Review

An Overview of the Skin Microbiome, the Potential for Pathogen

Shift, and Dysbiosis in Common Skin Pathologies
Anita Smith 1,2,3,4,5, *, Roberta Dumbrava 4 , Noor-Ul-Huda Ghori 1,6 , Rachael Foster 1,2,4,5 , James Campbell 7 ,
Andrew Duthie 7 , Gerard Hoyne 8,9 , Marius Rademaker 10 and Asha C. Bowen 1,2,3,11

1 Healthy Skin Team, Wesfarmers Centre of Vaccines and Infectious Diseases, The Kids Research Institute
Australia, Perth, WA 6009, Australia
2 Perth Children’s Hospital, Perth, WA 6009, Australia
3 School of Medicine, University of Notre Dame, Fremantle, WA 6160, Australia
4 Sir Charles Gairdner Hospital, Perth, WA 6009, Australia
5 Department of Dermatology, Fiona Stanley Hospital, Perth, WA 6150, Australia
6 Division of Infection and Immunity, School of Biomedical Sciences, University of Western Australia,
Perth, WA 6009, Australia
7 Central Perth Skin Clinic, Perth, WA 6000, Australia
8 Institute of Respiratory Health, QEII Medical Centre, Perth, WA 6009, Australia
9 School of Health Sciences, University of Notre Dame, Fremantle, WA 6160, Australia
10 Clinical Trials New Zealand, Hamilton 3204, New Zealand
11 Division of Paediatrics, School of Medicine, University of Western Australia, Perth, WA 6009, Australia
* Correspondence: anita.smith2@health.wa.gov.au; Tel.: +61-8-6457-3333

Abstract: Recent interest in the diverse ecosystem of bacteria, fungi, parasites, and viruses
that make up the skin microbiome has led to several studies investigating the microbiome in
healthy skin and in a variety of dermatological conditions. An imbalance of the normal skin
flora can cause some skin diseases, and current culture techniques are often unable to detect
a microorganism to further our understanding of the clinical–microbiological correlates
of disease and dysbiosis. Atopic dermatitis and rosacea are presentations that GPs often
manage that may have an infective or microbiological component and can be challenging
to treat. We aim to discuss the implications of the skin microbiome including the impact of
Academic Editor: Pabulo Rampelotto dysbiosis on conditions such as these. We will also discuss some clinical pearls for initial
Received: 5 December 2024 and future directions of the management of conditions such as atopic dermatitis, rosacea,
Revised: 22 December 2024 and hidradenitis suppurativa. Further research using culture-independent techniques is
Accepted: 27 December 2024 needed for conditions involving microbial dysbiosis to advance our knowledge of skin
Published: 1 January 2025
disease pathophysiology and guide future management.
Citation: Smith, A.; Dumbrava, R.;
Ghori, N.-U.-H.; Foster, R.; Campbell, Keywords: skin microbiome; atopic dermatitis; rosacea; hidradenitis suppurativa
J.; Duthie, A.; Hoyne, G.; Rademaker,
M.; Bowen, A.C. An Overview of the
Skin Microbiome, the Potential for
Pathogen Shift, and Dysbiosis in
Common Skin Pathologies.
1. Introduction
Microorganisms 2025, 13, 54. The skin microbiome is a diverse ecosystem composed of bacteria, fungi, and viruses;
https://doi.org/10.3390/ however, compared to other body sites, it has a very low biomass due to its nutrient-poor,
microorganisms13010054
exposed, and dry environment compared to the respiratory or gastrointestinal tracts [1,2].
Copyright: © 2025 by the authors. The skin microenvironment has distinct physical–chemical properties of three major types,
Licensee MDPI, Basel, Switzerland. sebaceous (oily), dry, and axillae/follicular (moist), across the surface of the body and can
This article is an open access article
therefore pose significant challenges to scientists in accurately sampling and characterising
distributed under the terms and
the microbial composition within these regions. Skin microbiome studies to inform the
conditions of the Creative Commons
Attribution (CC BY) license
diagnosis and treatment of common dermatoses have focussed on bacterial species to date.
(https://creativecommons.org/ Whilst viruses and fungi may contribute, our review will predominantly feature bacterial
licenses/by/4.0/). understandings that aid in diagnosis and treatment.

Microorganisms 2025, 13, 54 https://doi.org/10.3390/microorganisms13010054

Microorganisms 2025, 13, 54 2 of 13

Over the past two decades, there have been numerous studies highlighting the im-
portance of the skin microbiome in health and disease. The Human Microbiome Project
Consortium found that the diversity and abundance of each habitat’s signature microbes
among healthy subjects vary widely [3]. Further studies provided a framework for human
microbiome research [4]. Oh et al. [5] identified strain-level variation in dominant species
on the skin as heterogenous and multiphyletic, forming a foundation for human disease
studies investigating inter-kingdom interactions, metabolic changes, and strain tracking.
Specifically in regard to eukaryotic organisms (such as Malassezia and Demodex) in
the skin, these are reduced in abundancy compared to bacteria. Demodex predominantly
resides in hair follicles and is an arachnid-genus, eight-legged mite [6]. Demodex are
sebum-consuming mites (obligate human ecto-parasites), which are typically found in
facial regions classically associated with rosacea. In cases of rosacea, skin samples have
demonstrated higher frequencies of the demodex mite species when compared to control
skin [7,8]. Research has also proposed that Demodex mites and their associated bacteria
upregulate proteases that are linked to the further dysregulation of the cutaneous innate
immune response [9]. In terms of the fungal components of the skin microbiome, these are
unique in that there is predominantly Malassezia, a single fungus, in the skin mycobiome. It
has been suggested that given this lack of diversity, Malassezia may outcompete other fungi
from living on the skin [10]. Hypersensitivity to Malassezia furfur (yeast found naturally
on the skin of humans) can result in a flare of atopic dermatitis on the head and neck,
with Malassezia-directed treatment controlling the disease. Systematic reviews of the skin
microbiome in patients with atopic dermatitis have found that there is a depletion of
Malassezia spp. and high non-Malassezia fungal diversity [11]. Other systematic reviews [12]
on seborrheic dermatitis have shown that the predominant fungi on the face and scalp
were predominantly the fungi of Ascomycota and Basidiomycota. Additionally, there was an
increased ratio of Malassezia restrica/Malassezia globosa in the setting of seborrheic dermatitis.
Currently, there is little information regarding the skin virome. Studies have described
eukaryotic DNA viruses to be unique not to the site, but to the individual [13].
Most available protocols for microbial characterisation are based on those originally
developed to analyse the high-biomass, high-diversity gut microbiome [14]. Low-biomass
samples are susceptible to contamination from environmental sources in comparison to
samples with a high deoxyribonucleic acid (DNA) microbial biomass, for example, faecal
samples that are less likely to have issues with contamination during processing leading
to false positives that have a reduced likelihood of other biases [15–17]. Until as recently
as twenty years ago, methods of investigating human skin microbes relied primarily on
culture-based techniques [1].
These initial culture studies found that the main skin bacterial genera included Staphy-
lococcus, Cutibacterium (formerly Propionibacterium), Corynebacterium, and fungi such as
Malassezia [1,18]. The challenge with traditional culture-based methods in a low-biomass
environment is that not all microbes on the skin are able to be grown via culture techniques,
creating a sampling bias, with the microbial richness of the skin being underestimated [19]
and with some microbes not surviving once removed from the skin microenvironment [1].
There are several advantages of utilising 16S ribosomal ribonucleic acid (rRNA) gene
sequencing techniques, including (i) the ability to reveal the presence of a large number
of individual bacterial phyla; (ii) the ability to study the microbiome of particular skin
diseases; (iii) the low cost compared to other sequencing methods; and (iv) the ability to
avoid sequencing host DNA [19]. However, molecular techniques (e.g., amplicon-based)
used for microbiome analysis are also limited in that short-read sequences are unable to
provide accurate information about species or strains of microorganisms on the skin [1]
and are highly dependent on the sampling and DNA extraction methods used. Other
Microorganisms 2025, 13, 54 3 of 13

