Advertisement
Research Article| Volume 39, ISSUE 5, P829-839, September 2021

The skin microbiome and the gut-skin axis

      Abstract

      The microbiome plays a significant role in human health, homeostasis, immune system, and disease pathogenesis. Disrupted communication between the microbiome and host has been extensively studied in gastrointestinal diseases. To a lesser extent, there is emerging research on the skin microbiome and its connection with the gut, referred to as the gut-skin axis and its effects on dermatologic conditions. A basic overview will be provided of the gut and skin microbiome with a focus on the impact of this connection on cutaneous diseases, such as psoriasis, atopic dermatitis, rosacea, acne vulgaris, photoaging, and cutaneous wounds. In addition, we shall discuss nutrition-based approaches mediated through the gut-skin axis and topical treatments that could serve as potential adjunctive management by manipulation of the microbiome. In particular, there is a growing body of research on oral probiotics, prebiotics, and dietary modifications that may help improve symptoms for a variety of dermatologic conditions in select demographic groups.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinics in Dermatology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Gallo RL.
        Human skin is the largest epithelial surface for interaction with microbes.
        J Invest Dermatol. 2017; 137: 1213-1214
        • Cui L
        • Jia Y
        • Cheng ZW
        • et al.
        Advancements in the maintenance of skin barrier/skin lipid composition and the involvement of metabolic enzymes.
        J Cosmet Dermatol. 2016; 15: 549-558
        • Lederberg J.
        Infectious history.
        Science. 2000; 288: 287-293
        • Amon P
        • Sanderson I.
        What is the microbiome?.
        Arch Dis Child Educ Pract Ed. 2017; 102: 257-260
        • Dréno B
        • Araviiskaia E
        • Berardesca E
        • et al.
        Microbiome in healthy skin, update for dermatologists.
        J Eur Acad Dermatol Venereol. 2016; 30: 2038-2047
        • Bay L
        • Barnes CJ
        • Fritz BG
        • et al.
        Universal dermal microbiome in human skin.
        mBio. 2020; 11 (-19): e02945
        • Byrd AL
        • Belkaid Y
        • Segre JA.
        The human skin microbiome.
        Nat Rev Microbiol. 2018; 16: 143-155
        • Costello EK
        • Lauber CL
        • Hamady M
        • et al.
        Bacterial community variation in human body habitats across space and time.
        Science. 2009; 326: 1694-1697
        • Fredricks DN.
        Microbial ecology of human skin in health and disease.
        J Investig Dermatol Symp Proc. 2001; 6: 167-169
        • Grice EA
        • Kong HH
        • Conlan S
        • et al.
        Topographical and temporal diversity of the human skin microbiome.
        Science. 2009; 324: 1190-1192
        • Kong HH
        • Oh J
        • Deming C
        • et al.
        Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis.
        Genome Res. 2012; 22: 850-859
        • Mukherjee S
        • Mitra R
        • Maitra A
        • et al.
        Sebum and hydration levels in specific regions of human face significantly predict the nature and diversity of facial skin microbiome.
        Sci Rep. 2016; 6: 36062
        • Oh J
        • Conlan S
        • Polley EC
        • Segre JA
        • Kong HH.
        Shifts in human skin and nares microbiota of healthy children and adults.
        Genome Med. 2012; 4: 77
        • Agans R
        • Rigsbee L
        • Kenche H
        • et al.
        Distal gut microbiota of adolescent children is different from that of adults.
        FEMS Microbiol Ecol. 2011; 77: 404-412
        • Rajilić-Stojanović M
        • Heilig HG
        • Tims S
        • Zoetendal EG
        • de Vos WM.
        Long-term monitoring of the human intestinal microbiota composition [e-pub ahead of print].
        Environ Microbiol. 2012; 15 (accessed): 1146-1159https://doi.org/10.1111/1462-2920.12023
        • Grice EA
        • Segre JA.
        The skin microbiome.
        Nat Rev Microbiol. 2011; 9: 244-253
        • Huang R
        • Ning H
        • Shen M
        • et al.
