Role of Cutaneous Microbiome in Dermatology

Abstract

The cutaneous microflora consists of various microorganisms which interact with host epithelial cells and innate and acquired immunity. This microbial milieu and its interaction with host cells prevent the growth of pathogenic organisms and educate host immunity to fight against harmful microorganisms. The microbial composition depends on various intrinsic and extrinsic factors and an imbalance in the cutaneous microflora predisposes the individual to both infectious and non-infectious diseases. Even though probiotics have been extensively studied in various diseases, their efficacy and safety profile are still unclear. A better understanding of the cutaneous microflora is required to develop newer therapeutic targets. In this review, we describe the commensal microbiome and its variation, the current role of the cutaneous microbiome in the pathogenesis of various dermatological diseases, and their therapeutic implications.

Introduction

Skin is the largest organ in the body. Apart from barrier protection, skin is also involved in thermoregulation, maintaining water and electrolyte imbalance, vitamin D synthesis, innate immunity, secretion of hormones, sensation, and anti-oxidant function.[1,2,3] Human skin is composed of various microorganisms such as bacteria, fungi, parasites, viruses, and archaea which are responsible for the normal functioning of the skin. The type of microorganisms, their abundance, and their distribution depend on various intrinsic and extrinsic factors. Interaction between cutaneous microflora and host cells is crucial for the normal functioning of the human skin. Alternation in the cutaneous microbiome has been observed in various dermatological diseases, but its exact causative role in the pathogenesis of the disease is not known.

Skin and Microflora in Health

Cutaneous microflora prevents the growth of the exogenous pathogenic microorganisms known as the ‘barrier effect’ or ‘colonization resistance’.[4] Identification of the cutaneous microflora has been an important advance in cutaneous biology. This is possible because of the advantages of gene sequencing over conventional culture methods, wherein the bacteria are identified using 16S ribosomal RNA (16S rRNA) and fungi using internal transcribed spacer 1 (ITS1). This has led to a better understanding of the physiology, disease pathogenesis, and implications of the cutaneous microbiome in disease management.

The human skin consists of various microorganisms depending on the site, temperature, humidity, pH, proteins, and lipids. Skin microflora is divided into resident (have the ability to repopulate and reside for a longer time) and transient microflora (unable to multiply and present only for a short period of time). The commensal bacterial microflora belongs to 4 major phyla: Actinobacteria, Bacteroidetes, Firmicutes, or Proteobacteria, and 5 major genera: Cutibacteria, Corynebacterium, Micrococcus, Acinetobacter or Staphylococcus. Commensal fungal microflora consists of Malassezia, Candida, Aspergillus, Fusarium, and Rhodotorula. In contrast to bacterial microflora, fungal microflora remains constant throughout the body. Viral microflora consists of Papillomaviridae, Polyomaviridae, and Circoviridae. The details of the families and genera of commensal microflora are given in Table 1.[5,6,7,8,9] The cutaneous microflora is not constant in every individual, there is significant physiological variation in the microflora due to multiple endogenous and exogenous factors. These are summarized in Table 2.[9,10,11,12,13,14,15,16,17,18,19]

Table 1.

Summary of the commensal human cutaneous microflora

A) Bacteria[5]	B) Fungi[6]
I) Actinobacteria	I) Basidiomycetes
Corynebacterium	Malassezia
Corynebacterium tuberculostearicum	Malassezia globosa
Corynebacterium fastidiosum	Malassezia restricta
Corynebacterium afermentans	Malassezia compacta
Corynebacterium simulans	Malassezia sympodialis
Cutibacteria	Rhodotorula
Cutibacterium acne	Cryptococcus
Micrococcus	II) Ascomycetes
Micrococcus luteus	Candida
II) Firmicutes	Candida parapsilosis
Staphylococcus	Aspergillus
Staphylococcus epidermidis	Aspergillus tubingensis
Staphylococcus hominis	Fusarium
Staphylococcus capitis	C) Viruses
Streptococcus	Propionibacteriaceae
Streptococcus pseudopneumoniae	Propionibacterium phage
Streptococcus oralis	Polyomaviridae
Streptococcus mitis	Merkel cell polyomavirus
Streptococcus sanguinis	Myoviridae
III) Proteobacteria	Staphylococcus phage
Enhydrobacter aerosaccus	Papillomaviridae
Acinetobacter	Alphapapillomavirus
Xanthomonas	D) Parasites[7]
Enterobacter	Demodex
IV) Bacteroidetes	Demodex folliculorum
	Demodex brevis

Table 2.

