than the in‐
fundibulum, shifts in their composition might have an impact on the
collapse of the immune‐privileged status of specific compartments
6.5 | Alopecia areata
of the HF. Such disturbance of the HF immune system has direct
Alopecia areata is a type of non‐scarring alopecia considered to be implications for the regular hair cycle and substantial impact on the
of autoimmune origin. In contrast to the cicatricial alopecias, in‐ clinical manifestation of a disease, namely permanent loss vs preser‐
flammation targets deeper parts of the HFs leading to disruption vation of the HF (Figure 4). For scarring alopecia such as FD or lichen
of the immune privilege found around the bulbs of anagen HFs. planopilaris, the bulge area would be a place of interest, whereas
Inflammation and the invasion of cytotoxic T cells (Figure 3) during for AA changes in the microbiome of the peribulbar area could be
the growth phase lead to premature entry of the follicle into catagen a triggering factor.[13,79] Furthermore, microbiome‐host interactions
may aggravate scalp disorders, in which inflammation takes place in barrier. With regard to the unique juxtaposition of immune‐acti‐
superficial compartments of the HF. In addition, the type of micro‐ vated and immune‐privileged sites, the increasing evidence for a
organism as well as characteristics of the skin barrier of the host regulatory role of microbiota colonization on the hair cycle and its
may facilitate microbe penetration along the root sheaths towards key role as stem cell niche could have wider implications for our un‐
deeper compartments. As an example, atopic predisposition is asso‐ derstanding of the skin as barrier organ.
ciated with impaired skin barrier function. It frequently manifests in Such insights would further help develop more effective ther‐
very minor forms at a subclinical level. Presence of atopy, however, is apeutic strategies against chronic inflammatory scalp diseases, a
associated with a more severe course of AA.[80] Similarly, epidermal field of multiple unmet clinical needs. The possibility to reach both,
barrier disturbance can be found as secondary event after inflamma‐ the microorganism and the target site of inflammation, by topical
tion caused by other factors. application of drugs opens perspectives for a whole range of new
In conclusion, a better understanding of microorganism distribu‐ therapeutic options. Advanced delivery technologies based on parti‐
tion and penetration in healthy and diseased scalp HFs may yield cle‐based drug delivery systems allow for targeted deposition of ac‐
profound new insights in host‐microbe interactions across the skin tives in HFs and form drug reservoirs over time.[81] Thus, loading with
actives directed to specific microbiome changes observed in those
diseases could open new therapeutic options for those chronic dis‐
eases with high psychosocial impact on the affected individuals.[82]
Due to the fact that topical drugs can be delivered to and via HFs,
there is a question of potential influence of microbes residing in HFs
on their transport. At this point, it is largely unknown how the infun‐
dibular environment influences penetration processes. For example,
physical properties of microbial colonies like their size, consistency,
permeability for molecules or building a biofilm structure may play
a role.[83] Moreover, substances released by microorganisms such as
enzymes, toxins or AMPs, or direct interactions between microbes
and drug particles, may facilitate or hamper follicular transport, and
be worth studying to optimize this method.[33]
C O N FL I C T O F I N T E R E S T
The authors have declared no conflicting interests.
AU T H O R C O N T R I B U T I O N S
KPW, AV, UBP and LR drafted the manuscript and designed the fig‐
ures. All the authors have read the manuscript and have approved
this submission.
METHODS
F I G U R E 4 Microbiota connected with scalp diseases.
Selected literature was mainly recovered from the US National
Involvement of microbiota in scalp disease pathogenesis can
potentially occur on different levels, but at this point, clear Library of Medicine National Institutes of Health (PubMed data‐
connections have only been made to certain diseases. For example, base). There were no limits on the age of sources. Searched MeSH
pro‐inflammatory effects of yeast (purple) via lipase‐mediated Terms were as follows: “microbiota/ bacteria/ fungi/ viruses/ mites/
release of free fatty acids from sebaceous triglycerides have biofilms,” “scalp/ hair follicle/ skin,” “immune system/ immunity,” “na‐
been described in dandruff/seborrheic dermatitis.[54] Especially,
noparticles,” “inflammation,” “alopecia/ areata/ psoriasis/ dermatitis,
unsaturated free fatty acids can stimulate inflammation and
epidermal hyperproliferation (1), but yeasts may further stimulate seborrheic/ dandruff/ scarring” and “immune privilege”. Additional
psoriasis flare‐ups by induction of cytokines release, complement sources were obtained from references of analysed publications and
activation and neutrophil recruitment (2).[61] S. aureus (blue) is hand‐searching of relevant papers that were not found in PubMed
often cultured from pustules and erosions in FD (3), but may also database.
contribute to pro‐inflammatory or immunoregulatory environment
in other diseases, for example by triggering Th17 immune response
in psoriasis (4),[11,68] more interdisciplinary research in such ORCID
direction may reveal new mechanisms by which external microbiota
in this specific anatomical niche influence skin microenvironment Annika Vogt https://orcid.org/0000-0001-9134-8413
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Experimental Dermatology - 2019 - Polak Witka - The Role of The Microbiome in Scalp Hair Follicle Biology and Disease

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Received: 1 October 2018 | Revised: 2 March 2019 | Accepted: 18 March 2019

The role of the microbiome in scalp hair follicle biology and

Katarzyna Polak‐Witka1,2 | Lidia Rudnicka2 | Ulrike Blume‐Peytavi1 | Annika Vogt1

2 | S C A LP H A I R FO LLI C LE A S A D I S TI N C T In contrast to the massive exposure to microbial material in its

The authors have declared no conflicting interests.

REFERENCES Zheng, B. P. Hodkinson, D. Artis, E. A. Grice, Microbiome 2018, 6,

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