        Probiotics for the treatment of atopic dermatitis in children: a systematic review and meta-analysis of randomized controlled trials.
        Front Cell Infect Microbiol. 2017; 7: 392
        • Makrgeorgou A
        • Leonardi-Bee J
        • Bath-Hextall FJ
        • et al.
        Probiotics for treating eczema.
        Cochrane Database Syst Rev. 2018; 11CD006135
        • Thomas CL
        • Fernández-Peñas P.
        The microbiome and atopic eczema: more than skin deep.
        Australas J Dermatol. 2017; 58: 18-24
        • Noble WC.
        Cornyeform bacteria, infection and immunity.
        in: Delves PJ Roitt IM Encyclopedia of Immunology. 2nd ed. Academic Press, Cambridge, MA1998: 661-663
        • Feingold AR
        • Meislich D.
        Anaerobic gram-positive nonsporulating bacilli (including actinomyces).
        in: Long SS Prober CG Fischer M Principles and Practice of Pediatric Infectious Diseases. 5th ed. Elsevier, Philadelphia, PA2018: 1019-1022
        • Szántó M
        • Dózsa A
        • Antal D
        • et al.
        Targeting the gut-skin axis-probiotics as new tools for skin disorder management?.
        Exp Dermatol. 2019; 28: 1210-1218
        • Christensen GJ
        • Brüggemann H.
        Bacterial skin commensals and their role as host guardians.
        Benef Microbes. 2014; 5: 201-215
        • Cavalieri S
        • Knoop F
        Corynebacterium infections.
        in: Enna SJ Byland DB xPharm: The Complete Pharmacology Reference. Biomedical Sciences, Boston, MA2007: 1-5
        • Kolios AGA
        • Cozzio A
        • Zinkernagel AS
        • et al.
        Cutaneous corynebacterium infection presenting with disseminated skin nodules and ulceration.
        Case Rep Dermatol. 2017; 9: 8-12
        • Quan C
        • Chen XY
        • Li X
        • et al.
        Psoriatic lesions are characterized by higher bacterial load and imbalance between Cutibacterium and Corynebacterium.
        J Am Acad Dermatol. 2020; 82: 955-961
        • Cogen AL
        • Nizet V
        • Gallo RL.
        Skin microbiota: a source of disease or defence?.
        Br J Dermatol. 2008; 158: 442-455
        • Vaughn AR
        • Notay M
        • Clark AK
        • et al.
        Skin-gut axis: the relationship between intestinal bacteria and skin health.
        World J Dermatol. 2017; 6: 52-58
        • Namvar AE
        • Bastarahang S
        • Abbasi N
        • et al.
        Clinical characteristics of Staphylococcus epidermidis: a systematic review.
        GMS Hyg Infect Control. 2014; 9: Doc23
        • Iwatsuki K
        • Yamasaki O
        • Morizane S
        • et al.
        Staphylococcal cutaneous infections: invasion, evasion and aggression.
        J Dermatol Sci. 2006; 42: 203-214
        • Kong HH
        • Segre JA.
        The molecular revolution in cutaneous biology: investigating the skin microbiome.
        J Invest Dermatol. 2017; 137: e119-e122
        • Baron S.
        Medical microbiology.
        University of Texas Medical Branch at Galveston, Galveston, TX1996
        • Ferretti JJ
        • Stevens DL
        • Fischetti VA.
        Streptococcus pyogenes: basic biology to clinical manifestations [internet].
        University of Oklahoma Health Sciences Center, Oklahoma City, OK2016
        • Limon JJ
        • Tang J
        • Li D
        • et al.
        Malassezia is associated with Crohn's disease and exacerbates colitis in mouse models.
        Cell Host Microbe. 2019; 25 (e376): 377-388
        • Alberts B
        • Johnson A
        • Lewis J
        • et al.
        Innate immunology of the cell.
        Molecular Biology of the Cell. 4th ed. Garland Science, New York, NY2002
        • Picardo M
        • Ottaviani M.
        Skin microbiome and skin disease: the example of rosacea.
