The influence of lifestyle and environmental factors on host resilience through a homeostatic skin microbiota: An EAACI Task Force Report

Abstract

Human skin is colonized with skin microbiota that includes commensal bacteria, fungi, arthropods, archaea and viruses. The composition of the microbiota varies at different anatomical locations according to changes in body temperature, pH, humidity/hydration or sebum content. A homeostatic skin microbiota is crucial to maintain epithelial barrier functions, to protect from invading pathogens and to interact with the immune system. Therefore, maintaining homeostasis holds promise to be an achievable goal for microbiome‐directed treatment strategies as well as a prophylactic strategy to prevent the development of skin diseases, as dysbiosis or disruption of homeostatic skin microbiota is associated with skin inflammation. A healthy skin microbiome is likely modulated by genetic as well as environmental and lifestyle factors. In this review, we aim to provide a complete overview of the lifestyle and environmental factors that can contribute to maintaining the skin microbiome healthy. Awareness of these factors could be the basis for a prophylactic strategy to prevent the development of skin diseases or to be used as a therapeutic approach.

Abbreviations

AD

atopic dermatitis

AMPs

antimicrobial peptides

HS

hidradenitis suppurativa

Nb

narrowband

NPs

nanoparticles

SCFAs

short chain fatty acids

TGF‐β

transforming growth factor‐β

Th

T helper

Treg

regulatory T cells

UV

ultraviolet

UVB

ultraviolet B

UVR

ultraviolet‐radiation

1. INTRODUCTION

Humans are holobionts, ¹ , ² , ³ with over 3.8 × 10¹³ prokaryotic cells inhabiting a reference human (male, 20–30 years of age; 70 kg; 170 cm) in contrast to 3.0 × v10¹³ estimated human cells. Bacterial genes (3.3 million) exceed by around 150‐fold those of the human genome, (~19,000 genes). ⁴ , ⁵ Although higher in numbers, prokaryotic mass only represents ~0.3% (0.2 kg) of the total human biomass. ⁶ Human skin is colonized with commensal bacteria, fungi, arthropods, archaea and viruses, which compose the human skin microbiota. ⁷ , ⁸ , ⁹ , ¹⁰ , ¹¹ , ¹² , ¹³ , ¹⁴ , ¹⁵ , ¹⁶ , ¹⁷ , ¹⁸ , ¹⁹ , ²⁰ , ²¹ At different anatomical locations, the skin provides diverse microenvironments that vary in temperature, pH, humidity/hydration or sebum content, which affects the microbiota composition (Figure 1).

FIGURE 1.

Skin microbiota composition at different anatomical locations. Skin microenvironments differ in temperature, pH, humidity, and sebum content, which conditions the composition of skin microbiota.

Lifestyle factors, such as diet, exercise practice or the use of cosmetic products, as well as environmental factors, such as air pollution or ultraviolet‐light (UV) exposure, play a significant role on the skin microbiome and overall skin health, influencing the epidemiology and severity of skin diseases. ²² , ²³ Together with the environmental exposures, the skin microbiota modulates human homeostasis and skin immune responses.

In this review, research papers written in English were included, while abstracts were excluded. The goal of the EAACI Task Force is to provide an overview of the current knowledge on the lifestyle and environmental factors that contribute to maintaining a healthy skin microbiome, both as a prophylactic strategy to prevent the development of skin diseases and for future therapy. The lifestyle and environmental factors mentioned in the present review are intended for the general population and do not specifically apply to children or adults.

2. FUNCTIONS AND IMPORTANCE OF THE SKIN MICROBIOTA

Skin microbiota develops in concerto with the gut and lung microbiota during early‐life colonization. ²⁴ It is crucial to protect from invading pathogens and interact with the immune system. ⁹ It contributes to maintaining the epithelial barrier function and ensures skin homeostasis. Skin microbes secrete proteases involved in the skin renewal process via desquamation; sebum, and fatty acids involved in pH regulation; bacteriocins, indols and antimicrobial peptides (AMPs) that protect against infectious invaders, and lipase and urease enzymes involved in metabolite breakdown. ²⁵ , ²⁶ , ²⁷ , ²⁸ , ²⁹ , ³⁰ Moreover, skin microbes compete with pathogenic microbes and are able to communicate via quorum sensing. ²⁶ , ²⁷ Furthermore, they interact with host immune cells and train them to respond to potential pathogenic threats. ¹¹ , ³¹ In turn, skin microbiota homeostasis depends on the production of AMPs both by bacteria themselves and by host cells, such as keratinocytes (Figure 2).

FIGURE 2.

Functions of the skin microbiota. Skin microbiota is crucial to maintain the epithelial barrier function, to protect from invading pathogens and to interact with the immune system. These interactions ensure skin homeostasis.