challenges include the multiple layers associated with the skin and the uneven species
distribution on its surface [14].
Several sampling methods for investigating the skin microbiome have been described
in recent years [20–22]. Cotton swabs and skin scrapings give rise to comparable skin
microbiota profiles, representative of those obtained with skin biopsies, a technique often
used in dermatology clinical practice to further evaluate for deeper skin infection and
disease pathogenesis [20]. Tape stripping and scraping have also been reported in the
literature but are suboptimal for skin microbiome analysis [22]. The use of adhesive patch
sampling has been reported to be effective, well tolerated and non-invasive [23]; however,
adhesive patch-based skin biopsy devices are difficult to procure and are not currently
commercially available for clinical use. More invasive approaches including skin punch
biopsies have been used to analyse the follicular skin microbiome using 16S rRNA and
18S rRNA sequencing [24]. The disadvantages of punch biopsies include that they are
an invasive procedure that usually requires suturing, can leave a scar, which may be
problematic if one wants to sample sites on the face (forehead, nose), and may not be
appropriate for sensitive sites (such as axillae or the groin) [25]. Bjerre et al. previously
compared flocked swabs vs. skin scrapings in adults, reporting that 99.3% of the sequences
overlapped [14].
Further research using culture-independent techniques are needed for conditions
involving microbial dysbiosis and to advance our knowledge of skin diseases, wound
healing, and sepsis prevention. Dysbiosis describes the changes that occur in the microbiota,
which promote the overgrowth of pathogenic species. The means by which local species
establish specific niches on the skin and how they interact and alter the relative success
of specific microbes represent a possible explanation for dysbiosis. Such changes are
implicated in a range of skin conditions, several of which are commonly encountered
in general practice, including atopic dermatitis, rosacea, and hidradenitis suppurativa,
whereby antibiotics are commonly prescribed in management yet are often ineffective.
Specifically, these three diseases have been chosen to represent different skin zones (e.g.,
sebaceous (rosacea), follicular (hidradenitis suppurativa), and dry (eczema)). Studies have
shown that during a flare of atopic dermatitis, there is a decrease in bacterial diversity
and an increase of approximately 35–90% in the proportion of the bacteriome made up of
Staphylococcus spp. [26]. In hidradenitis suppurativa, studies have reported an increased
(relative) abundance of certain anaerobic bacteria (such as Peptoniphilus spp., Prevotella,
and Porphyromonas) in lesional skin in contrast to control or non-lesional skin. The relative
abundance of anaerobic bacteria and the increase in the diversity of bacteria were also
shown to correlate positively with the severity of hidradenitis suppurativa [27].
Compared to cotton swabs, flocked swabs have been shown to generate superior DNA
extraction yields and are more suitable for direct polymerase chain reaction (PCR) [28–30].
Manus et al. [21] analysed 16S rRNA bacterial gene sequencing from swab samples taken
from the axilla, hand, and forehead of 47 infants and found that the bacterial diversity
and composition were shaped by skin site, age, socioeconomic factors, and household
composition. The tip of a flocked swab is like a brush, allowing more surface area com-
pared to cotton swabs and an ability to collect more material. The brush-like tip also
enables the superior specimen collection and release of DNA during testing. To date,
there is no established standard sampling method that produces unbiased results for skin
microbiome studies.
Overall, further studies to optimise the molecular detection of bacteria from skin with
standardised methods for sampling [1] are required to inform a broader understanding of
skin health and skin disease and the complexity of its role in dysbiosis.
Microorganisms 2025, 13, 54 4 of 13

2. Methodology
A literature search using a narrative review style was performed to identify relevant
articles to provide an overview of the skin microbiome, the natural resistance of skin,
commensal organisms at different sites, and evidence to further outline the role of dysbiosis
in atopic dermatitis, rosacea, and hidradenitis suppurativa.

2.1. Natural Resistance of Skin to Infection Including Barrier and Innate Defences
The skin functions as a physical barrier preventing infection, whilst also allowing a
habitat for commensal organisms [31,32]. The skin constantly encounters pathogens, and
to avoid infection, the dermis and epidermis have developed multiple innate defences such
as antimicrobial peptides, including β-defensins, skin neuropeptide (substance P), and
cathelicidins [31,32]. Many of these peptides have anti-bacterial, anti-viral, and anti-fungal
activity in part due to their structural elements that allow the disruption of the microbial
membrane whilst allowing the human cell membranes to remain intact [32]. Some peptides
have a specific role in normal skin against certain microbes, whilst other peptides act when
the skin’s barrier is damaged [33]. For example, cathelicidin peptides are increased and
abnormally processed in rosacea [34] and in atopic dermatitis; a decreased expression of
antimicrobial peptides can lead to an increased infection risk. Other aspects of the skin’s
host defence include various cells such as natural killer cells, neutrophils, Langerhans cells,
and lymphoid cells.

2.2. Commensal Organisms at Different Sites

The skin microbiome varies depending on moisture content, pH, temperature, and
sebaceous gland concentration, in addition to other factors such as the exogenous environ-
ment and host genetics [32]. These can be represented by the sebaceous (oily) zone (e.g.,
Microorganisms 2025, 13, x FOR PEER REVIEW 6 of 16
forehead), the dry zone (e.g., volar forearm), and the moist zone (e.g., antecubital fossa,
axilla). Figure 1 highlights the microbiome differences throughout these zones [35].