        J Clin Gastroenterol. 2014; 48: S85-S86
        • Yu Y
        • Dunaway S
        • Champer J
        • et al.
        Changing our microbiome: probiotics in dermatology.
        Br J Dermatol. 2020; 182: 39-46
        • Maguire M
        • Maguire G.
        The role of microbiota, and probiotics and prebiotics in skin health.
        Arch Dermatol Res. 2017; 309: 411-421
        • Braff MH
        • Bardan A
        • Nizet V
        • et al.
        Cutaneous defense mechanisms by antimicrobial peptides.
        J Invest Dermatol. 2005; 125: 9-13
        • Nakatsuji T
        • Chen TH
        • Narala S
        • et al.
        Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis.
        Sci Transl Med. 2017; 9: eaah4680
        • Laforest-Lapointe I
        • Arrieta MC.
        Microbial eukaryotes: a missing link in gut microbiome studies. mSystems. 2018; 3 (-17): e00201
        • Nkamga VD
        • Henrissat B
        • Drancourt M.
        Archaea: essential inhabitants of the human digestive microbiota.
        Human Microbiome J. 2016; 3: 1-8
        • Thursby E
        • Juge N.
        Introduction to the human gut microbiota.
        Biochem J. 2017; 474: 1823-1836
        • Bäckhed F
        • Ley RE
        • Sonnenburg JL
        • et al.
        Host-bacterial mutualism in the human intestine.
        Science. 2005; 307: 1915-1920
        • Bengmark S.
        Gut microbiota, immune development and function.
        Pharmacol Res. 2013; 69: 87-113
        • Wexler HM.
        Bacteroides: the good, the bad, and the nitty-gritty.
        Clin Microbiol Rev. 2007; 20: 593-621
        • Wright DP
        • Rosendale DI
        • Robertson AM.
        Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucin.
        FEMS Microbiol Lett. 2000; 190: 73-79
        • Salem I
        • Ramser A
        • Isham N
        • et al.
        The gut microbiome as a major regulator of the gut-skin axis.
        Front Microbiol. 2018; 9: 1459
        • Ivanov II
        • Atarashi K
        • Manel N
        • et al.
        Induction of intestinal Th17 cells by segmented filamentous bacteria.
        Cell. 2009; 139: 485-498
        • Honda K
        • Littman DR.
        The microbiota in adaptive immune homeostasis and disease.
        Nature. 2016; 535: 75-84
        • Maslowski KM
        • Vieira AT
        • Ng A
        • et al.
        Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43.
        Nature. 2009; 461: 1282-1286
        • O'Neill CA
        • Monteleone G
        • McLaughlin JT
        • et al.
        The gut-skin axis in health and disease: a paradigm with therapeutic implications.
        Bioessays. 2016; 38: 1167-1176
        • Saarialho-Kere U.
        The gut-skin axis.
        J Pediatr Gastroenterol Nutr. 2004; 39: S734-S735
        • Huang BL
        • Chandra S
        • Shih DQ.
        Skin manifestations of inflammatory bowel disease.
        Front Physiol. 2012; 3: 13
        • Arck P
        • Handjiski B
        • Hagen E
        • et al.
        Is there a ‘gut-brain-skin axis’?.
        Exp Dermatol. 2010; 19: 401-405
        • Ellis SR
        • Nguyen M
        • Vaughn AR
        • et al.
        The skin and gut microbiome and its role in common dermatologic conditions.
        Microorganisms. 2019; 7: 550
        • Codoñer FM
        • Ramírez-Bosca A
        • Climent E
        • et al.
        Gut microbial composition in patients with psoriasis.
        Sci Rep. 2018; 8: 3812
        • Miyazaki K
        • Masuoka N
        • Kano M
        • et al.
        Bifidobacterium fermented milk and galacto-oligosaccharides lead to improved skin health by decreasing phenols production by gut microbiota.
        Benef Microbes. 2014; 5: 121-128
        • Cani PD
        • Amar J
        • Iglesias MA
        • et al.
        Metabolic endotoxemia initiates obesity and insulin resistance.