Fungi and viruses represent a poorly understood component of the human skin microbiota, which have the potential to modulate skin homeostasis. ³² , ³³ , ³⁴ , ³⁵ , ³⁶ , ³⁷ , ³⁸ , ³⁹ , ⁴⁰ Within the skin virome, bacteriophages are of special relevance as they can modulate bacterial communities through predation, and therefore, affect human skin health. ⁴¹ , ⁴² Several studies on healthy skin demonstrated bacteriophages dominated the skin virome, whereas the abundance of eukaryotic viruses was notably increased in altered skin samples. ³⁷ , ³⁹ , ⁴³ , ⁴⁴

The focus of skin‐related microbiome research has been directed towards disease‐related microbiota dysbiosis. However, maintaining homeostasis holds promise to be an achievable goal for microbiome‐directed preventative and therapeutic strategies. Studies suggested that skin diseases, such as atopic dermatitis (AD), psoriasis, acne or rosacea are associated with the disruption of homeostatic skin microbiota rather than the colonization of pathogens. Subsequently, dysbiosis contributes to skin inflammation. An optimal healthy skin microbiome is still to be defined and likely depends on genetic as well as environmental, biological and lifestyle factors. Nevertheless, a homeostatic and diverse microbiome exerting protective functions on the host by supporting its immune system to mount appropriate responses and maintain homeostatic barrier functions could be a definition for a healthy microbiome. ⁴⁵

3. LIFESTYLE FACTORS

3.1. Circadian rhythms

Circadian rhythms, the 24‐h cycles of the body's internal clock, affect skin functions including free radical production and neutralization, DNA damage and repair, keratinocyte and fibroblast proliferation and differentiation, as well as barrier and immune functions. During the day, the skin has the highest pH, sebum production and thickness with the lowest cell proliferation. At night, the skin has the highest DNA repair, cell proliferation, barrier permeability and blood flow. ⁴⁶

Recent studies have shown that the skin microbiome composition and function vary with host circadian oscillations. ⁴⁷ , ⁴⁸ Skin analysis of hand palms in the morning and the evening showed that some taxa (Propionibacteriaceae, Micrococcaceae, Gordoniaceae and Dermacoccaceae) present a diurnal abundance pattern. ⁴⁷ Circadian disruptions are associated with the loss of the homeostatic microbiome. ⁴⁹ , ⁵⁰ , ⁵¹ , ⁵² Alterations in sleep patterns can increase the risk of skin disorders or worsen their symptoms, like increased levels of pro‐inflammatory cytokines, contributing to the maintenance of inflammation. ⁵⁰ , ⁵¹ Regular late‐bedtime reduces the abundance and diversity of the microbiota of facial skin, which strongly correlates with physiological parameters like skin barrier integrity, skin structure damage and water–oil balance. ⁵² Additionally, light/dark cycles regulate the expression of genes encoding AMPs production, which, in turn, affects the survival of pathogenic microbes on the skin. ⁵³ Recently, the adaptive contact hypersensitivity response, relevant in contact allergic dermatitis, was found to depend on circadian rhythms in a mouse model of cutaneous type IV allergy. Being mice a nocturnally active species, several allergic parameters increased when sensitized at night compared to daytime sensitization. ⁵⁴

These studies suggest that lifestyle changes leading to circadian disruptions could be more important for skin diseases than previously recognized. However, the role of the skin commensals in this process still needs to be elucidated.

3.2. Diet and the gut‐skin axis

Diet plays a vital role in maintaining skin health and homeostasis of the skin microbiome. The bidirectional relationship between diet, the gut (microbiome), and the skin (microbiome) is an area of growing research interest. ²² , ²³ The gut‐skin axis is an integral part of the gut‐brain‐skin axis, which was first defined by the dermatologists Stokes and Pillsbury in 1930 ⁵⁵ ; and subsequently further described. ⁵⁶ , ⁵⁷ Emerging research shows the importance of the gut microbiome to modulate the immune response on various organs, including the skin and its residing skin microbiome. This bidirectional interaction plays a crucial role in the development of various skin diseases, including acne vulgaris, psoriasis and atopic dermatitis (AD) among others. ⁵⁸ , ⁵⁹

The microbiome is the primary component in the gut‐skin axis. Nutritional compounds, degraded by the gut microbiome, modulate immune responses instigating systemic effects (including REDOX reactions, inflammation and hormonal changes), and influencing skin conditions. Microbiota‐derived metabolites, such as short chain fatty acids (SCFAs) and secondary bile acids, neurotransmitters and hormones cross the epithelial barrier and interact with immune cells at the lamina propria stimulating the differentiation of regulatory T cells (Treg) or the production of IgA by B cells, while others are released in the bloodstream and travel towards distant organs such as skin, lungs or the brain. ⁶⁰ , ⁶¹ The gut‐skin axis may explain why many inflammatory skin disorders are associated with gut comorbidities, for example, psoriasis patients may also suffer from inflammatory bowel disease, hidradenitis suppurativa (HS) patients have an increased risk of developing Crohn's disease and ulcerative colitis, and severe AD in children is often associated with food allergy or eosinophilic esophagitis. ⁶² , ⁶³ , ⁶⁴ , ⁶⁵ , ⁶⁶