Factors affecting human cutaneous microbiota

Factor	Variation
Intrinsic
Genetics	Lower Cutibacterium in scalp and axilla in Africa and Latin America
Age	Birth: sterile Newborn, infants and elderly: Bacteriodetes predominant Children: Firmicutes predominant Adolescence: Proteobacteria predominant
Sex	More microbial diversity in female[8] Enterobacterales and Lactobacillaceae predominant in female[9] Cutibacterium and Corynebacterium predominant in male
Site  Moist areas (Groin, axilla, antecubital fossa, toe web)  Dry areas (arm, leg, volar forearm)  Sebaceous (face, chest, back)	Corynebacterium, Staphylococcus, Malassezia globosa and Malassezia restricta Proteobacteria, Bacteroidetes, Corynebacterium, Actinobacteria, Malassezia restricta and Malassezia globose Cutibacteria, Staphylococcus, Corynebacterium, Malassezia restricta and Malassezia globosa[9]
Mode of delivery  Caesarean  Vaginal	Staphylococcus, Corynebacterium, and Cutibacterium predominant Lactobacillus, Prevotella and Sneathia predominant[10]
Hormones  α-MSH  Acetylcholine  Catestatain	Act against Staphylococcus aureus and its biofilm Increased risk of infection by Streptococcus and Staphylococcus aureus Antibacterial against gram-positive and gram-negative bacteria[11]
Stress	Stress increases Actinobacteria (Corynebacterium and Cutibacteria) and Firmicutes (Staphylococcus), and lowers Proteobacteria and Bacteroidetes expression[12]
Others  Urban  Rural	Increase in Staphylococcaceae, Propionibacteriaceae, Streptococcaceae and Xanthomonadaceae Increase in Aspergillus, Malassezia, Candida, and Eurotiales Loss of Staphylococcus epidermidis, Lactobacillus spp., Burkholderis spp., Cutibacterium acne Acidobacteria and Bacteroidetes predominant Increase in Pseudomonas and Acinetobacter Decrease in Staphylococcus, Streptococcus, Corynebacterium and Cutibacterium[13]
Extrinsic factors
Sunlight	Increase in Cyanobacteria Decrease in Staphylococcus aureus, Cutibacterium acnes, Lactobacillaceae and Pseudomonadaceae[14]
Hygiene  Hand washing  Moisturizers	Decreases pathogens on hand[15] Lipid component promotes Staphylococcus and Cutibacterium
Antibiotics  Minocycline  Tetracycline/clindamycin/macrolides	Decrease in Cutibacterium, Corynebacterium, Prevotella, Lactobacillus, and Porphyromonas[16] Decrease in Cutibacterium acne and increase in Streptococcus, Staphylococcus, Micrococcus, and Corynebacterium[17] Long-term use lead to drug resistant species
Soap	Decreases microorganisms
Pollution  Soil (PAH exposure)  Air (NO2 and CO)	Increases Propionibacterium and Malassezia[18] Increase in Staphylococcus, Haemophilus, Enhydrobacter, Prevotella, and Veillonella19

Dysbiosis

Dysbiosis is the alteration in the composition, activity, or distribution of the cutaneous microflora. It occurs by 3 mechanisms: 1) Overgrowth of the member microflora (Cutibacterium acne in acne), 2) Invasion by non-member microflora (Staphylococcus aureus in atopic dermatitis), and 3) Elimination of member microflora. Dysbiosis is associated with various dermatological conditions such as acne, rosacea, atopic dermatitis (AD), psoriasis, seborrheic dermatitis, vitiligo, hidradenitis suppurativa, and leprosy, but currently, it is not fully known whether dysbiosis is cause or result of the disease.

Dysbiosis and Skin Diseases

Acne

Acne is a chronic benign inflammatory self-limiting disease of the pilosebaceous unit. Dysbiosis is one of the important mechanisms in the development of acne. The primary pathogenesis of acne is androgen-induced increased sebum production, follicular hyperkeratinization, inflammation, and follicular occlusion by microflora. Cutibacterium acne is a gram-positive, non-motile, non-spore-forming, and anaerobic rod. Cutibacterium acne under normal conditions produces propionic acid which maintains acidic pH leading to the prevention of colonization by pathogens. Acne is associated with a change in the strain of resident Cutibacterium acne. Type IA₁ and IC are associated with an increased risk of acne, while type IA₂, IB, II, and III are protective in nature. The density of Cutibacterium acne in healthy controls and acne patients does not differ.[20] Type IA₁ and IC strains of Cutibacterium acne in acne patients produces more proinflammatory mediators such as free fatty acids, porphyrin interferon-γ, IL-1, and IL-17 compared to normal commensal strains.[21,22] These mediators activate neutrophils and complement pathways leading to follicular inflammation and rupture. Apart from the above mechanisms, Cutibacterium acne also forms biofilm which leads to increased adhesive properties of corneocytes leading to the development of micro comedones.[23]