        Diabetes. 2007; 56: 1761-1772
        • Ramírez-Boscá A
        • Navarro-López V
        • Martínez-Andrés A
        • et al.
        Identification of bacterial DNA in the peripheral blood of patients with active psoriasis.
        JAMA Dermatol. 2015; 151: 670-671
        • Scher JU
        • Ubeda C
        • Artacho A
        • et al.
        Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease.
        Arthritis Rheumatol. 2015; 67: 128-139
        • Lyte M.
        Microbial endocrinology and the microbiota-gut-brain axis.
        Adv Exp Med Biol. 2014; 817: 3-24
        • Rea K
        • Dinan TG
        • Cryan JF.
        The microbiome: a key regulator of stress and neuroinflammation.
        Neurobiol Stress. 2016; 4: 23-33
        • Afzal R
        • Shim WS.
        Glucosylsphingosine activates serotonin receptor 2a and 2b: implication of a novel itch signaling pathway.
        Biomol Ther (Seoul). 2017; 25: 497-503
        • Peters EM
        • Michenko A
        • Kupfer J
        • et al.
        Mental stress in atopic dermatitis–neuronal plasticity and the cholinergic system are affected in atopic dermatitis and in response to acute experimental mental stress in a randomized controlled pilot study.
        PLoS One. 2014; 9e113552
        • Li ZJ
        • Park SB
        • Sohn KC
        • et al.
        Regulation of lipid production by acetylcholine signalling in human sebaceous glands.
        J Dermatol Sci. 2013; 72: 116-122
        • Makrantonaki E
        • Ganceviciene R
        • Zouboulis C.
        An update on the role of the sebaceous gland in the pathogenesis of acne.
        Dermatoendocrinol. 2011; 3: 41-49
        • Kligman AM.
        An overview of acne.
        J Invest Dermatol. 1974; 62: 268-287
        • Islam SA
        • Luster AD.
        T cell homing to epithelial barriers in allergic disease.
        Nat Med. 2012; 18: 705-715
        • Kulig M
        • Bergmann R
        • Klettke U
        • et al.
        Natural course of sensitization to food and inhalant allergens during the first 6 years of life.
        J Allergy Clin Immunol. 1999; 103: 1173-1179
        • Noti M
        • Kim BS
        • Siracusa MC
        • et al.
        Exposure to food allergens through inflamed skin promotes intestinal food allergy through the thymic stromal lymphopoietin-basophil axis.
        J Allergy Clin Immunol. 2014; 133 (1399.e1391-1396): 1390-1399
        • Mondoulet L
        • Dioszeghy V
        • Puteaux E
        • et al.
        Specific epicutaneous immunotherapy prevents sensitization to new allergens in a murine model.
        J Allergy Clin Immunol. 2015; 135 (e1544): 1546-1557
        • Bienenfeld A
        • Nagler AR
        • Orlow SJ.
        Oral antibacterial therapy for acne vulgaris: an evidence-based review.
        Am J Clin Dermatol. 2017; 18: 469-490
        • Kosmadaki M
        • Katsambas A.
        Topical treatments for acne.
        Clin Dermatol. 2017; 35: 173-178
        • Osborn DA
        • Sinn JK.
        Prebiotics in infants for prevention of allergy.
        Cochrane Database Syst Rev. 2013; CD006474
        • Seite S
        • Flores GE
        • Henley JB
        • et al.
        Microbiome of affected and unaffected skin of patients with atopic dermatitis before and after emollient treatment.
        J Drugs Dermatol. 2014; 13: 1365-1372
        • Seité S
        • Zelenkova H
        • Martin R.
        Clinical efficacy of emollients in atopic dermatitis patients - relationship with the skin microbiota modification.
        Clin Cosmet Investig Dermatol. 2017; 10: 25-33
        • Navarro-López V
        • Martínez-Andrés A
        • Ramírez-Boscá A
        • et al.
        Efficacy and safety of oral administration of a mixture of probiotic strains in patients with psoriasis: a randomized controlled clinical trial.