Western diets, containing highly saturated fats and high‐glycaemic foods are known to contribute to various skin disorders, including psoriasis, HS and acne vulgaris. ⁶⁷ , ⁶⁸ , ⁶⁹ , ⁷⁰ A high‐fat diet exacerbated psoriasis in mice by increasing IL‐17‐producing γδ‐T cells. ⁶⁷ In contrast, a modified intermittent fasting diet was proposed to improve psoriasis lesions. ⁷¹ HS pathogenesis was influenced by the intake of high‐glycaemic load diets and dairy, while certain food triggers containing wheat or brewer's yeast, such as beer, wine, bread and other bakery products, lead to HS reoccurrence. ⁶⁸ , ⁶⁹ Niacin (vitamin B3), found in meat, poultry, fish, grains and legumes, is a known factor that can trigger a flare‐up in rosacea patients. ⁷² Niacin activates niacin receptors, present in dermal Langerhans cells, which leads to the release of prostaglandins around the capillaries in the skin. This might instigate symptoms such as erythema, an increase in skin temperature, and a sensation of stinging and itching. ⁷³ Regarding other vitamins, optimal serum biotin (vitamin B7) levels (>400 ng/L) have been associated with a lower risk of seborrheic dermatitis. ⁷⁴ Additionally, the antifungal activity of kombucha tea ethyl acetate against Malassezia strains, suggesting a potential therapeutic implication for seborrheic dermatitis. ⁷⁵ Furthermore, adherence to a Mediterranean diet, characterized by high consumption of fruits, vegetables, whole grains, legumes and olive oil, was inversely associated with the presence of acne and improved non‐scarring alopecia. ⁷⁶ , ⁷⁷ In addition, a recent study found that a fermentable fibre‐rich diet limits allergen sensitization and AD severity through SCFA production by the gut microbiome. Butyrate, in particular, strengthened epidermal barrier function by modulating the metabolism of epidermal keratinocytes and production of key structural components. ⁷⁸ Although these studies point to the influence of the diet on the skin function, they do not address the role of skin microbiota in these processes. The association of macronutrients in the diet, as well as dietary energy or alcohol consumption with the composition of skin microbiota was investigated. ⁷⁹ The diet influenced the skin microbiota composition via the immune response modulation and/or via the gut‐skin axis. Studies on the effect of vegan diets focused on the skin/ skin diseases, but not specifically on skin microbiota. ⁸⁰ , ⁸¹ , ⁸² Alcohol consumption was associated with modulation of the gut microbiota, but no evidence exists for the skin microbiota. ⁸³

Oral probiotics are considered as safe and cheap alternatives to synthetic drugs for improving the gut microbiome and inflammatory skin conditions, including AD, acne vulgaris, psoriasis, rosacea, HS. Currently, the numerous heterogeneous experimental study designs are limiting the implementation of probiotics into clinical practice. ⁸⁴ , ⁸⁵ Nevertheless, mice that were fed with a probiotic mixture present in yoghurt or a Lactobacillus reuteri strain showed improved body weight, fur quality and thickness, mediated through an IL‐10‐dependent mechanism. ⁸⁶ In a human study, supplementation with Lactobacillus paracasei NCC 2461 resulted in improved skin barrier function, as indicated by lower trans epidermal water loss and higher levels of transforming growth factor‐β (TGF‐β). ⁸⁷ Furthermore, the bidirectional gut‐skin axis was demonstrated in a study where female participants exposed to narrow‐band ultraviolet B (UVB) light showed alterations in the gut microbiome composition. ⁸⁸

Understanding the intricate relationship between diet, the gut microbiome and the skin microbiome is essential for maintaining skin homeostasis, preventing the emergence of skin disorders, and exploring potential therapeutic interventions. Adequate intake of essential nutrients through diet, for example, vitamin C, supports collagen synthesis, enhances skin barrier function, and protects against oxidative damage. ⁸⁹ , ⁹⁰ , ⁹¹ Additionally, maintaining proper hydration through dietary water intake is important for skin hydration and biomechanical properties. ⁸⁹ Based on studies of the Mediterranean diet, a nutrient‐rich diet containing fruits, vegetables, whole grains, legumes, and unsaturated fats, can help individuals to maintain a healthy skin. ⁷⁶ , ⁷⁷

Finally, it would be of interest to address the link between skin microbiota and microbiota residing at other body sites such as the nose, the oral cavity or the airways. However, there is still little evidence on the interaction of microbiota at different body sites. A recent review reported a lack of studies on the impact of airway microbiota on skin allergy, although a frequent association between AD and asthma has been described. ⁹² , ⁹³ , ⁹⁴ , ⁹⁵ In healthy respiratory tract and skin, predominant bacterial genera such as Firmicutes, Proteobacteria or Actinobacteria, have been reported. ⁹⁶

3.3. Exercise practice

Few studies investigated the relationship between exercise practice and skin microbiota functions. The skin microbiome in athletes is subject to the type of contact sport, training intensity and environment. Inflammatory skin diseases, such as acne, or viral, bacterial or fungal infections, commonly occur in professional athletes of contact sports. In wrestlers, Bacillus cereus, Staphylococcus aureus, S. epidermidis, and S. saprophyticus were common opportunistic species found on the skin. ⁹⁷ Standard infection‐control protocols can be effective in decreasing the bacterial and viral burden in athletes. ⁹⁸ An isopropyl alcohol disinfectant was found to be effective in inhibiting unwanted bacterial growth and decreasing the number of skin infections in wrestlers, ⁹⁷ as fungal infections, for example, dermatophytes causing Tinea corporis, are more common in wrestlers. ⁹⁹ The question arises whether dysbiosis of the skin microbiome is a result of sweating, contact with different microbiota or a consequence of excessive showering.