Figure 1. Skin microbial communities by the microenvironment of the skin [27,35]. Four sites are
shown to represent the major microenvironments of the skin: face (forehead) (sebaceous/oily);
Figure 1. Skin microbial communities by the microenvironment of the skin [27,35]. Four sites are
antecubital fossa (moist); volar forearm (dry); and toe web space (foot). Bar graphs represent consensus
shown to represent the major microenvironments of the skin: face (forehead) (sebaceous/oily);
antecubital fossa (moist); volar forearm (dry); and toe web space (foot). Bar graphs represent con-
sensus relative abundances of the bacteria. The bacterial species Cutibacterium spp., Staphylococcus
spp., and Corynebacterium spp. are displayed in bar charts to highlight relative abundance, with
colours identified in the legend. Unlabelled species are grouped as ‘Other’. Figure adapted from
Microorganisms 2025, 13, 54 5 of 13

relative abundances of the bacteria. The bacterial species Cutibacterium spp., Staphylococcus spp., and
Corynebacterium spp. are displayed in bar charts to highlight relative abundance, with colours identi-
fied in the legend. Unlabelled species are grouped as ‘Other’. Figure adapted from [36]. Adaptation
and reproduction of figure permitted by Creative Commons Attribution 4.0 International License,
available from http://creativecommons.org/licenses/by/4.0/ (accessed on 26 December 2024).

The microbiota are involved not only as commensal microorganisms but also in epithe-
lial health and immune modulation [32]. Further research into these recently described roles
has the potential to allow greater insight into the pathophysiology of skin conditions such
as atopic dermatitis, as well as into the role of antimicrobial and promicrobial therapeutics
such as probiotics [37].
Skin microbiome studies sample multiple sites to allow for differences in the zones
of the skin. The most commonly employed sites used to sample and model the microbial
community are (1) wet/non-oily (antecubital fossa); (2) dry/non-oily (volar forearm);
(3) wet/oily (face-cheek/forehead); and (4) wet/oily (scalp) [38,39]. The toe web space is
unique but minimally investigated (Reynolds, 2023) [40]. The results of a study conducted
by our group [39] showed that in sampling the skin microbiome of three body sites,
namely, the cubital fossa, cheek, and axilla, there was marked interpersonal variability, with
each body site showing different taxa for each participant. In addition, this same study
also showed that the skin microbiome was relatively stable over longitudinal sampling,
maintaining temporal stability.

2.3. Pathogenicity of Bacteria and Potential for Commensal–Pathogen Shift

The main species of skin bacteria are Cutibacteria, Corynebacteriae, and Staphylococci [41].
There is a dynamic and rich interplay between these commensal organisms, many of which
can modulate pathogenicity. Some Cutibacterium spp., for example, promote the virulence
of Staphylococcus aureus [42]. Others, such as Corynebacterium striatus, have a “nurturing
effect” of sorts, changing S. aureus from a pathogen into a commensal [43]. Other species
such as Corynebacterium accolens act indirectly by making the local environment inhospitable
for Streptococcus pneumoniae [44].

2.4. Dysbiosis in Atopic Dermatitis

Atopic dermatitis (AD) is a chronic inflammatory condition caused by an impaired skin
barrier, dysregulated immunity, and microbial dysbiosis of the skin. The skin microbiome
plays a critically important role in epidermal homeostasis, with dysbiosis in the microbiome
being a contributing factor in the pathogenesis of atopic dermatitis [45]. The most prevalent
organism isolated in areas of active eczema is S. aureus, which has also been shown to
correlate with increased eczema flares [37]. A longitudinal study conducted in paediatric
populations with eczema found that an increased total quantity of S. aureus correlated with
greater disease severity during AD flares [37]. Hypersensitivity to Malassezia furfur (yeast
found naturally on the skin of humans) can result in a flare of AD on the head and neck,
with Malassezia-directed treatment controlling the disease. In addition, superantigens have
also been implicated, with the proposed role of superantigens being that they promote the
development of the Th2 immune response. In atopic dermatitis, up to 65% of S. aureus
strains that colonise patients with atopic dermatitis have exotoxins with superantigenic
properties [46].
Over 90% of patients with atopic dermatitis are colonised with S. aureus on their
skin, in comparison to 5% of patients without atopic dermatitis, which has been proposed
to reflect the decreased antimicrobial peptides (e.g., defensins, cathelicidins), disrupted
acid mantle, and altered cytokine profile of skin in atopic dermatitis [47]. Studies have
Microorganisms 2025, 13, 54 6 of 13

shown that during a flare of atopic dermatitis, there is a decrease in bacterial diversity
and an increase of approximately 35–90% in the proportion of the bacteriome made up
of Staphylococcus spp. [26]. Research has also shown that clinical improvement in atopic
dermatitis correlates with the normalisation of the microbial population [48].
From a management point of view, there has been evidence to suggest that a multi-
modal approach restores the skin bacteriome and reduces disease severity in AD. The use
of topical corticosteroids, antimicrobials, and bleach baths in combination decreased the
colonisation of S. aureus species and promoted further diversity in skin microbiota [49]. By
using a variety of therapeutic interventions (Table 1), management may be able to alter the
dysbiotic bacteriome in AD and restore it back to equilibrium.

Table 1. Management of atopic dermatitis based upon severity [32,50].

Mild Moderate Severe

Emollients: Apply moisturiser at
least daily in thick layer. Emollients: Apply moisturiser at
Moderate-strength topical least daily in thick layer.
corticosteroids, i.e., Potent topical corticosteroids (such as
methylprednisolone aceponate 0.1%, betamethasone dipropionate 0.05%)
Emollients: Apply moisturiser at for use until skin is pruritus-free and to affected areas on trunk and limbs.
least daily in thick layer. smooth, then reduce gradually to If non-responsive or symptoms
If unresponsive to use of regular minimum frequency that allows skin persist while on potent topical
moisturiser, recommend to be inflammation-free. steroids, refer to dermatologist.
mild–moderate-strength topical Facial or eyelid dermatitis To decrease severity during flares,
corticosteroids: treat until clear then maintenance (age > 3 months): wet wraps with topical
reduce frequency. pimecrolimus 1% cream corticosteroids are recommended.
Research suggests that daily recommended for patients who have Immune modulation with
application of some topical not had satisfactory control with use phototherapy, methotrexate,
corticosteroids is adequate; however, of intermittent topical corticosteroid ciclosporin, mycophenolate, and
topical corticosteroids twice daily is or where topical steroid is azathioprine may be indicated in
usually recommended for AD. contra-indicated. severe disease (refer
To prevent recurrent skin infections: Consider referral to dermatologist if to dermatologist).
dilute bleach baths (details below). no improvement. New management options such as
To prevent recurrent skin infections: dupilumab and JAK inhibitor,
dilute bleach baths (details below). upadacitinib, can be accessed via
Oral antibiotics (e.g., cephalexin)—if dermatologists in patients meeting
clinically impetiginised, or anti-virals PBS criteria.
if Herpes Simplex is present.

