The skin, as the largest organ of the human body,
provides a protective barrier against mechanical, microbial,
chemical and allergenic insults (1). The gastrointestinal tract, a
crucial mucosal immune organ, maintains immune homeostasis through
dynamic interactions between the microbiome and the intestinal
immune system (2). The
intestinal mucosal immune function is mediated by the mucus layer,
epithelial barrier and resident immune cells, all of which engage
with the gut microbiota (3). The
collective genome of gut microbes is termed the 'gut microbiome,'
which is intimately linked to long-term health (4). As interfaces with the external
environment, both the gut and skin host diverse microbial
communities and are richly innervated and vascularized. As early as
1930, John H. Stokes and Donald M. Pillsbury proposed an intrinsic
relationship between gut microbiota and skin inflammation,
conceptualizing the 'gut-skin axis' (5). Recent advances in microbiology and
immunology have begun to clarify the mechanisms through which gut
microbiota influences skin health. Lee and Sung (6) identified immune pathways by which
alterations in gut and skin microbiota contribute to
dermatopathology, while Szanto et al (7) suggested that gut microbiota
modulation may hold therapeutic potential for specific skin
disorders. These findings not only validate the gut-skin axis
theory but also open new avenues for clinical dermatology. In the
context of increasing antibiotic resistance, therapeutic strategies
are shifting toward alternatives such as probiotics, prebiotics and
dietary interventions, which can restore microbial balance and
modulate immune responses to improve skin health (8,9).
This review examines novel strategies for treating skin diseases
from the perspective of the gut-skin axis and explores future
translational research directions.
The gut microbiota comprises diverse and dynamic
microbial communities residing in the human gastrointestinal tract
(10) (Fig. 1A). Anatomically and functionally,
the gut is divided into the small and large intestines, each with
distinct physiological conditions and microbial populations
(11). Numerous factors
influence the gut microbiota (Fig.
1B), with diet being a primary determinant of its structure and
function (12). The gut
microbiota evolves from infancy and changes in composition and
diversity over time within an individual (13). There is considerable
interindividual variation in gut microbial composition. Through
host-microbe coevolution, the gut microbiome plays a critical role
in regulating host physiology, including metabolism, immune
development and behavioral responses (14,15).
As the body's outermost barrier, the skin is
continuously exposed to environmental factors and serves as the
first line of immune defense (16). The skin microbiota consists of
microbial communities adapted to the cutaneous environment through
long-term colonization, persisting in the chemical milieu of the
stratum corneum, sweat and sebaceous secretions (17). Environmental factors such as
ultraviolet radiation, temperature, humidity, sebum levels, oxygen
availability and pH create distinct ecological niches across skin
regions, leading to spatial variation in microbial composition
(18). Based on physiological
characteristics, Mahmud et al (19) classified skin into sebaceous
(e.g., between eyebrows), moist (e.g., forearm flexure) and dry
(e.g., palmar forearm) types. Lipophilic bacteria dominate
sebum-rich areas, whereas dry regions may support a more diverse
microbiota (Fig. 1C).
The 'gut-skin axis' theory is part of the broader
'gut-organ axis' framework, emphasizing bidirectional communication
between the gut and other organs via neurological, endocrine and
immune pathways (23). This
theory integrates multiple organs, the gut and the immune system
with the gut microbiota (24).
The gut and skin share structural and functional similarities,
including embryonic origin, symbiotic microbial communities,
innervation patterns and immune functions (19). As internal and external surfaces
in contact with the environment, they utilize similar signaling and
innervation pathways. T-cell-mediated immune responses often
manifest in both intestinal and cutaneous tissues (25).
The gut microbial community is central to
maintaining gut-skin homeostasis and underpins the gut-skin axis
theory (26). The gut microbiota
includes bacteria, fungi, parasites, protozoa and viruses, with
bacteria predominating (27).
Over 90% of gut bacteria belong to the Bacteroidetes and Firmicutes
phyla (28). The
Bacteroidota-to-Firmicutes ratio is commonly used to assess gut
microbiota characteristics and diversity (29). Gut bacteria can be categorized as
beneficial (e.g., Bifidobacteria, Lactobacillus) or opportunistic
pathogens (e.g., Staphylococci, Clostridia), which may cause
infection under certain conditions (30).