Atopic dermatitis

AD is a chronic inflammatory itchy disease with relapsing and remitting course, and commonly affecting infants and young children. The decreased level of anti-microbial peptides and barrier defect promote the colonization with staphylococcus species. AD is associated with the abundance of Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus hominins, and Staphylococcus capitis, but only Staphylococcus aureus and Staphylococcus epidermidis abundance are associated with disease flare in AD patients. Staphylococcus aureus exacerbates AD through the following mechanisms: 1) Activate keratinocytes to produce kallikrein which subsequently causes degradation of filaggrin and barrier defect, 2) Stimulates keratinocytes to produce IL-1α and IL-36-α which subsequently act on their receptor leading to the inflammation via IL-17 production,[24] 3) Produces superantigens which lead to activation of MHC-II[25] and 4) Form biofilm which produces robust inflammatory response leading to disease.[26] Staphylococcus epidermidis has a dual role in AD, through cysteine protease activity cleaves LL-37 and desmoglein-1 which leads to disruption in the barrier and subsequent inflammation, and it also activates non-inflammatory pathways by inhibiting TLR-3 expression on keratinocytes. Staphylococcus epidermidis predominant AD is associated with less severe disease as compared to Staphylococcus aureus predominant AD. The role of decolonization is not well studied and can be considered in patients at high risk of infection. Apart from bacterial dysbiosis, there is an abundance of Malassezia in AD and it is associated with head and neck dermatitis, severe disease, exacerbation during adolescence, and other atopic diseases. These patients respond to anti-fungal therapy and long-term weekly therapy can be considered.[27,28]

Psoriasis

Psoriasis is a chronic inflammatory disease of the skin characterized by discrete erythematous scaly plaques over the scalp and extensor aspect of extremities. The role of dysbiosis in the pathogenesis of psoriasis is controversial due to inconsistent results which could be due to differences in study design, study population, and sampling methods. In contrast to normal microflora that is actinobacteria predominant, firmicutes are most abundant and actinobacteria are reduced in the lesional skin. Dysbiosis activates conventional dendritic cells to secrete IL-23 which subsequently activates the Th17 pathway.[29] In addition, Malassezia sympodial-is produces pro-inflammatory cytokines such as TNF-α, IL-1, IL-6, and IL-8 which activate keratinocyte proliferation.[30] The presence of dysbiosis is associated with an increased risk of developing psoriatic arthritis and correcting the imbalance could have a therapeutic role.

Seborrheic dermatitis

Seborrheic dermatitis (SD) is a chronic benign inflammatory disease characterized by a yellow-greasy scale in seborrheic distribution. Malassezia globose, Malassezia restricta, and staphylococcus are the predominant microflora and Cutibacterium are underrepresented in SD. Malassezia and Staphylococcus act via the following mechanisms in the development of SD: 1) Malassezia produces lipases that act on triglycerides to form fatty acids which cause hyperproliferation, scaling, and inflammation, 2) Malassezia also produces arachidonic acid that promotes inflammation, and 3) Staphylococcus promotes the growth of Malassezia by providing nutrients (hydrolyzed sebum). This suggests that SD is a result of dysbiosis rather than infection.[31]

Rosacea

Rosacea is a chronic inflammatory disease characterized by recurrent facial flushing, papules, and pustules after exposure to a triggering agent. The abundance of Demodex mites (Demodex folliculorum and Demodex brevis) is significantly increased in all subsets of rosacea. Demodex mite alters innate immunity through the following pathways. 1) Stimulates TLR-2 that causes an increased level of LL-37 leading to inflammation and angiogenesis 2) Increases the level of vascular endothelial growth factor (VEGF) leading to vasodilatation, increase in vascular permeability and chemotaxis, 3) Induction of tolerogenic dendritic cells which act via VEGF, and 4) Induction of proinflammatory cytokines by mite exoskeleton.[32]

Apart from Demodex, Cutibacterium acne abundance is decreased and Staphylococcus epidermidis is increased significantly in erythematotelangiectatic and papulopustular rosacea as compared to healthy skin.[33] Further studies targeting dysbiosis in the treatment of rosacea are required.