A study including adolescent swimmers investigated the relative abundance of the skin microbiota pre‐ and post‐swimming using skin swabs. Seven out of sixteen swimmers had facial acne. All swimmers showed a decrease of Coproporphyrin III, as a measure of acne‐specific inflammation after 1 h of swimming, while the relative abundance of pathogenic Cutibacterium acnes remained unchanged, and Pseudomonadaceae increased. Probably, the continuous shift between colonization and decolonization of C. acnes and Pseudomonadaceae may be associated and contribute to swimmers' acne pathogenesis. ¹⁰⁰

3.4. Hygiene habits

Personal hygiene habits directly affect the skin microbiota. Therefore, it is essential to follow appropriate personal hygiene practices and a healthy lifestyle to retain the homeostatic microbiota and to avoid skin alterations. These hygiene habits should not be confused with sterilization, which means the removal of all microbes, including the skin commensals.

Time since last hand washing using soap affects the bacterial composition of the hands, but it has no impact on the overall diversity. ¹⁰¹ This might indicate that hand hygiene acts on the outer surface and does not change the resident populations at lower skin layers. Healthcare workers undergo more frequent hand washing than the general population leading to skin irritation and higher abundances of pathogenic antimicrobial‐resistant S. aureus and Gram‐negative bacteria. ¹⁰² Skin antisepsis preparation for surgery reduces the number of skin microbiota at local areas. The type of antiseptics and the exposure time are important factors. Antiseptics, such as alcohol‐based hand sanitizers, ethanol, and povidone‐iodine, reduce the number of observed resident species in the skin shortly after use. ¹⁰³ , ¹⁰⁴ Less abundant members of the skin microbiota are more likely to be displaced and replaced by the most abundant taxa. ¹⁰³ The Propionibactericeae family is notoriously resistant, suggesting a competitive advantage when skin microbiota homeostasis is disturbed by hand sanitizers. ¹⁰³ A beneficial effect was found of alcohol‐based povidone‐iodine over alcohol‐based chlorhexidine to remove Cutibacterium acnes from the deeper skin layers from the shoulder area for antiseptic treatment prior to surgery. ¹⁰⁵ A study on the use of alcohol‐based hand rub found a reduction of pathogenic microbes without disturbing the skin commensals. ¹⁰⁶

Studies on the effect of hygiene procedures on other body skin areas are scarcer, but some interventions have induced a clinical improvement in certain skin conditions. After a three‐week selenium‐rich water balneotherapy treatment, the skin of psoriatic patients showed an increase in the level of the Xanthomonadaceae family, known to be keratolytic. ¹⁰⁷ In contrast, the compounds contained in hygiene and skin care products, which have a half‐life of up to 2 weeks once applied on the skin, can negatively impact stable microbial communities. ¹⁰⁸ Microbial shifts associated with personal care products are more pronounced for the armpit and feet than for the face. ¹⁰⁸ The use of deodorants and antiperspirants increases the abundance of Gram‐negative bacteria. ¹⁰⁸ Moreover, propylene glycol, a compound commonly used in such products, accumulates on the skin causing contact dermatitis in a subset of the population. ¹⁰⁹ On the other hand, in cosmetics, the use of probiotics to maintain or re‐establish skin homeostasis is gaining more attention. Lactobacillus plantarum‐GMNL6 displays beneficial effects on skin care like collagen synthesis, moisturizing, melanogenesis and antibiofilm formation. ¹¹⁰

3.5. Detergent use/ water hardness

When using hard water, frequent exposure to detergents and sodium lauryl sulphate as compared to deionized water. ¹¹¹ Surfactants in traditional soaps and soaps containing sodium lauryl sulphate can deposit more easily on the skin when hard water is used. ¹¹² This is due to the reduced solubility of surfactants in solutions containing metal ions, such as calcium. ¹¹³ The impact of chlorine levels in tap water on the skin microbiome remains uncertain. ¹¹⁴ , ¹¹⁵ Tap water contains high calcium carbonate levels which might particularly weaken the epidermal barrier. ¹¹⁶ , ¹¹⁷ Detergents and hard water are thought to impair skin barrier functions by increasing skin pH, solubilizing the stratum corneum lipids, altering the protein secondary structure on the skin, reducing a natural moisturizing factor, and upregulating protease activity. ¹¹¹ , ¹¹⁸ These changes may ultimately impact the skin microbiome.

3.6. Clothing/ laundry habits

Skin is constantly in contact with our clothes, thereby, continuously being exposed to chemicals and particles, which affect the homeostatic skin microbiota. ¹¹⁹ In the modern clothing industry, antimicrobial agents are typically incorporated during clothing production to control and prevent future odour development. Silver ions or nanoparticles (NPs) are common antimicrobial additives shown to have a higher impact on the metabolome than the microbiome by increasing the abundance of monounsaturated fatty acids correlated with opportunistic Cutibacterium presence. ¹²⁰ Further, crude flax fibres can inhibit S. aureus and S. epidermidis development and cotton and flax sterile extract can modulate biofilm formation by these bacteria. ¹²¹ Nevertheless, the impact of other textile additives and fibre types on the homeostatic skin microbiota require further research. The type of fibres, for example, polyester and nylon, can worsen symptoms of skin disorders. ¹²² , ¹²³