Alterations in gut microbiome composition,
metabolism and immunity can impact skin health. Manos (31) identified interspecies
communication within microbial communities as a key factor in
maintaining cutaneous homeostasis and responding to environmental
stressors, with dysregulation contributing to skin disease.
External factors such as genetics, diet, antimicrobials, and
lifestyle influence microbial diversity (32) (Fig. 2A).
Gut microbiota-derived metabolites mediate skin
interactions through short-chain fatty acids (SCFAs), tryptophan
metabolites and amine derivatives (e.g., trimethylamine N-oxide),
which exert systemic effects via specific receptors (36). SCFAs play important roles in
immune regulation; Trompette et al (37) demonstrated that gut-derived
butyrate enhances skin barrier function by modifying mitochondrial
metabolism in keratinocytes. Fang et al (38) reported that Bifidobacterium
longum produces indole derivatives that alleviate AD via the
tryptophan pathway. Tryptophan metabolites (e.g., indoleacetic
acid) are critical for maintaining intestinal and systemic immune
homeostasis (39) (Fig. 2B).
Bidirectional interaction between the gut microbiome
and skin health is central to the gut-skin axis theory. While most
evidence highlights gut microbes influencing skin health, Dokoshi
et al (43) demonstrated
that skin injury directly remodels the gut microbiome (Fig. 2B), providing experimental support
for bidirectional signaling and indicating that skin damage may
impair gut immune homeostasis. Long et al (44), in a two-sample Mendelian
randomization study, established a causal relationship between gut
microbiota and four common inflammatory skin diseases: Eczema,
acne, psoriasis and rosacea.
Understanding gut microbiota-skin interactions
offers novel mechanistic insights for managing dermatological
conditions. Clinical evidence reveals frequent comorbidity of skin
and intestinal disorders, such as enteropathic acrodermatitis (zinc
malabsorption causing dermatitis, alopecia and diarrhea) (45), and celiac disease (associated
with eczema, psoriasis and urticaria) (46).
Restoring gut microbiota balance enhances intestinal
barrier integrity and regulates immune responses (47). This involves upregulating
immunomodulatory cytokines (e.g., IL-10) (48) and suppressing pro-inflammatory
mediators (e.g., TNF-α) (49).
Clinical interventions include probiotics, prebiotics, synbiotics
and fecal microbiota transplantation (FMT) (50).
FMT involves transferring processed stool from
healthy donors to patients to rebuild gut microbiota. Initially
used for digestive diseases (51-53), FMT's efficacy depends on donor
and recipient factors (immune status, genetic diversity, gut
microbial composition) and treatment protocols (stool amount,
number of infusions, delivery route and adjuvant therapy) (54) (Fig. 2C).
While most FMT research focuses on gastrointestinal
disorders, recent trials suggest it may modulate systemic immune
responses, including in skin cancers like melanoma. Kim et
al (55) showed that FMT
improved AD symptoms in mice by restoring gut microbiota. FMT
enhances immunotherapy efficacy in cancer patients by modulating
gut microbiota (56). Melanoma,
the most common and prognostically worst skin cancer, is increasing
globally (57). Baruch et
al (58) observed that FMT
induced favorable changes in immune cell infiltration and gene
expression in intestinal and tumor microenvironments. Liu et
al (59) demonstrated that
FMT is effective for moderate to severe AD in adults, altering gut
microbiota composition and function. However, FMT carries risks;
Eshel et al (60) found
that while FMT capsules rarely transmit bloodstream pathogens
directly, they may indirectly promote bacterial translocation via
gut inflammation, potentially compromising intestinal barrier
integrity and increasing infection risk. Further in-depth studies
are required to ascertain the efficacy and safety of FMT in
treating other skin diseases.
Prebiotics are indigestible food components that
selectively stimulate beneficial bacteria (e.g.,
Bifidobacterium, Lactobacillus) while inhibiting
pathogenic overgrowth, thereby improving intestinal microecology
(61). Probiotics are live
microorganisms that, when administered in adequate amounts, confer
health benefits through intestinal colonization (62). These interventions show promise
beyond gastrointestinal and cardiovascular diseases (63,64) with emerging applications in
dermatology.