Hidradenitis suppurativa (HS)

HS is a chronic inflammatory disease of the hair follicle characterized by recurrent nodules, abscesses, and sinuses leading to a scar. HS is characterized by an abundance of polymicrobial aerobic and anaerobic microflora. Aerobic microflora includes Staphylococcus aureus, coagulase-negative Staphylococci, Peptostreptococcus, Pseudomonas aeruginosa, Streptococcus pyogenes and Cutibacterium acne, and, anaerobic microflora consist of Peptostreptococcus, Prevotella, Fusobacterium, Bacteroides and microaerophilic streptococci. Staphylococcus predominates in acute nodules and abscesses and anaerobes in chronic suppurative lesions. Biofilm formation is one of the reasons for persistent lesions and is common in chronic HS (65-75%).[34] The presence of keratinous debris, dilated hair follicles and sinuses in chronic lesions promotes biofilm formation. Biofilms are larger in lesional skin as compared to perilesional skin and are associated with poor response to antibiotics.

Leprosy

Leprosy is a chronic bacterial infectious disease primarily affecting skin and peripheral nerves. In leprosy lesions, there is a higher expression of Proteobacteria and Bacteroidetes and an underrepresentation of Firmicutes and Actinobacteria. Lesional leprosy skin is rich in Micrococcus and Acinetobacter with a decrease in Streptococcus, Corynebacterium, and Cutibacterium indicating the protective role of the latter three genera.[35] The expression of staphylococcus in leprosy is controversial. After treatment with multidrug therapy, Firmicutes, and Actinobacteria expression increases with a decrease in Proteobacteria and Bacteroidetes.[35] Currently, there is no literature comparing dysbiosis in different spectrums of leprosy.

Dermatophytosis

Dermatophytosis is common contagious superficial fungal infection affecting skin, hair, and nail. Based on the site of involvement, dermatophytosis is classified into tinea capitis (scalp), tinea cruris (groin), tinea facies (face), tinea manuum (hands), and tinea pedis (feet). Tinea cruris is associated with the abundance of Firmicutes (Staphylococcus) and Actinobacteria (Corynebacterium). Proteobacteria is predominant microflora in tinea pedis, tinea corporis, and tinea capitis. Compared to other sites with dermatomycoses, the bacterial diversity in tinea cruris patients was comparatively low. Interestingly, Propionibacterium is the predominant microflora in patients with tinea pedis and psoriasis, and the same is not seen in patients with tinea pedis alone.[36]

Role of Microorganisms in Treatment Strategies

The cutaneous microbiome modulates and influences the host immune system, enabling immune tolerance of environmental and dietary antigens.[37] The resident flora of the skin function in immune regulation and pathogenesis of various dermatoses.[38]

Probiotics refer to “live microorganisms which when administered in adequate amounts, confer a health benefit on the host.”[39,40] Their influence extends to various organs of the body including skin via complex mechanisms. United States Food and Drug Administration (USFDA) has categorized probiotics into various categories which include dietary supplements, foods, cosmetics, food additives, or drugs. They are used in various dermatoses like acne, AD, photo aging, psoriasis, and wound healing.[37]

Probiotics when applied topically serve as a protective barrier by functioning as a competitive inhibitor of binding sites, thus preventing the colonization by other pathogenic flora and restoring the well-balanced microbiome.[37] They passively occupy the ecological niche similar to the pathogenic microbe, thus preventing their colonization, and decreasing the incidence of infections and the need for antibiotic therapy. They secrete various antimicrobial peptides which have an immunomodulatory effects.[38] Potential side effects of probiotics include allergic reactions to inactive ingredients, bacteremia, and antibiotic resistance transfer among pathogens.[37]

In AD, probiotics have been shown to be beneficial among patients of age groups of more than 1 year, moderate-severe AD flares, and when used for a period of more than 8 weeks. A mixture of probiotics is preferred rather than a single probiotic (eg. a mixture of lactobacillus and bifidobacterial). Probiotics cause a reduction in IL-4, IL-5, and IL-13 to some extent suggesting a decrease in Th2 cell response which is involved in AD.[41]

In acne vulgaris, various organisms like Streptococcus salivarius and Enterococcus faecalis, inhibit the growth of pathogenic Cutibacterium acnes by the production of antibacterial proteins (Bacteriocin-like inhibitory substance; BLIS), immunomodulatory action on the keratinocytes and anti-inflammatory action (inhibit IL-8 production). Staphylococcus epidermidis is shown to ferment glycerol and inhibit the production of Cutibacterium acnes in a culture media. These probiotics have similar benefits to antibiotics but do not have their side effects. The effects of probiotics are best in high grades or inflammatory forms of acne.[42] Other dermatoses where the role of probiotics has been explored are enlisted in Table 3.[39,40,41,42,43,44]

Table 3.