Additionally, direct skin contact leads to a continuous transfer of microbes and the formation of a textile microbiome. ¹²⁴ , ¹²⁵ Laundry habits further contribute to the textile microbiome and incorporate chemicals into the clothing that can affect the skin homeostasis and microbiota. ¹²⁴ A correlation was found between the frequent use of detergents and cosmetics and the loss of bacterial diversity on the skin commensals. ¹²⁶ Liquid detergents containing cytotoxic and irritant ingredients remove lipids from the skin, resulting in an impaired skin barrier integrity, thus acting as adjuvants for allergic sensitization. Also, a relationship was found between the preservatives in cosmetics and changes in the microbiota of healthy skin. ¹²⁷ , ¹²⁸ , ¹²⁹ , ¹³⁰ , ¹³¹

3.7. Socioeconomic status

The impact of socioeconomic status on the skin microbiome is not well studied. However, AD is generally more prevalent in higher socioeconomic regions and high‐income countries. ¹³² , ¹³³ Increased prevalence of AD is also associated with a higher level of family education, smaller family size and an urban environment. ¹³⁴ This is often related to a lower skin microbial diversity leading to higher abundances of pathogenic bacteria, such as S. aureus, which is strongly upregulated on lesional skin. Indian children born and raised in the United Kingdom and the United States of America are more susceptible to AD compared to their counterparts born and raised in India. ¹³⁵ In contrast, AD may be more severe in patients with lower socioeconomic status due to restricted access to health care. ¹³² The socioeconomic impact is important and can be strongly related to the environment, lifestyle and access to healthcare. ¹³⁶

4. ENVIRONMENTAL FACTORS

4.1. Urbanization, nature

Industrialization has undoubtedly affected our skin health and the skin microbiome. Skin microbial diversity richness significantly decreases with an increasing urbanization gradient and the use of more cleaning and cosmetic products. ¹²⁶ For example, the prevalence of AD has been on a steep rise since World War II. ¹³⁷

A study on the Amazon showed that an increasing urbanization gradient, going from a jungle settlement to a metropolis, correlated to major changes in skin bacterial, fungal and eukaryotic microbiome. ¹²⁶ Many environmental species and taxa that are not commonly associated with human skin decreased or nearly disappeared. ¹²⁶ In contrast, the commonly described skin microbiota, including Corynebacterium, Micrococcus, Pseudomonas and Enhydrobacter, became more enriched on skin surfaces with urbanization. ¹²⁶ An increased relative abundance of staphylococci and pathogenic fungi on the feet were associated with more frequent shoe use. ¹²⁶ The mycobiome also drastically changed in urbanized areas, with more frequently detected potentially pathogenic strains, for example, Aspergillus, Malassezia, Candida, and Eurotiales. In the jungle settlements, there were no reports of auto‐inflammatory disorders amongst the inhabitants.

A difference in the prevalence of AD is also seen in the border area of Finland and Russia, where a sharp boundary is found in the standard of living and health. Western society has a focus on a clean environment and little contact with nature and surroundings. On the Finnish side, over 25% of the adults (25‐54y) had AD symptoms and the prevalence of AD in children was 38.4% as compared to the Russian side of the border (only 10% of the adults and 7.7% in children reported AD). ¹³⁸ , ¹³⁹ A study from Madagascar concerning living in rural areas with close proximity to cattle showed that lifestyle (human–human interaction) and genetic factors override the microbial signature of close contact with animals, which had some weak effects on the human skin microbiome. ¹⁴⁰

4.2. Parasites

Intestinal saprophytes and helminths have co‐evolved with humans throughout the years. These parasites can rapidly skew the immune response toward an anti‐inflammatory (T helper (Th) 1 response) to secure their own survival, and alter or suppress Th2 immune responses, important for the development of allergic diseases. In the last decades, these intestinal parasites are rapidly disappearing. Improvement in socioeconomic status and hygiene has reduced exposure to parasites, which may be a plausible explanation for the increased burden of AD in India. ¹³⁵ Similarly, on the Russian side of the Finnish border, half of the investigated people had intestinal worms versus almost none on the Finnish side, where more allergies were reported. ¹⁴¹ , ¹⁴² However, no direct link between parasitic infections and their impact on the skin microbiome has been reported.

4.3. Indoor environment

In general, reported rates of AD are higher in Western countries than in developing countries. ¹⁴³ Numerous studies conducted in rural areas have found lower incidences of atopic and allergic diseases in children and adults growing up on farms, as compared to growing up in urban environments. ¹³⁹ , ¹⁴⁴ , ¹⁴⁵ , ¹⁴⁶ , ¹⁴⁷ , ¹⁴⁸ , ¹⁴⁹ , ¹⁵⁰ , ¹⁵¹ , ¹⁵² , ¹⁵³ , ¹⁵⁴ A high microbial diversity of the house dust was associated with a lower risk of allergic diseases. ¹⁵⁴ The most commonly studied microbial agent is endotoxin or lipopolysaccharide, derived from Gram‐negative bacteria. ¹⁵⁵ Differences in dust microbiota between Russian and Finnish households showed that the microbial load and diversity in house dust was much higher in Russian households, and contained more Gram‐positive taxa, including Staphylococcaceae and Corynebacteriaceae. ¹⁴² Similarly, bacterial diversity was remarkably higher in Finnish barn dust, while urban dust in Finnish households was generally dominated by Gram‐negative Proteobacteria. ¹⁴² Additionally, the microbial cell levels in drinking water can have an impact on the development of skin auto‐inflammatory diseases. Drinking water cell count was ten times higher on the Russian as compared to the Finnish side of the border, and as such, could be protective against later development of atopic disorders. ¹⁴¹