2.5. General Skin Care Measures for Atopic Dermatitis

Bath or shower once a day using warm (not hot) water and keep it short (5–10 min).
Avoid using soap.
A bath oil can be added to the bath and a soap-free wash can be used if required.
Care must be taken with bath oil use in older children as it can make the bath
very slippery.
The use of non-soap cleansers is recommended (i.e., soap-free wash or a soap substitute).
After bathing/showering, pat-dry the skin and apply moisturiser over the whole body
and face.
Emollients (such as lanolin and glycerol stearate) are products used to smooth and
soften the skin.
Avoid scratching the skin and keep the nails trimmed short.
Avoid triggers to prevent flares of AD. These include soaps, shampoos, shower gels
and bubble baths, prickly or rough clothing (including wool), overheating, overdressing,
Microorganisms 2025, 13, 54 7 of 13

sweat, friction, direct contact with grass and sand, prolonged exposure to chlorine and salt
water, or emotional stress.

2.6. Dysbiosis in Rosacea

Rosacea is a chronic inflammatory disease, which typically presents with facial flushing,
persistent centrofacial erythema, telangiectasia, and inflammatory pustules. The relationship
between dysbiosis and rosacea is thought to involve several organisms, namely, Demodex spp.,
Bacillus oleronius, S. epidermidis, and Cutibacterium acnes [50]. Demodex are a family of sebum-
consuming mites (obligate human ecto-parasites), which are typically found in facial regions
classically associated with rosacea. In cases of rosacea, skin samples have demonstrated higher
frequencies of the demodex mite species when compared to control skin [7,51]. Research has also
proposed that Demodex mites and their associated bacteria upregulate proteases that are linked
to the further dysregulation of the cutaneous innate immune response [9]. The pathophysiology
of this disease is a complex interplay, which interacts with barrier dysfunction and can lead to a
decreased tolerability to skincare products in this patient cohort.
Whilst erythematotelangiectatic rosacea and seborrhoea are often treated with topical
vasoconstrictors, pulse dye laser/intense pulsed light or topical retinoids respectively,
the papulopustular flares of rosacea are associated with dysbiosis. Rosacea responds
well to topical metronidazole 0.75% for 12 weeks but often recurs. Topical ivermectin 5%
cream, a topical antiparasitic ointment, has been used in studies to decrease the burden
of demodex mites, with clinical improvement in rosacea [49,52,53]. Bacillus oleronius, a
Gram-negative non-commensal bacterium, has been isolated from Demodex mites and has
been proposed as a possible inflammatory trigger in rosacea mediated through neutrophil
activation [54]. Studies have demonstrated that this Gram-negative bacterium is susceptible
to many antibiotics in conjunction with other therapies (Table 2) used to treat rosacea, and
may well explain the link with dysbiosis [55]. While the previous mechanism of action
for antimicrobial therapy in rosacea was presumed to be anti-inflammatory, there is a
suggestion from these studies that antimicrobial effects are also exerted.

Table 2. Treatment options for rosacea subtypes (Australia/New Zealand Algorithm) [56] (reproduced with
permission on behalf of the Australasian Medical Dermatology Group). Rademaker M. Medical Management
of Rosacea—an Australian/New Zealand Medical Dermatology narrative. Presented at The Australasian
College of Dermatologists 55th Annual Scientific Meeting; 28 May 2023; Sydney, Australia [57].

Treatment Options for Rosacea Subtypes

Phenotype Erythema Papules and/or Pustules Phyma
Non-
Transient Persistent Telangiectasis * Mild Moderate * Severe * Inflamed
Inflamed
Start one of
Start one of Start one of
topical Start one of Start one of Start one of
topical Trial one of doxycycline
brimonidine topical topical Doxycycline
Starting brimonidine IPL or Ablative
gel azelaic acid azelaic acid or
Rx gel Laser low-dose laser *
or ivermectin ivermectin low-dose
or oxymeta- RF isotretinoin
oxymetazoline metronidazole metronidazole isotretinoin *
zoline cream *
cream
Add in
another
Add in a
Try a topical:
physical Low-dose
different azelaic acid
Add in therapy *: isotretinoin * Surgical
Inadequate physical or
oral IPL 3/12 of or curettage *
response therapy *: ivermectin or RF *
β-blocker or Laser doxycycline hydroxychloroquine * or
at 3/12 * IPL metronidazole
clonidine RF or RF *
Laser Consider
Consider RF *
RF topical
BoNTA *
BPO or
retinoid
Microorganisms 2025, 13, 54 8 of 13

Table 2. Cont.

Treatment Options for Rosacea Subtypes

Phenotype Erythema Papules and/or Pustules Phyma
Non-
Transient Persistent Telangiectasis * Mild Moderate * Severe * Inflamed
Inflamed
Oral ivermectin or
Consider treating low-grade inflammation
with Low-dose
Consider short-course
Next step low-dose isotretinoin * isotretinoin *
systemic Rx systemic steroids *
or RF *
or
hydroxychloroquine for 12 months *
dapsone *
Maintenance
Continue topical Rx if it was effective, Switch to topical Rx if possible, or continue low-dose Continue low-dose
(12
repeat physical therapy when appropriate isotretinoin * isotretinoin *
months)
IPL (intense pulsed light); RF (fractional radiofrequency); Rx (therapy/medication); BoNTA (Botulinum toxin
type A); BPO (benzoyl peroxide). * Referral to a dermatologist recommended.