Role of Microorganisms in treatment strategies

Condition	Relation with microbiome	Potential Organism	Mechanism of action
Acne[37,39,40,43,44,45]	Interaction between skin microbes and host immunity plays a role in the pathogenesis. Cutibacterium strains, ribotype 4 and ribotype 5 are involved directly in disease pathogenesis. Bacteria induce Th1 and Th17 responses and suppresses IL-10 anti-inflammatory response in the skin. Bacteriotherapy is an emerging therapy encompassing various bacterial products and application modalities.	Streptococcus thermophilus	Increase production of ceramides (phytosphingosine) which gives both antimicrobial action (against Cutibacterium acnes and anti-inflammatory action.
		Enterococcus faecalis SL-5 (10% concentration powder made into a lotion of 6.400 AU/100)	Gram-negative action against Cutibacterium acnes. (Significantly reduces the pustules)
		Streptococcus salivarious (Resident of Oral microbiota)	Antimicrobial and immunomodulatory (inhibit IL-8 in epithelial cells and keratinocytes) action. Production of Bacteriocin-like inhibitory substance (BLIS) to inhibit growth of Cutibacterium acnes.
		Combination of Lactobacillus and Bifidobacteria spp.	Improvement in innate and adaptive immunity dysregulation. Production of bacteriocidin which suppresses both inflammation and pathogenic bacteria.
		Lactobacillus plantarum (5%)	Reduce lesion concentration (Produce antimicrobial peptides) and pathogenic bacterial load.
		Lactobacillus paracasei CNCM I-2116 (ST11) (In vitro study)	Inhibit substance P induced inflammation and regeneration of skin barrier. Decrease mast cell degranulation and TNF-alpha production.
		Staphylococcus epidermidis (In vitro study)	Ferment glycerol and inhibit growth of Cutibacterium acne.
		Nitrosomonas eutropha	Reduce the number of inflammatory lesions.
		Cutibacterium acnes bacteriophage	Lyse only the acne-associated and uncorrelated phylotypes of Cutibacterium.
Atopic Dermatitis[[38,39,41,43,45]	Traditional treatment options might be insufficient for certain group of patients. AD patients have a decreased capacity to produce Antimicrobial peptides like Cathelicidins and beta-defensins.	Streptococcus thermophilus	Increase in the levels of ceramides in the stratum corneum (by hydrolysis of sphingomyelin by the bacterial sphingomyelinase) and decrease the symptoms of AD. Probiotics induce a positive biome balance. Decrease the use of steroids during AD flares.
		5% lyasate of Vitreoscilla filiformis	Reduction in Staphylococcus aureus colonisation. Direct immunomodulatory action (Activation of TLR2 which subsequently suppresses the T effector cells and serine protease secretion).
		Lactobacillus johsonii NCC 533	Decrease in Staphylococcus aureus colonisation via species antagonism and decrease the severity of disease.
		Lactobacillus salivarius	Inhibits the increase of IL-4 production associated with interferon reduction.
		Roseomonas mucosa	Decrease in disease severity and pruritus, steroid application requirement and S aureus colonisation.
		Coagulase-negative Staphylococcus spp.	Produce AMPs to inhibit the growth of Staphylococcus aureus.
		Staphylococcus epidermidis	Increase human beta-defensins 2 and 3 which inhibit S aureus growth. Decrease surface area involved in AD. Activate TLR2 signalling and expression of antimicrobial peptides. Serine protease secreted inhibits the biofilm formation and destroys the pre-existing biofilm of S aureus.
Photoageing and ageing skin[38]	Probiotics can restore the acidic Ph, attenuate photoageing (UVB induced) and improve barrier function of skin. Alleviation of oxidative stress.	Plant extracts with Lactobacillus buchneri (PELB)	PELB decreases the elastase action and increases Type 1 collagen expression in photodamaged skin. Reduce collagenase activity and increase expression of moisture factor.
		Nitrosomonas eutropha	Improves the severity of depth of wrinkles and hyperpigmentation.
		Streptococcus thermophilus	Increase ceramide production and skin hydration.
		Bifidobacteria longum	Decrease skin sensitivity and improve resistance to physical manipulation.
Psoriasis[38,45]	Psoriatic skin shows a decreased colonisation of Staphylococcus epidermidis and Cutibacterium acnes leading to higher Staphylococcus aureus colonisation. Dysbiosis contributes to inappropriate activation of immune system. Group A beta-hemolytic streptococcus is linked to guttate psoriasis.	Cutibacterium acnes	Presence of Cutibacterium acnes promotes Th2 mediated response and downregulates Th1 mediated inflammatory pathway implicated in causation of psoriasis.
		Lactobacillus sakei (Anima model)	Anti-inflammatory action.
		Bifidobacterium infantis (oral)	Immunoregulatory and anti-inflammatory (decrease C-reactive protein and tumour necrosis factor-alpha) response.
		Lactobacillus oentosus (oral)	Reduced tumor necrosis factor and IL-23-17 axis cytokines.
Wound Healing[38,39]	Topical probiotics can prevent infection and inflammation and help augment the healing process.	Lactobacillus plantarum	Decreases the colonisation of pseudomonas infection after burns. (mouse model) Decreases bacterial load, decreases neutrophilic and necrotic cells, modifies IL-8 production.
		Lactobacillus Brevis	Promote granulation tissue formation and decreases the inflammatory markers.
		Propioniferax innocua	Degrades the established biofilms.
		Staphylococcus caprae	Antimicrobial action against MRSA and inhibits Staphylococcus aureus colonisation.
		Staphylococcus epidermidis	Antimicrobial peptides against Staphylococcus aureus suppress inflammation by production of lipoteichoic acid.
Seborrheic dermatitis[39,45]	Inflammatory response to free fatty acids produced by Malassezia spp. Decreased bacterial diversity is a predictor of disease severity.	Vitreoscilla filiformis	Decrease erythema, scaling and pruritus. Increase IL-10 production from dendritic cells and increase regulatory T cell activity.
		Lactobacillus paracasei (Oral)	Increase levels of IL-10 and transforming growth factor- beta.
Skin cancers[39]	Continued inflammatory state of skin promotes carcinogenesis.	Lactobacilli spp. (Oral)	Decrease incidence of ultraviolet (UV) rays induced damage to skin, thus prevent carcinogenesis. Control inflammation by activation of antineoplastic pathways.
		Staphylococcus epidermidis	Produce nucleobase molecules that inhibit tumor proliferation selectively and reduce incidence of UV-rays induced photodamage.