Having dogs and cats in early life and childhood was negatively associated with later development of atopic diseases. ¹³⁹ , ¹⁵⁶ , ¹⁵⁷ Having domestic pets can lead to a greater bacterial diversity in the house and on the skin of their owners. ¹⁵⁸ It is also known that domestic pets share their microbes with humans and affect our microbiota. ¹⁵⁹

Exposure to mould in the first year of life and the presence of visible mould in the house has been suggested to be associated with AD. ¹⁶⁰ , ¹⁶¹ Exposure to indoor mould can increase the risk of developing AD, as well as aggravating existing symptoms. ¹⁶⁰ Moulds and fungi produce toxins, proteases, enzymes and volatile organic compounds and they develop rapidly on food, surfaces and indoor environments. ¹⁶² Therefore, exposure to moulds and fungi should be avoided to reduce the risk of immune activation by disrupting the skin microbiome balance.

4.4. Pollutants

Living in an urban environment is linked to a greater exposure to environmental stressors, including particulate matter, volatile organic compounds, and dust. ¹⁶³ , ¹⁶⁴ Pollution can influence the bilateral relationship with the microbiome by impairing the stability of the microbial ecosystem and altering both the composition and functional capacities of the skin microbiota. ¹⁶⁵ Polycyclic aromatic hydrocarbons, a family of organic pollutants commonly found in air, can be inhaled, ingested, and absorbed through the skin, penetrating the human body and blood circulation. Prolonged exposure to polycyclic aromatic hydrocarbons is associated with changes in the microbiome's ability to metabolize carbohydrates, lipids, and amino acids, increased potential for pathogenicity, and the breakdown of aromatic compounds, which could be responsible for the worsening of skin conditions. ¹⁶⁵ Nitrogen dioxide can cause dysbiosis of skin microbiota. C. tuberculostearicum and S. capitis are particularly sensitive to nitrogen dioxide, whereas S. aureus is more resistant. ¹⁶⁶

Ozone is an unstable molecule that primarily targets the mucosa and skin surface. Animal studies have revealed that ozone exposure can cause oxidative stress, lipid peroxidation, and protein oxidation, suggesting that air pollution may induce barrier dysfunction. ¹⁶⁷ Additionally, a 10 μg/m³ rise in ozone has been associated with an increase in urticaria, eczema, contact dermatitis, rash, and infectious skin diseases. ¹⁶⁸ However, ozone is currently used as a therapy targeting dysbiosis to improve skin disorders. ¹⁶⁹ , ¹⁷⁰ Therapeutic small doses of ozone limit its toxicity, triggering a precisely calculated and acute oxidative stress. ¹⁷¹ Topical ozone significantly increased microbial diversity in the lesional skin of AD patients. ¹⁶⁹ , ¹⁷² , ¹⁷³ , ¹⁷⁴

Cigarette smoke also has a negative effect on skin health. Smoking is associated with changes in microbial β‐diversity and the relative abundance of many bacterial taxa on the skin. Nevertheless, some of the skin microbiota disruptions associated with smoking may be reversible. ¹⁷⁵

Further, inorganic NPs are widely utilized in the food industry, as cosmetics and drug delivery carriers in the medical field. This has resulted in a frequent interaction between NPs and the human microbiome. The effects of this interaction depend on the nature, structure and concentration of the NPs, and can range from destabilizing the microbiota to restoring it or showing no toxic effect. ¹⁷⁶ Inorganic NPs are the most commonly used type in commercial products, including supplements, foods, pharmaceuticals, and personal care products (e.g. sunscreen and toothpaste). Titanium dioxide and zinc oxide have antibacterial properties against S. aureus. Spherical and hierarchical flower‐like silver/ titanium dioxide composites have been found to have a higher bacteriostatic rate and improved antimicrobial activities. ¹⁷⁷ Additionally, the antibacterial effects of organic NPs, such as chitosan against Cutibacterium acnes have been investigated. Thus, NPs can be used to regulate the microbiota or to treat some associated diseases. ¹⁷⁶

4.5. Climate

The skin microbiome is generally stable under healthy conditions, and largely stable over time despite exposure to external environments. ⁴⁴ , ¹⁷⁸ By examining the diversity and function of the skin microbiome at differing body locations of individuals from China and Pakistan attending a single college in China, it was found that body location and ethnic background had an impact on the community structures, whereas season and gender only had an impact on the skin microbial community members. ¹⁷⁹

A temperature range of 33.2–35.0°C is optimal for the survival and growth of skin bacteria species, such as Staphylococcus, Propionibacteria, Micrococcus, Corynebacterium, and Acinetobacter. These bacteria demonstrate a better resistance to warmer temperatures and saltier conditions than other non‐commensal bacteria. Furthermore, skin bacterial growth is also likely to be stimulated by higher humidity and temperature. ¹⁸⁰ Changes in ambient conditions due to climate change, for example, heat waves or extended periods with/without rain, are therefore expected to exert increased effects on our skin conditions. Chronic cutaneous inflammatory dermatoses are expected to flare‐up during hot weather. ¹⁸¹ Furthermore, conditions of extreme heat and increased perspiration have been identified as contributing factors to Malassezia folliculitis colonization. HS‐patients are particularly vulnerable to changes in heat and humidity, as it affects the pilosebaceous unit. Additionally, high temperatures may increase the frequency of secondary infections caused by fungi and bacteria, such as Candida and S. aureus and floodings can cause cutaneous infections, immersion injuries, non‐infectious contact exposures, and can exacerbate existing skin diseases. Soft tissue infections are usually caused by pathogens, including S. aureus, S. pyogenes, and P. aeruginosa, which typically present as impetigo, cellulitis, and abscesses. ¹⁸¹