2.7. Dysbiosis in Hidradenitis Suppurativa

Hidradenitis suppurativa (HS) is a chronic condition of the apocrine pilosebaceous
unit with evidence of some role of dysbiosis [58]. As with rosacea, when compared with
healthy controls, individuals with HS have lower counts of Cutibacterium acnes, possibly due
to an associated disease-promoting disruption of the bacteriome, and a higher number of
anaerobic Gram-negative bacteria [58,59]. Specific organisms may play a role, with lesions
found to have a higher count of Corynebacterium, Porphyromonas, and C. peptoniphilus [24]. In
addition, studies have reported an increased (relative) abundance of certain anaerobic bacte-
ria (such as Peptoniphilus spp., Prevotella, and Porphyromonas) in lesional skin in hidradenitis
suppurativa in contrast to control or non-lesional skin. The relative abundance of anaerobic
bacteria and the increase in the diversity of bacteria were also shown to correlate positively
with the severity of hidradenitis suppurativa [27].
The use of targeted antibiotics to induce HS remission in patients with syndromic
disease forms has been documented and forms an important part of HS management
(Figure 2). Syndromic forms associated with HS include PASH (pyoderma gangrenosum,
acne conglobata, and suppurative hidradenitis) and PAPASH (pyogenic arthritis, pyoderma
gangrenosum, acne, and suppurative hidradenitis) when HS presents as part of other
inflammatory disorders. There are currently two biologic treatments that are FDA-approved
for HS for treatment by a dermatologist. These are secukinumab (an interleukin-17A
inhibitor) and adalimumab (an antibody targeting tumour necrosis factor-alpha) [60].
These biologic agents form management options for those with moderate-to-severe disease
(Figure 2), and previous non-response/allergy/adverse reactions to two different courses
of antibiotics, each for 3 months [61].
The formation of sinus tracks/tunnels and scarring in HS is likely part of the reason for
an abnormal microbiome. The pathophysiology of hidradenitis suppurativa initially starts
with follicular occlusion in areas of friction with skin rubbing on skin (e.g., axillae, groin) in
addition to the hyperkeratinisation and dilatation of the follicles [62]. From here, bacteria
and keratin are released into the dermis following the rupture of the follicle. Abscess
formation can then be seen with profuse inflammatory responses. Immune dysregulation
in hidradenitis involves a variety of chemokines and cytokines including IL-17, TNF,
IL-1 α/β, G-CSF, and IL-6 [63,64]. From here, tissue is damaged via recruited neutrophils
and associated neutrophil extracellular traps, reactive oxygen species, the involvement of
pro-inflammatory cytokines, and the activation of the complement cascade (e.g., C5a, C3a)
from recruited macrophages. Overall, tunnels and the generation of epithelial strands form
from the rupture of the follicular epithelium and matrix metalloproteinases (degrading
enzymes). Targeting the microbiome in patients with HS is a logical therapeutic option,
Microorganisms 2025, 13, 54 9 of 13

Microorganisms 2025, 13, x FOR PEER REVIEW 11 of 16

and a greater understanding of skin microbiota may very well lead to a more precise
therapeutic approach.

Figure 2. Hidradenitis suppurativa treatment based on Hurley Stage [32,45]. Flow diagram of
Figure 2. Hidradenitis
treatment suppurativa suppurativa
options for hidradenitis treatment based on on
based Hurley Stage
Hurley [32,44].
Stage. WLEFlow diagram
(wide of
local excision);
treatment options
I&D (incision andfor hidradenitis
drainage); suppurativa based on Hurley Stage. WLE (wide local excision);
IM (intra-muscular).
I&D (incision and drainage); IM (intra-muscular).
3. Conclusions
[60].
FutureThenovel
formation
work is of needed
sinus tracks/tunnels
to explore theand skinscarring in HSin
microbiome is clearly
likely part of the
defined in-
reason for an abnormal microbiome. The pathophysiology of hidradenitis
fectious diseases, in skin diseases that are exacerbated by infection, e.g., eczema, and insuppurativa
initially starts with
skin diseases follicular
that are treatedocclusion in areasantibiotics
with long-term of friction with skin
for the rubbing on
presumed butskin (e.g.,
currently
axillae, groin) in addition to the hyperkeratinisation and dilatation of the follicles
poorly defined role of bacterial pathogenesis, e.g., hidradenitis suppurativa. Understanding [61].
From
normalhere,
skinbacteria andhelp
flora will keratin arehow
define released into the
microbial dermis following
imbalance the rupture
may be associated ofskin
with the
follicle. Abscess formation can then be seen with profuse inflammatory responses.
disease and skin healing. This will be invaluable in populations with a high burden of skin Im-
mune dysregulation in hidradenitis involves a variety of chemokines and cytokines in-
cluding IL-17, TNF, IL-1 α/β, G-CSF, and IL-6 [62,63]. From here, tissue is damaged via
recruited neutrophils and associated neutrophil extracellular traps, reactive oxygen
Microorganisms 2025, 13, 54 10 of 13

disease (e.g., children living in remote Indigenous communities in Australia who have the
highest reported rates of impetigo in the world [65]). Future studies could also have wider
implications for health in terms of the skin–gut microbiome axis and an impact on systemic
infection and disease states [66].
In addition, skin microbiome protocols could be utilised to evaluate microbial dysbio-
sis in dermatological conditions (e.g., atopic dermatitis, papulopustular rosacea, hidradeni-
tis suppurativa), the changes in the skin microbiome with biological therapies such
as dupilumab in atopic dermatitis, and the impact on the skin microbiome in healing
and burns.
Once skin microbiome protocols are optimised, future research could also further
investigate the interplay between the skin and gut microbiota. Recent research into the
“gut–skin axis” shows that connections between the skin and gut microbiota can influence
both an individual’s likelihood of developing AD and the severity of disease after onset [67].
In rosacea, there is conflicting evidence in relation to the role of Helicobacter pylori and
rosacea. A recent meta-analysis did not find any improvement in the symptoms of rosacea
with H. pylori eradication or any statistically significant association between rosacea and
H. pylori infection [68].
Future research will be able to utilise optimised skin microbiome protocols in or-
der to further evaluate the composition of healthy/normal skin. Further research using
culture-independent techniques is needed for conditions involving microbial dysbiosis
(e.g., periorificial dermatitis, papulopustular rosacea, hidradenitis suppurativa). Temporal
shifts in the composition of the skin microbiome have been described in skin conditions
such as atopic dermatitis [26]. Future research aimed at understanding immune responses
to certain bacteria as well as therapeutic agents to target pathogens and dysbiosis may
offer novel treatment ideas for specific dermatological conditions. To understand these
conditions better, we need improved techniques that extend our understanding of microbi-
ology, from routine cultures to molecular techniques where the bacterial DNA signature
can be determined.
Future studies could use an intensive bacterial ‘culturomic’ approach to isolate difficult-
to-culture bacteria and to establish a repository of bacterial isolates, which we will use to
try to understand why some bacteria are associated with disease and others with healthy
skin. Developing high-quality protocols for the collection and testing of samples for skin
microbiome analysis would yield unique resources globally, representing the leading edge
of this emerging field.
It is evident that a lack of awareness about the diversity of the skin microbiome and
poor sampling has hindered our progress in understanding the role of dysbiosis in inflam-
matory skin disease. Further research is required to discern the impact of the therapeutic
actions of antibiotics and topical probiotics on the skin microbiome in inflammatory skin
conditions. There is, however, great potential in that these individualised treatments in
AD, rosacea, and HS may translate into targeted antimicrobial care, enhancing our future
management of such dermatological conditions.