Conclusion

The cutaneous microbiome serves as a potential therapeutic target for various dermatoses. Probiotics promote a healthy microbiomes and reduce the inflammation and colonization of pathogenic bacteria. In recent times, probiotics are being used extensively, however, their long-term safety, optimal dosing, and efficacy are still being explored. Their safety in immunocompromised and pregnant patients is also yet to be explored. Newer studies are required to characterize the organisms as risk factors or therapeutic agents in the treatment of various dermatoses. Studies that can verify the pathogenic role of dysbiosis and its reversal causing remission (if so, then how long it lasts) are also yet to be reported. Most efficacious strategies may include the combination of topical and oral therapy.

Questions (answers provided after references)

1. Human cutaneous microflora is constant in all individuals

   1. True
   2. False

2. Atopic dermatitis is characterized by an abundance of Staphylococcus aureus

   1. True
   2. False

3. Abundance of Malassezia is associated with head and neck dermatitis in atopic dermatitis

   1. True
   2. False

4. Dysbiosis in psoriasis is associated with an increased risk of psoriatic arthritis

   1. True
   2. False

5. Demodex mite causes a decrease in LL-37 in rosacea

   1. True
   2. False

6. Biofilm formation is one of the reasons for chronic lesions in hidradenitis suppurative

   1. True
   2. False

7. Probiotic works better in inflammatory forms of acne

   1. True
   2. False

8. Plant extracts with Lactobacillus buchneri inhibit type-1 collagen expression in photodamaged skin

   1. True
   2. False

9. Staphylococcus epidermidis promotes the growth of Staphylococcus aureus

   1. True
   2. False

10. Atopic dermatitis is characterized by the low level of antimicrobial peptides

    1. True
    2. False

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Answers to Questions

1. False

2. True

3. True

4. True

5. False

6. True

7. True

8. False

9. False

10. True