4.6. UV/sunlight

Synthesis of vitamin D controls the production of AMPs (e.g. β‐defensin and cathelicidin), which results in the inhibition of S. aureus and in a change in the microbial community. ¹⁸² Homeostatic skin microbiota act as a protective barrier against the noxious effects of UVR‐radiation (UVR). Skin commensals can lower immunosuppressive responses of skin cells by modulating cellular microenvironment and gene expression. ¹⁸³ However, UVR has qualitative and quantitative influences on the composition of the skin microbiota. ¹⁸⁴ UVR can affect the viability and re‐colonization potential of skin microbes, such as Lactobacillus spp, and influence the microbial production of specific metabolites, which can serve as biomarkers for radiation risk of developing sun‐related disorders. ¹⁸⁵ Increasing doses of UVB lead to reduced porphyrin production by facial Cutibacterium acnes in a dose‐dependent manner, which can occur before significant skin injury is detected. ¹⁸⁶ Therefore, unravelling the response of skin microbiome to UV will facilitate pre‐symptomatic diagnosis of sun‐related skin diseases.

The gut‐skin axis is the basis for the oral administration of prebiotics and probiotics to restore the homeostasis of skin microbiota and to protect against UVR. ¹⁸⁷ Several studies have shown that orally administrated probiotic lactic acid bacteria (e.g. Lactobacillus plantarum, L. reuteri and L. johnsonii) are promising anti‐photoaging agents based on their antioxidant and anti‐inflammatory capacities. ¹⁸⁸ , ¹⁸⁹ , ¹⁹⁰ , ¹⁹¹ , ¹⁹² Ingestion of probiotic Bifidobacterium breve has similar beneficial effects in protecting the skin barrier function after UVR exposure. ¹⁹³ , ¹⁹⁴ , ¹⁹⁵ Orally administered oligosaccharides are known to reduce/prevent transepidermal water loss, reduce erythema and prevent skin damage. ¹⁹⁶ Also, dietary supplementation of green tea extract has proven to modulate various skin metabolites related to skin barrier function after UVR‐stress, which may help prevent skin erythema formation. ¹⁹⁷ Alternatively, prebiotics and probiotics can be applied topically. Topical application of S. epidermis with glycerol ameliorates inflammation in chronic UVB‐exposed skin. ¹⁹⁸ S. epidermis ferments glycerol into butyric acid, which ultimately modulates the production of pro‐inflammatory cytokines induced by UVB. Moreover, glycerol enhances bacteria resistance to UVB (Figure 3). ¹⁹⁸ , ¹⁹⁹

FIGURE 3.

Gut‐skin axis and sunlight exposure. The gut‐skin axis plays an important role in skin homeostasis and skin immunity via the production of various metabolites and compounds. Topical and oral administration of pre‐ and probiotics modulate the fitness of both skin and gut microbiota and protect the skin barrier from UV sunlight. In turn, UV sunlight is used as a therapy to restore skin microbiota homeostasis.

UVR is also used as a therapy, that is, phototherapy, to improve skin barrier disorders, such as AD and psoriasis. In AD, microbial diversity at lesional skin sites increases after narrowband UVB (nb‐UVB; 311–312 nm) phototherapy and is accompanied by reduced proportions of S. aureus. ²⁰⁰ , ²⁰¹ , ²⁰² , ²⁰³ In addition, nb‐UVB phototherapy suppresses superantigen production. ²⁰³ In chronic plaque‐type psoriasis, nb‐UVB treatment increases the proportion of the genus Clostridium and decreases the proportion of the genus Pseudomonas in both lesional and non‐lesional skin, and increases the proportion of the genus Megasphaera in non‐lesional skin. ²⁰⁴

5. UNMET RESEARCH QUESTIONS AND CONCLUDING REMARKS

Despite an increasing interest in the field of skin and gut microbiome, the main focus has been on the investigation of the microbiome in diseased conditions, while maintaining a homeostatic microbiome has been underestimated. It is still unclear whether an unbalanced skin microbiome is the cause or the consequence of a skin disorder. What is clear is that many of the lifestyle and environmental factors that have been discussed are a result of Industrialization/urbanization, which is also related with the rise in atopic/ allergic and inflammatory disorders. Therefore, the main questions are: How can we maintain a healthy skin in an ‘increased risk’ environment? Which factors can we easily improve?