Author Contributions: Conceptualization, A.S., R.D., A.C.B., R.F., G.H. and N.-U.-H.G.; Methodology
A.S., R.D., N.-U.-H.G., R.F., A.C.B. and G.H.; Writing original draft preparation A.S., R.D., R.F., A.C.B.,
M.R., J.C., A.D., N.-U.-H.G. and G.H.; writing review and editing A.S., R.D., R.F., M.R., A.C.B.,
N.-U.-H.G., G.H., J.C. and A.D.; supervision A.C.B. and G.H. All authors have read and agreed to the
published version of the manuscript.

Funding: This research received no external funding.

Data Availability Statement: No specific data were required in the preparation of this manuscript.
Microorganisms 2025, 13, 54 11 of 13

Acknowledgments: We would like to acknowledge the work of the Healthy Skin and Skin Mi-
crobiome Team at The Kids Research Institute, Australia, and, in particular, Eloise Delaney and
Megumi Joseph for their assistance with the creation of figures and tables and in the formatting of
this manuscript.

Conflicts of Interest: The authors declare no conflicts of interest.

References
1. Chen, Y.; Knight, R.; Gallo, R.L. Evolving approaches to profiling the microbiome in skin disease. Front. Immunol. 2023,
14, 1151527. [CrossRef] [PubMed]
2. Chen, Y.E.; Fischbach, M.A.; Belkaid, Y. Skin microbiota-host interactions. Nature 2018, 553, 427–436. [CrossRef] [PubMed]
3. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486,
207–214. [CrossRef] [PubMed] [PubMed Central]
4. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 2012, 486, 215–221. [CrossRef]
[PubMed] [PubMed Central]
5. Oh, J.; Byrd, A.L.; Deming, C.; Conlan, S.; NISC Comparative Sequencing Program; Kong, H.H.; Segre, J.A. Biogeography and
individuality shape function in the human skin metagenome. Nature 2014, 514, 59–64. [CrossRef] [PubMed] [PubMed Central]
6. Harris-Tryon, T.A.; Grice, E.A. Microbiota and maintenance of skin barrier function. Science 2022, 376, 940–945. [CrossRef]
[PubMed]
7. Roihu, T.; Kariniemi, A.L. Demodex mites in acne rosacea. J. Cutan. Pathol. 1998, 25, 550–552. [CrossRef]
8. Forton, F.M.N. The Pathogenic Role of Demodex Mites in Rosacea: A Potential Therapeutic Target Already in Erythematotelang-
iectatic Rosacea? Dermatol. Ther. 2020, 10, 1229–1253. [CrossRef] [PubMed]
9. Lacey, N.; Ní Raghallaigh, S.; Powell, F.C. Demodex mites--commensals, parasites or mutualistic organisms? Dermatology 2011,
222, 128–130. [CrossRef] [PubMed]
10. Tuor, M.; LeibundGut-Landmann, S. The skin mycobiome and intermicrobial interactions in the cutaneous niche. Curr. Opin.
Microbiol. 2023, 76, 102381. [CrossRef]
11. Bjerre, R.D.; Bandier, J.; Skov, L.; Engstrand, L.; Johansen, J.D. The role of the skin microbiome in atopic dermatitis: A systematic
review. Br. J. Dermatol. 2017, 177, 1272–1278. [CrossRef] [PubMed]
12. Tao, R.; Li, R.; Wang, R. Skin microbiome alterations in seborrheic dermatitis and dandruff: A systematic review. Exp. Dermatol.
2021, 30, 1546–1553. [CrossRef] [PubMed]
13. Oh, J.; Byrd, A.L.; NISC Comparative Sequencing Program; Kong, H.H.; Segre, J.A. Temporal stability of the human skin
microbiome. Cell 2016, 165, 854–866. [CrossRef] [PubMed]
14. Bjerre, R.D.; Hugerth, L.W.; Boulund, F.; Seifert, M.; Johansen, J.D.; Engstrand, L. Effects of sampling strategy and DNA extraction
on human skin microbiome investigations. Sci. Rep. 2019, 9, 17287. [CrossRef] [PubMed]
15. Greathouse, K.L.; Sinha, R.; Vogtmann, E. DNA extraction for human microbiome studies: The issue of standardization. Genome
Biol. 2019, 20, 212. [CrossRef] [PubMed]
16. Eisenhofer, R.; Minich, J.J.; Marotz, C.; Cooper, A.; Knight, R.; Weyrich, L.S. Contamination in Low Microbial Biomass Microbiome
Studies: Issues and Recommendations. Trends Microbiol. 2019, 27, 105–117. [CrossRef] [PubMed]
17. Salter, S.J.; Cox, M.J.; Turek, E.M.; Calus, S.T.; Cookson, W.O.; Moffatt, M.F.; Turner, P.; Parkhill, J.; Loman, N.J.; Walker, A.W.
Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014, 12, 87.
[CrossRef] [PubMed]
18. De Pessemier, B.; Grine, L.; Debaere, M.; Maes, A.; Paetzold, B.; Callewaert, C. Gut-Skin Axis: Current Knowledge of the
Interrelationship between Microbial Dysbiosis and Skin Conditions. Microorganisms 2021, 9, 353. [CrossRef]
19. Santiago-Rodriguez, T.M.; Le François, B.; Macklaim, J.M.; Doukhanine, E.; Hollister, E.B. The Skin Microbiome: Current
Techniques, Challenges, and Future Directions. Microorganisms 2023, 11, 1222. [CrossRef]
20. Grice, E.A.; Kong, H.H.; Renaud, G.; Young, A.C.; Bouffard, G.G.; Blakesley, R.W.; Wolfsberg, T.G.; Turner, M.L.; Segre, J.A.
A diversity profile of the human skin microbiota. Genome Res. 2008, 18, 1043–1050. [CrossRef]
21. Manus, M.B.; Kuthyar, S.; Perroni-Marañón, A.G.; la Mora, A.N.-D.; Amato, K.R. Infant Skin Bacterial Communities Vary by Skin
Site and Infant Age across Populations in Mexico and the United States. mSystems 2020, 5, e00834-20. [CrossRef] [PubMed]
22. Alyami, R.Y.; Cleary, D.W.; Forster, J.; Feelisch, M.; Ardern-Jones, M.R. Methods for the analysis of skin microbiomes:
A comparison of sampling processes and 16S rRNA hypervariable regions. bioRxiv 2023. [CrossRef]
23. Yao, Z.; Moy, R.; Allen, T.; Jansen, B. An Adhesive Patch-Based Skin Biopsy Device for Molecular Diagnostics and Skin Microbiome
Studies. J. Drugs Dermatol. JDD 2017, 16, 979–986. [PubMed]
Microorganisms 2025, 13, 54 12 of 13