        Acta Derm Venereol. 2019; 99: 1078-1084
        • Parodi A
        • Paolino S
        • Greco A
        • et al.
        Small intestinal bacterial overgrowth in rosacea: clinical effectiveness of its eradication.
        Clin Gastroenterol Hepatol. 2008; 6: 759-764
        • Lev-Tov H
        • Rill JS
        • Liu G
        • et al.
        Trends in utilization of topical medications for treatment of rosacea in the United States (2005-2014): a cohort analysis.
        J Am Acad Dermatol. 2019; 80: 1135-1137
        • van Zuuren EJ
        • Fedorowicz Z.
        Interventions for Rosacea.
        JAMA. 2015; 314: 2403-2404
        • Fabbrocini G
        • Bertona M
        • Picazo Ó
        • et al.
        Supplementation with Lactobacillus rhamnosus SP1 normalises skin expression of genes implicated in insulin signalling and improves adult acne.
        Benef Microbes. 2016; 7: 625-630
        • Jung GW
        • Tse JE
        • Guiha I
        • et al.
        Prospective, randomized, open-label trial comparing the safety, efficacy, and tolerability of an acne treatment regimen with and without a probiotic supplement and minocycline in subjects with mild to moderate acne.
        J Cutan Med Surg. 2013; 17: 114-122
        • Kim J
        • Ko Y
        • Park YK
        • et al.
        Dietary effect of lactoferrin-enriched fermented milk on skin surface lipid and clinical improvement of acne vulgaris.
        Nutrition. 2010; 26: 902-909
      1. AOBiome Therapeutics. Press releases. October 19, 2017. AOBiome therapeutics reports positive efficacy results from phase 2b clinical trial of ammonia oxidizing bacteria (AOB) for the treatment of acne vulgaris. Available at: https://www.aobiome.com/pressreleases/aobiome-therapeutics-reports-positive-efficacy-results-from-phase-2b-clinical-trial-of-ammonia-oxidizing-bacteria-aob-for-the-treatment-of-acne-vulgaris/. Accessed March 15, 2020.

        • Gueniche A
        • Philippe D
        • Bastien P
        • et al.
        Oral supplementation with probiotic Lactobacillus paracasei ST-11 improves dandruff condition.
        Int J Trichology. 2011; 3: S22
        • Reygagne P
        • Bastien P
        • Couavoux MP
        • et al.
        The positive benefit of Lactobacillus paracasei NCC2461 ST11 in healthy volunteers with moderate to severe dandruff.
        Benef Microbes. 2017; 8: 671-680
        • Guéniche A
        • Cathelineau AC
        • Bastien P
        • et al.
        Vitreoscilla filiformis biomass improves seborrheic dermatitis.
        J Eur Acad Dermatol Venereol. 2008; 22: 1014-1015
        • Peguet-Navarro J
        • Dezutter-Dambuyant C
        • Buetler T
        • et al.
        Supplementation with oral probiotic bacteria protects human cutaneous immune homeostasis after UV exposure-double blind, randomized, placebo controlled clinical trial.
        Eur J Dermatol. 2008; 18: 504-511
        • Keshari S
        • Balasubramaniam A
        • Myagmardoloonjin B
        • et al.
        Butyric acid from probiotic staphylococcus epidermis in the skin microbiome down-regulates the ultraviolet-induced pro-inflammatory il-6 cytokine via short-chain fatty acid receptor.
        Int J Mol Sci. 2019; 20: 4477
        • Notay M
        • Saric-Bosanac S
        • Vaughn AR
        • et al.
        The use of topical Nitrosomonas eutropha for cosmetic improvement of facial wrinkles.
        J Cosmet Dermatol. 2020; 19: 689-693
        • Fijan S
        • Frauwallner A
        • Langerholc T
        • et al.
        Efficacy of using probiotics with antagonistic activity against pathogens of wound infections: an integrative review of literature.
        Biomed Res Int. 2019; 20197585486
        • Koren L
        • Gurfinkel R
        • Glezinger R
        • et al.
        The effect of Lactobacillus bacteria supplement on sepsis and its complications in patients with acute burns.