Focusing on the skin microbiome, we should first define what a homeostatic microbiome is in the 21st century and what the relative effect size of the skin microbiome is in keeping cutaneous homeostasis. Is it possible to have a homeostatic skin microbiome or are we all at risk of developing an inflammatory skin disease? Does restoration of the microbiome help to enhance the treatment response of inflammatory skin diseases? Is there a primordial skin microbiome that is residing in a protected ‘stem cell‐like’ niche and re‐colonizes the skin after ‘trauma’ such as wounds, disinfection, antibiotic use, environmental hazards or systemic disease? Can the skin microbiome be reprogrammed to be protective? Is the microbiome of the interfollicular epidermis different from the microbiome associated with the pilo‐sebaceous unit? Regarding the discussed factors affecting skin microbiome, the gut‐skin axis may play a pivotal role in keeping skin microbiome homeostatic. However, some unsolved questions arise: Which diet interventions and gut microbiota or gut microbiota‐derived metabolites help prevent inflammatory diseases? Which are the responsible mechanisms? Is there a direct link between intestinal parasites and the skin microbiota composition? Does it make sense to use probiotics when we are continuously exposed to harmful/ manipulating factors in the environment? Or should we adapt our lifestyle to keep our skin microbiome in shape? Another important factor modulating skin's health is the UV‐light exposure. Is UV‐light directly (bactericidal effect) or indirectly (UV‐induced immunomodulation, barrier damage…) affecting the skin microbiome? In times of increasing interest in healthy ageing, how can we take care of our skin microbiome? Does climate change enhance the prevalence of pathogens?

Finally, depending on the sampling method used to study skin microbiome (swab, tape strip, biopsy…), microbes residing at different depths are captured, therefore, impacting the reported skin microbial composition. There is a need for a universal consensus for skin microbiome sampling. Viruses are more challenging to collect for investigating their direct (pathogenic) role on the skin microbiome in homeostatic or diseased conditions, which could explain the limited knowledge of the role of the virome (especially bacteriophages) in this context. These aspects definitely deserve more attention.

With the present review, we aimed to provide an overview of lifestyle and environmental factors that affect our skin microbiome. Awareness of these factors influencing one another could be the basis of a prophylactic strategy to prevent the development of skin diseases or to be used as therapy (Figure 4). We propose that maintaining a resilient homeostatic microbiome might be critical to the prevention of disease over a lifetime. There are, however, still many open questions that need to be addressed; therefore, the research on this topic is further guaranteed.

FIGURE 4.

Take home message. Recommended practices to keep skin microbiota healthy based on the information compiled in this review.

HYGIENE MEASURES DURING COVID‐19.

Protective measures (e.g. gloves, face masks or hand sanitizers) taken during the SARS‐CoV‐2 pandemic affected the skin barrier function, inducing dryness, scales, papules or erythema, ²⁰⁵ , ²⁰⁶ Wearing face masks for prolonged times increased the severity of acne (´maskne´) and rosacea (mask rosacea). ²⁰⁷ , ²⁰⁸ , ²⁰⁹ Moreover, people with a defective skin barrier were also more prone to develop irritant contact dermatitis (ICD). ²¹⁰ , ²¹¹ An altered skin microenvironment with a higher temperature and increased sweat retention in a mask‐occlusive space lowered the microbial diversity and shifted the microbial proportions, ultimately leading to dermatoses. The mask‐wearing moist and warm environment favours the growth of dermatoses‐associated Staphylococcus and Corynebacterium and increases the susceptibility tβo Candida and Malassezia fungal infections, both common commensal of healthy skin. ²⁰⁸ , ²¹² , ²¹³

Early in the pandemic, maternal COVID‐19 was associated with an increased rate of caesarean delivery and restricted skin‐to‐skin contact in the perinatal period due to the lack of evidence on risks of transmission to the new‐born. C‐section and restricted skin‐to‐skin contact directly limit new‐born skin exposure to microbial stimuli from the mother's vagina and skin. It is known that birth and early life are critical periods for microbiome establishment and development, though the long‐term effects are still unclear. ²⁰⁹ , ²¹⁴ , ²¹⁵

Finally, although no specific information is available regarding the impact of limited socialization on the skin microbiota during the COVID pandemic, it is well defined that human behaviour plays a role in driving microbial dispersal and exchange. ²¹⁶

AUTHOR CONTRIBUTIONS

BH, CC, CGC, IKK, and LOM conceptualized the manuscript and suggested figures. BDP, CC, CDL, CGC, EU, IKK, MPG, MS, and ZU did the literature research. CGC wrote the abstract and designed the figures and graphical abstract. BH, CC, CDL, and CGC wrote chapters 1 and 2. CDL wrote chapter 3.1 and the information box on COVID‐19. BDP, CGC, CGM, EU, and MPG wrote chapter 3.2. IKK wrote chapter 3.3. CC, CDL, CGM and IKK wrote chapter 3.4. CC wrote chapter 3.5. CC, CDL, and BH wrote chapter 3.6. CC and CGM wrote chapter 3.7. CC wrote chapters 4.1, 4.2, 4.3, 4.5, 4.6, and 4.4. together with ZU. CGC and IKK wrote chapter 5 and designed the information boxes. HB, BDP, CDL, IKK and CGC formatted the references. All authors revised the manuscript and agreed with the final version.

CONFLICT OF INTEREST STATEMENT

MS has received research grants from the Swiss National Science Foundation, GSK, Novartis, Stiftung vorm. Bündner Heilstätte Arosa and OM Pharma as well as speaker's fee from AstraZeneca. The other authors declare that they do not have any conflict of interest to disclose in relation to this manuscript.

Kortekaas Krohn I, Callewaert C, Belasri H, et al. The influence of lifestyle and environmental factors on host resilience through a homeostatic skin microbiota: An EAACI Task Force Report. Allergy. 2024;79:3269‐3284. doi: 10.1111/all.16378

DATA AVAILABILITY STATEMENT

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.