In oncology, gut microbiome modulation may enhance
immunotherapy efficacy. Specific probiotics influence
T-cell-mediated therapies (e.g., anti-programmed cell death 1,
chimeric antigen receptor-T) (68), though strain-specific effects
require further validation. Bender et al (69) demonstrated that Lactobacillus
reuteri translocates to melanoma sites in mice, secreting
indole-3-aldehyde to activate CD8+ T-cell receptors and potentiate
immunotherapy. Such mechanisms hold potential for future
immunomodulatory strategies pending resolution of delivery
challenges and dose optimization.
Psoriasis is an immune-mediated skin disease
characterized by abnormal keratinocyte proliferation and
differentiation, posing significant physical and psychological
burdens (70). Previous studies
suggested gut microbiota dysbiosis in patients with psoriasis, but
the relationship remained vague (71). Zang et al (72) used bidirectional Mendelian
randomization to identify Pasteurellaceae, Brucella
and Methanobrevibacter smithii as potential pathogenic
contributors, suggesting microbial targets for therapy (Table I). Zhao et al (73) demonstrated through metabolomics
that gut microbiota transplantation from severely affected mice
exacerbated skin inflammation in mild cases, while a
phosphodiesterase-4 inhibitor alleviated symptoms and restored the
gut microbiota, providing a theoretical basis for gut
microbiota-skin axis-based psoriasis treatment (Table I).
AD is a common chronic inflammatory skin disease
characterized by persistent itching and eczematous rash (74). It increases the risk of
comorbidities like food allergies, asthma, allergic rhinitis and
mental health disorders (75).
The pathogenesis involves hereditary immune dysregulation, skin
barrier dysfunction and environmental factors (76). The gut microbiota modulates
immune system development, implying a key role in AD (77).
First-line AD treatment includes topical
corticosteroids and calcineurin inhibitors (e.g., pimecrolimus,
tacrolimus). For moderate to severe cases, ultraviolet phototherapy
is used adjunctively (78).
Probiotic supplementation is increasingly used, particularly in
children, to modulate gut microbiota and regulate immune responses
(79,80). Meta-analyses indicate certain
probiotics reduce Scoring Atopic Dermatitis indices in adults
(81). Fang et al
(82) showed that
Bifidobacterium CCFM16 and Lactobacillus plantar
CCFM8610 specifically improve AD by altering gut microbiota
composition and function (Table
I).
AV is a chronic inflammatory skin disease affecting
sebaceous units, characterized by comedones, papules, pustules,
nodules and scars, typically on the face, upper trunk and
extremities (83). The global
prevalence is estimated at 8.96% in men and 9.81% in women
(84). The pathogenesis involves
multifactorial mechanisms, with pubertal sebum hypersecretion being
a key factor. AV often persists into adulthood with distinct
features (85). Androgens and
testosterone regulate sebum production, explaining why males often
experience more severe symptoms (86).
Gut dysbiosis may exacerbate AV through upregulated
insulin-like growth factor 1 signaling, insulin resistance and
systemic pro-inflammatory cytokines (87). First-line treatments include
topical retinoids, azelaic acid and benzoyl peroxide (88). The role of gut microbiota
modulation via probiotics in improving AV is underexplored. Jung
et al (89) found that
probiotic-antibiotic combination therapy synergistically reduced
inflammation and antibiotic side effects. Fabbrocini et al
(90) showed that
Lactobacillus rhamnosus SP1 (LSP1) probiotic normalized skin
insulin signaling gene expression. Eguren et al (91) conducted a 12-week trial with
Lactobacillus rhamnosus and Arthrospira in patients
with AV aged 12-30 years, finding the probiotic adjunct safe and
effective (Table I).
Rosacea is a chronic recurrent inflammatory skin
condition affecting the central face (forehead, nose, cheeks, chin)
(92). It is classified into
erythematotelangiectatic, papulopustular, phymatous and ocular
subtypes (93).
According to 2021 guidelines, urticaria is
classified as acute (lasting <6 weeks) or chronic urticaria
(CU). CU is a common inflammatory skin disorder involving mast
cell-mediated allergy and autoimmunity, characterized by recurrent
wheals, angioedema and itching lasting ≥6 weeks (99). Pathophysiology involves immune
dysregulation, inflammatory cascade imbalance and
coagulation-fibrinolytic activation (100). CU subtypes include chronic
spontaneous urticaria (CSU) and chronic inducible urticarial
(101).
Vitiligo is a depigmentation disorder affecting
0.5-2% globally, with a genetic component (106). It presents as white, scaleless
patches (107).