        Burns. 2007; 33: 594-598
        • Peral MC
        • Martinez MA
        • Valdez JC.
        Bacteriotherapy with Lactobacillus plantarum in burns.
        Int Wound J. 2009; 6: 73-81
        • Peral MC
        • Rachid MM
        • Gobbato NM
        • et al.
        Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with Lactobacillus plantarum.
        Clin Microbiol Infect. 2010; 16: 281-286
        • Lee ES
        • Song EJ
        • Nam YD
        • et al.
        Probiotics in human health and disease: from nutribiotics to pharmabiotics.
        J Microbiol. 2018; 56: 773-782
        • Baquerizo Nole KL
        • Yim E
        • Keri JE.
        Probiotics and prebiotics in dermatology.
        J Am Acad Dermatol. 2014; 71: 814-821
        • El-Ghazely MH
        • Mahmoud WH
        • Atia MA
        • et al.
        Effect of probiotic administration in the therapy of pediatric thermal burn.
        Ann Burns Fire Disasters. 2016; 29: 268-272
        • Fölster-Holst R
        • Müller F
        • Schnopp N
        • et al.
        Prospective, randomized controlled trial on Lactobacillus rhamnosus in infants with moderate to severe atopic dermatitis.
        Br J Dermatol. 2006; 155: 1256-1261
        • Rayes N
        • Hansen S
        • Seehofer D
        • et al.
        Early enteral supply of fiber and Lactobacilli versus conventional nutrition: a controlled trial in patients with major abdominal surgery.
        Nutrition. 2002; 18: 609-615
        • Rayes N
        • Seehofer D
        • Theruvath T
        • et al.
        Effect of enteral nutrition and synbiotics on bacterial infection rates after pylorus-preserving pancreatoduodenectomy: a randomized, double-blind trial.
        Ann Surg. 2007; 246: 36-41
        • Rayes N
        • Seehofer D
        • Theruvath T
        • et al.
        Supply of pre- and probiotics reduces bacterial infection rates after liver transplantation–a randomized, double-blind trial.
        Am J Transplant. 2005; 5: 125-130
        • Zhang Y
        • Chen J
        • Wu J
        • et al.
        Probiotic use in preventing postoperative infection in liver transplant patients.
        Hepatobiliary Surg Nutr. 2013; 2: 142-147
        • Ziegler E
        • Vanderhoof JA
        • Petschow B
        • et al.
        Term infants fed formula supplemented with selected blends of prebiotics grow normally and have soft stools similar to those reported for breast-fed infants.
        J Pediatr Gastroenterol Nutr. 2007; 44: 359-364
        • Aguirre E.
        An international model for antibiotics regulation.
        Food Drug Law J. 2017; 72: 295-313
        • Pradhan S
        • Madke B
        • Kabra P
        • et al.
        Anti-inflammatory and immunomodulatory effects of antibiotics and their use in dermatology.
        Indian J Dermatol. 2016; 61: 469-481
        • Kim JE
        • Kim HS.
        Microbiome of the skin and gut in atopic dermatitis (ad): understanding the pathophysiology and finding novel management strategies.
        J Clin Med. 2019; 8: 444
        • Paller AS
        • Kong HH
        • Seed P
        • et al.
        The microbiome in patients with atopic dermatitis.
        J Allergy Clin Immunol. 2019; 143: 26-35
        • Ismail IH
        • Oppedisano F
        • Joseph SJ
        • et al.
        Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants.
        Pediatr Allergy Immunol. 2012; 23: 674-681
        • Abrahamsson TR
        • Jakobsson HE
        • Andersson AF
        • et al.
        Low diversity of the gut microbiota in infants with atopic eczema.
        J Allergy Clin Immunol. 2012; 129 (440.e431-432): 434-440
        • Watanabe S
        • Narisawa Y
        • Arase S
        • et al.
        Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects.
        J Allergy Clin Immunol. 2003; 111: 587-591
        • Reddel S
        • Del Chierico F
        • Quagliariello A
        • et al.