24. Ring, H.C.; Thorsen, J.; Saunte, D.M.; Lilje, B.; Bay, L.; Riis, P.T.; Larsen, N.; Andersen, L.O.; Nielsen, H.V.; Miller, I.M.; et al. The
Follicular Skin Microbiome in Patients with Hidradenitis Suppurativa and Healthy Controls. JAMA Dermatol. 2017, 153, 897–905.
[CrossRef] [PubMed]
25. Pistone, D.; Meroni, G.; Panelli, S.; D’auria, E.; Acunzo, M.; Pasala, A.R.; Zuccotti, G.V.; Bandi, C.; Drago, L. A Journey on the Skin
Microbiome: Pitfalls and Opportunities. Int. J. Mol. Sci. 2021, 22, 9846. [CrossRef] [PubMed]
26. Kong, H.H.; Oh, J.; Deming, C.; Conlan, S.; Grice, E.A.; Beatson, M.A.; Nomicos, E.; Polley, E.C.; Komarow, H.D.; NISC
Comparative Sequence Program; et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in
children with atopic dermatitis. Genome Res. 2012, 22, 850–859. [CrossRef] [PubMed] [PubMed Central]
27. Langan, E.A.; Recke, A.; Bokor-Billmann, T.; Billmann, F.; Kahle, B.K.; Zillikens, D. The Role of the Cutaneous Microbiome in
Hidradenitis Suppurativa-Light at the End of the Microbiological Tunnel. Int. J. Mol. Sci. 2020, 21, 1205. [CrossRef] [PubMed]
[PubMed Central]
28. Toohey-Kurth, K.L.; Mulrooney, D.M.; Hinkley, S.; Killian, M.L.; Pedersen, J.C.; Bounpheng, M.A.; Pogranichniy, R.; Bolin, S.;
Maes, R.; Tallmadge, R.L.; et al. Best practices for performance of real-time PCR assays in veterinary diagnostic laboratories.
J. Vet. Diagn. Investig. 2020, 32, 815–825. [CrossRef]
29. Van Horn, K.G.; Audette, C.D.; Tucker, K.A.; Sebeck, D. Comparison of 3 swab transport systems for direct release and recovery
of aerobic and anaerobic bacteria. Diagn. Microbiol. Infect. Dis. 2008, 62, 471–473. [CrossRef] [PubMed]
30. Wise, N.M.; Wagner, S.J.; Worst, T.J.; Sprague, J.E.; Oechsle, C.M. Comparison of swab types for collection and analysis of
microorganisms. MicrobiologyOpen 2021, 10, e1244. [CrossRef]
31. Nakatsuji, T.; Gallo, R.L. Antimicrobial peptides: Old molecules with new ideas. J. Investig. Dermatol. 2012, 132 Pt 2, 887–895.
[CrossRef]
32. Griffiths, C.; Barker, J.; Bleiker, T.; Chalmers, R.; Creamer, D. (Eds.) Rook’s Textbook of Dermatology, 9th ed.; John Wiley & Sons Inc.:
Chichester, UK, 2016.
33. Afshar, M.; Gallo, R.L. Innate immune defense system of the skin. Vet. Dermatol. 2013, 24, e8–e9. [CrossRef] [PubMed]
34. Steinhoff, M.; Schauber, J.; Leyden, J.J. New insights into rosacea pathophysiology: A review of recent findings. J. Am. Acad.
Dermatol. 2013, 69 (Suppl. S1), S15–S26. [CrossRef] [PubMed]
35. Byrd, A.L.; Belkaid, Y.; Segre, J.A. The human skin microbiome. Nat. Rev. Microbiol. 2018, 16, 143–155. [CrossRef] [PubMed]
36. Yang, Y.; Qu, L.; Mijakovic, I.; Wei, Y. Advances in the human skin microbiota and its roles in cutaneous diseases. Microb. Cell
Fact. 2022, 21, 176. [CrossRef]
37. Chen, Y.E.; Tsao, H. The skin microbiome: Current perspectives and future challenges. J. Am. Acad. Dermatol. 2013, 69, 143–155.
[CrossRef] [PubMed] [PubMed Central]
38. Smythe, P.; Wilkinson, H.N. The Skin Microbiome: Current Landscape and Future Opportunities. Int. J. Mol. Sci. 2023, 24, 3950.
[CrossRef] [PubMed] [PubMed Central]
39. Smith, A.; Ghori, N.U.; Foster, R.; Nicol, M.P.; Barnett, T.; Pickering, J.; Whelan, A.; Strunk, T.; Wood, F.; Raby, E.; et al. Optimisation
of the sampling method for skin microbiome studies in healthy children: A pilot cohort study. Front. Microbiomes 2024, 3, 1446394.
[CrossRef]
40. Reynolds, F.H., 2nd; Tusa, M.G.; Banks, S.L. Toe Web Infections, the Microbiome, and Toe Web Psoriasis: A Review. Adv. Skin
Wound Care 2023, 36, 377–384. [CrossRef] [PubMed] [PubMed Central]
41. Leyden, J.J.; McGinley, K.J.; Nordstrom, K.M.; Webster, G.F. Skin microflora. J. Investig. Dermatol. 1987, 88 (Suppl. S3), 65s–72s.
[CrossRef] [PubMed]
42. Wollenberg, M.S.; Claesen, J.; Escapa, I.F.; Aldridge, K.L.; Fischbach, M.A.; Lemon, K.P. Propionibacterium-produced copropor-
phyrin III induces Staphylococcus aureus aggregation and biofilm formation. mBio 2014, 5, e01286-14. [CrossRef]
43. Ramsey, M.M.; Freire, M.O.; Gabrilska, R.A.; Rumbaugh, K.P.; Lemon, K.P. Staphylococcus aureus Shifts toward Commensalism in
Response to Corynebacterium Species. Front. Microbiol. 2016, 7, 1230. [CrossRef]
44. Bomar, L.; Brugger, S.D.; Yost, B.H.; Davies, S.S.; Lemon, K.P. Corynebacterium accolens Releases Antipneumococcal Free Fatty
Acids from Human Nostril and Skin Surface Triacylglycerols. mBio 2016, 7, e01725-15. [CrossRef] [PubMed]
45. Bolognia, J.L. (Ed.) Dermatology: ExpertConsult, 4th ed.; Elsevier: Edinburgh, UK, 2018.
46. Alomar, A. Can microbial superantigens influence atopic dermatitis flares? Chem. Immunol. Allergy 2012, 96, 73–76. [CrossRef]
[PubMed]
47. Cookson, W. The immunogenetics of asthma and eczema: A new focus on the epithelium. Nat. Rev. Immunol. 2004, 4, 978–988.
[CrossRef] [PubMed]
48. Woo, T.E.; Sibley, C.D. The emerging utility of the cutaneous microbiome in the treatment of acne and atopic dermatitis. J. Am.
Acad. Dermatol. 2020, 82, 222–228. [CrossRef] [PubMed]
49. Ellis, S.R.; Nguyen, M.; Vaughn, A.R.; Notay, M.; Burney, W.A.; Sandhu, S.; Sivamani, R.K. The Skin and Gut Microbiome and Its
Role in Common Dermatologic Conditions. Microorganisms 2019, 7, 550. [CrossRef] [PubMed]
Microorganisms 2025, 13, 54 13 of 13