Pathophysiologically, vitiligo is an autoimmune condition where
melanocytes are sensitive to oxidative stress, triggering
inflammatory cytokine release and innate immune activation.
CD8+ T cells destroy melanocytes, driven by IFN-γ.
Oxidative stress may induce gut dysbiosis, promoting autoimmunity.
IFN-γ blockade therapies temporarily reverse depigmentation but
relapse occurs upon cessation (108). The chronic course of vitiligo
affects patients' appearance and psychological well-being;
Kussainova et al (109)
reported a 35.8% anxiety prevalence, higher in women.
Current evidence on the gut-vitiligo link is
limited. Emerging studies suggest gut microbiome involvement. Hadi
et al (110) reported
vitiligo-inflammatory bowel disease comorbidity. Ni et al
(111) documented a
Firmicutes/Bacteroidetes ratio reduction in patients
with vitiligo (Table I), while
Luan et al (112)
observed decreased microbial alpha diversity with altered
cysteine/galactose metabolism (Table
I). These findings support the gut-microbiota-skin hypothesis
but require further investigation for therapeutic applications.
Skin cancer is the fifth most common cancer
globally, with its incidence rising (113). It arises from genetic defects
or DNA mutations in skin cells, primarily due to ultraviolet
exposure (114). Skin cancers
are classified as malignant melanoma (MM) or non-melanoma skin
cancer (NMSC). MM originates from melanocytes, while NMSC (e.g.,
squamous cell carcinoma, basal cell carcinoma) arises from
epidermal cells (115).
Treatments include cryotherapy, radiotherapy and photodynamic
therapy, but novel approaches are needed (116).
MM is highly metastatic, has a poor prognosis and is
the leading cause of death among patients with skin cancer
(117). Mrazek et al
(118) found compositional
differences between melanoma and healthy skin microbiomes, with
elevated Fusobacterium and Eubacterium in tumors
(Table I). Mekadim et al
(119) demonstrated distinct
gut and skin microbiome profiles in melanoma models, addressing
knowledge gaps (Table I).
Several studies confirmed that the gut microbiota
can modulate the response to cancer immune checkpoint blockade
therapy (120-122). Spencer et al (123) reported improved
progression-free survival in ICB-treated patients with higher fiber
intake, particularly without probiotics; fiber/prebiotics enhanced
antitumor T-cell responses via microbiome modulation (Table I). Routy et al (124)'s phase I trial confirmed FMT
safety combined with first-line melanoma therapy, though efficacy
requires further validation (Fig.
2D) (Table I). Future
investigations of the gut-skin axis may yield innovative
therapeutic strategies for skin cancer.
Rare dermatoses like AIBD and LP receive limited
research due to funding and recruitment challenges (125). AIBD involve chronic
immune-mediated blistering, with fragile cutaneous/mucosal vesicles
rupturing into erosions. These include pemphigus vulgaris (PV),
bullous pemphigoid (BP) and mucous membrane pemphigoid (126). PV subtypes include vulgaris,
foliaceus, IgA pemphigus and paraneoplastic pemphigus. BP, the most
common pemphigoid, features tense, rupture-resistant subepidermal
blisters, often involving the oropharyngeal and ocular mucosa. It
primarily affects adults aged >50 years but can also occur in
younger individuals (127).
Pemphigus has a long course and poor prognosis,
severely affecting patients' quality of life, with most deaths due
to uncontrollable secondary infections (128). The pathogenesis involves
Th1/Th2 and Th17/Treg imbalances, leading to IgG autoantibodies
that target epidermal/mucosal antigens, causing loss of cell
adhesion and blister formation (129).
LP is a chronic inflammatory disease presenting as
violaceous pruritic papules on skin, mucosa or nails. Subtypes
include cutaneous LP (CLP) and oral LP (OLP), with possible
esophageal, genital or nail involvement (132). The prevalence of LP ranges from
0.22 to 1%, with OLP about five times more common than CLP
(133). Genital subtypes have
been reported (134), and
concurrent subtypes complicate diagnosis (135). The pathogenesis of CLP involves
cell-mediated immune responses against basal keratinocytes
(136). Georgescu et al
(137) reported an
oxidant-antioxidant imbalance in patients with LP, suggesting
oxidative stress plays a role.