50. The Australian Healthy Skin Consortium. National Healthy Skin Guideline: For the Diagnosis, Treatment and Prevention of Skin
Infections for Aboriginal and Torres Strait Islander Children and Communities in Australia, 2nd ed.; Telethon Kids Institute: Nedlands,
Australia, 2023.
51. Marson, J.; Bhatia, N.; Graber, E.; Harper, J.; Lio, P.; Tlougan, B.; Nussbaum, D.; Baldwin, H. Supplement Article: The Role of
Epidermal Barrier Dysfunction and Cutaneous Microbiome Dysbiosis in the Pathogenesis and Management of Acne Vulgaris and
Rosacea. J. Drugs Dermatol. 2022, 21, SF3502915–SF35029114. [PubMed]
52. Sattler, E.C.; Hoffmann, V.S.; Ruzicka, T.; Braunmühl, T.V.; Berking, C. Reflectance confocal microscopy for monitoring the density
of Demodex mites in patients with rosacea before and after treatment. Br. J. Dermatol. 2015, 173, 69–75. [CrossRef] [PubMed]
53. Paichitrojjana, A.; Chalermchai, T. Comparison of in vitro Killing Effect of Thai Herbal Essential Oils, Tea Tree Oil, and Metron-
idazole 0.75% versus Ivermectin 1% on Demodex folliculorum. Clin. Cosmet. Investig. Dermatol. 2023, 16, 1279–1286. [CrossRef]
54. Jarmuda, S.; McMahon, F.; Żaba, R.; O’Reilly, N.; Jakubowicz, O.; Holland, A.; Szkaradkiewicz, A.; Kavanagh, K. Correlation
between serum reactivity to Demodex-associated Bacillus oleronius proteins, and altered sebum levels and Demodex populations
in erythematotelangiectatic rosacea patients. J. Med. Microbiol. 2014, 63 Pt 2, 258–262. [CrossRef]
55. Whitfeld, M.; Gunasingam, N.; Leow, L.J.; Shirato, K.; Preda, V. Staphylococcus epidermidis: A possible role in the pustules of
rosacea. J. Am. Acad. Dermatol. 2011, 64, 49–52. [CrossRef]
56. Rademaker, M. Medical Management of Rosacea—An Australian/New Zealand Medical Dermatology narrative. In Proceedings
of the Australasian College of Dermatologists 55th Annual Scientific Meeting, Sydney, Australia, 28 May 2023.
57. Armour, K. Cosmeceuticals: Advice in Rosacea including sun protection. In Proceedings of the Australasian College of
Dermatologists 55th Annual Scientific Meeting, Sydney, Australia, 28 May 2023.
58. McCarthy, S.; Barrett, M.; Kirthi, S.; Pellanda, P.; Vlckova, K.; Tobin, A.-M.; Murphy, M.; Shanahan, F.; O’toole, P.W. Altered Skin
and Gut Microbiome in Hidradenitis Suppurativa. J. Investig. Dermatol. 2022, 142, 459–468.e15. [CrossRef] [PubMed]
59. Mintoff, D.; Borg, I.; Pace, N.P. The Clinical Relevance of the Microbiome in Hidradenitis Suppurativa: A Systematic Review.
Vaccines 2021, 9, 1076. [CrossRef] [PubMed]
60. Kimball, A.B.; Ganguli, A.; Fleischer, A. Reliability of the hidradenitis suppurativa clinical response in the assessment of patients
with hidradenitis suppurativa. J. Eur. Acad. Dermatol. Venereol. 2018, 32, 2254–2256. [CrossRef] [PubMed]
61. Join-Lambert, O.; Duchatelet, S.; Delage, M.; Miskinyte, S.; Coignard, H.; Lemarchand, N.; Alemy-Carreau, M.; Lortholary, O.;
Nassif, X.; Hovnanian, A.; et al. Remission of refractory pyoderma gangrenosum, severe acne, and hidradenitis suppurativa
(PASH) syndrome using targeted antibiotic therapy in 4 patients. J. Am. Acad. Dermatol. 2015, 73 (Suppl. S1), S66–S69. [CrossRef]
62. Fontao, F.; von Engelbrechten, M.; Seilaz, C.; Sorg, O.; Saurat, J.H. Microcomedones in non-lesional acne prone skin New
orientations on comedogenesis and its prevention. J. Eur. Acad. Dermatol. Venereol. 2020, 34, 357–364. [CrossRef] [PubMed]
63. Frew, J.W.; Hawkes, J.E.; Krueger, J.G. A systematic review and critical evaluation of inflammatory cytokine associations in
hidradenitis suppurativa. F1000Res 2018, 7, 1930. [CrossRef] [PubMed] [PubMed Central]
64. Wolk, K.; Join-Lambert, O.; Sabat, R. Aetiology and pathogenesis of hidradenitis suppurativa. Br. J. Dermatol. 2020, 183, 999–1010.
[CrossRef]
65. Bowen, A.C.; Mahé, A.; Hay, R.J.; Andrews, R.M.; Steer, A.C.; Tong, S.Y.C.; Carapetis, J.R. The Global Epidemiology of Impetigo:
A Systematic Review of the Population Prevalence of Impetigo and Pyoderma. PLoS ONE 2015, 10, e0136789. [CrossRef]
66. Piewngam, P.; Khongthong, S.; Roekngam, N.; Theapparat, Y.; Sunpaweravong, S.; Faroongsarng, D.; Otto, M. Probiotic for
pathogen-specific Staphylococcus aureus decolonisation in Thailand: A phase 2, double-blind, randomised, placebo-controlled trial.
Lancet Microbe 2023, 4, e75–e83. [CrossRef] [PubMed]
67. Sadowsky, R.L.; Sulejmani, P.; Lio, P.A. Atopic Dermatitis: Beyond the Skin and Into the Gut. J. Clin. Med. 2023, 12, 5534.
[CrossRef] [PubMed]
68. Jørgensen, A.H.; Egeberg, A.; Gideonsson, R.; Weinstock, L.B.; Thyssen, E.P.; Thyssen, J.P. Rosacea is associated with Helicobacter
pylori: A systematic review and meta-analysis. J. Eur. Acad. Dermatol. Venereol. 2017, 31, 2010–2015. [CrossRef] [PubMed]

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