Few studies have focused on the role of the 'gut
microbe-skin axis' in rare skin diseases such as LP and pemphigus
(22). Li et al (138) observed a distinct gut
microbiota in patients with active pemphigus, with
Prevotella spp. and Coriobacteriaceae abundance
correlating with autoantibodies. Roy et al (139) reviewed intestinal
microecological dysregulation in several rare diseases, including
LP, and highlighted the complexity of host-microbiota interactions,
emphasizing knowledge gaps, the need for improved study designs,
and the promise of microbiome-based therapeutics. Kamal et
al (140)'s trial on 60
patients with OLP showed a greater reduction in pain and
Thongprasom scores with combined clobetasol/probiotic therapy vs.
clobetasol alone. Despite research challenges, such as scarce
pathogenic data and small cohorts, elucidating microbiota-skin
interactions could yield novel diagnostics and therapies for rare
dermatoses.
Despite progress, translating gut microbiome
research into clinical applications remains challenging.
Methodological limitations in data collection, representativeness
and analysis are key barriers. Resources like GMrepo (https://gmrepo.humangut.info/home) and gutMGene
(https://bio-computing.hrbmu.edu.cn/gutmgene/#/home)
provide valuable data, but heterogeneity due to geographic,
demographic and lifestyle factors complicates sampling and
standardization (Fig. 2A). The
lack of a consensus definition for 'healthy gut microbiota' impedes
benchmark establishment (141,142).
Patient and provider acceptance barriers persist,
especially in culturally conservative settings. Probiotics, though
generally safer than FMT, carry risks such as bacteremia in
immunocompromised hosts and horizontal gene transfer (152,153). Cases like Lactobacillus
rhamnosus infections in immunosuppressed individuals underscore
the need for further safety research (154-156).
Preclinical gut microbiome research will continue
diversifying. International data-sharing collaborations may
overcome ethnographic limitations (157). Integrating medicine, biology
and informatics could expand the research scope, as seen in machine
learning applications for microbial community analysis (158). Current algorithms predict
health status and identify disease-microbiome associations through
differential abundance analysis (159).
In clinical translation, precision medicine
requires refinement. Longitudinal studies with larger cohorts may
better evaluate probiotic efficacy across populations, informing
targeted microbiome-based interventions using adaptive trial
designs (e.g., cluster randomized controlled trials). These
frameworks would strengthen disease prevention and treatment
strategies.
Emerging technologies like high-intensity
ultrasound show potential for enhancing functional food development
by improving probiotic stability and bioactivity (160), Future validation studies should
assess gut health optimization and personalized approaches
(161,162). Beyond dairy probiotics,
fermented foods and beverages are demonstrating health benefits
(163,164).
The following conclusions can be drawn from the
present review: i) The gut-skin axis framework highlights the
influence of gut microbiota on skin homeostasis, with dysbiosis
implicated in psoriasis, AD, acne and AIBD; ii) the gut microbiota
modulates skin health through immune regulation, microbial
metabolite production (e.g., SCFAs) and systemic inflammation
control. FMT, probiotics and prebiotics show promise in restoring
microbial balance and reducing inflammation, though larger trials
are needed; iii) current evidence primarily establishes
correlations, but causal relationships require validation via
multi-omics approaches integrating genomics, metabolomics and
immune profiling; iv) clinical translation faces challenges
including methodological limitations, ethical concerns with FMT and
insufficient long-term safety data for probiotics; v) mechanistic
insights into rare skin diseases via the gut-skin axis are scarce,
warranting targeted investigations; vi) future research should
prioritize patient-specific microbiome interventions,
machine-learning diagnostics and cross-disciplinary collaboration
(e.g., dermatology-gastroenterology-bioinformatics) to advance
precision dermatology; and vii) the gut-skin axis redefines
skincare paradigms, emphasizing gut health as integral to
dermatological wellness, with breakthroughs in microbiome
engineering and Artificial Intelligence-driven interventions
offering transformative potential.
Not applicable.
YZ performed the analyses and wrote the first draft
of the manuscript. CY, JZ, QY, XZ and XZ performed the literature
search and discussed and edited the manuscript. XZ and XZ
supervised the preparation of the manuscript. Data authentication
is not applicable. All authors have read and approved the final
manuscript.
Not applicable.
Not applicable.
The authors declare that they have no competing
interests.
Not applicable.
This study was partially supported by the National Natural
Science Foundation of China (grant nos. 32170915 and 82172931).
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