        Gut microbiota profile in children affected by atopic dermatitis and evaluation of intestinal persistence of a probiotic mixture.
        Sci Rep. 2019; 9: 4996
        • Nagpal R
        • Wang S
        • Ahmadi S
        • et al.
        Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome.
        Sci Rep. 2018; 8: 12649
        • Kalliomäki M
        • Salminen S
        • Poussa T
        • et al.
        Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial.
        Lancet. 2003; 361: 1869-1871
        • Zeichner J
        • Seite S.
        From probiotic to prebiotic using thermal spring water.
        J Drugs Dermatol. 2018; 17: 657-662
        • Gao Z
        • Tseng CH
        • Strober BE
        • et al.
        Substantial alterations of the cutaneous bacterial biota in psoriatic lesions.
        PLoS One. 2008; 3: e2719
        • Shapiro J
        • Cohen NA
        • Shalev V
        • et al.
        Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls.
        J Dermatol. 2019; 46: 595-603
        • Tan L
        • Zhao S
        • Zhu W
        • et al.
        The Akkermansia muciniphila is a gut microbiota signature in psoriasis.
        Exp Dermatol. 2018; 27: 144-149
        • Eppinga H
        • Sperna Weiland CJ
        • Thio HB
        • et al.
        Similar depletion of protective faecalibacterium prausnitzii in psoriasis and inflammatory bowel disease, but not in hidradenitis suppurativa.
        J Crohns Colitis. 2016; 10: 1067-1075
        • Yan HM
        • Zhao HJ
        • Guo DY
        • et al.
        Gut microbiota alterations in moderate to severe acne vulgaris patients.
        J Dermatol. 2018; 45: 1166-1171
        • Chen YH
        • Wu CS
        • Chao YH
        • et al.
        Lactobacillus pentosus GMNL-77 inhibits skin lesions in imiquimod-induced psoriasis-like mice.
        J Food Drug Anal. 2017; 25: 559-566
        • Egeberg A
        • Weinstock LB
        • Thyssen EP
        • et al.
        Rosacea and gastrointestinal disorders: a population-based cohort study.
        Br J Dermatol. 2017; 176: 100-106
        • Weiss E
        • Katta R.
        Diet and rosacea: the role of dietary change in the management of rosacea.
        Dermatol Pract Concept. 2017; 7: 31-37
        • Utaş S
        • Ozbakir O
        • Turasan A
        • et al.
        Helicobacter pylori eradication treatment reduces the severity of rosacea.
        J Am Acad Dermatol. 1999; 40: 433-435
        • Woo YR
        • Lee SH
        • Cho SH
        • Lee JD
        • Kim HS.
        Characterization and analysis of the skin microbiota in rosacea: impact of systemic antibiotics.
        J Clin Med. 2020; 9: 185
        • Deng Y
        • Wang H
        • Zhou J
        • et al.
        Patients with acne vulgaris have a distinct gut microbiota in comparison with healthy controls.
        Acta Derm Venereol. 2018; 98: 783-790
        • Deplewski D
        • Rosenfield RL.
        Role of hormones in pilosebaceous unit development.
        Endocr Rev. 2000; 21: 363-392
        • Sivamani R.
        The gut-skin axis and mechanisms for communication.
        Nat Med J. 2018; 10: 22-26
        • Adalsteinsson JA
        • Kaushik S
        • Muzumdar S
        • et al.
        An update on the microbiology, immunology and genetics of seborrheic dermatitis.
        Exp Dermatol. 2020; 29: 481-489
        • Maarouf M
        • Platto JF
        • Shi VY.
        The role of nutrition in inflammatory pilosebaceous disorders: implication of the skin-gut axis.
        Australas J Dermatol. 2019; 60: e90-e98
        • Sanders MGH
        • Pardo LM
        • Uitterlinden AG
        • et al.
        The genetics of seborrheic dermatitis: a candidate gene approach and pilot genome-wide association study.
        J Invest Dermatol. 2018; 138: 991-993
        • Opländer C
        • Suschek CV.
        The role of photolabile dermal nitric oxide derivates in ultraviolet radiation (UVR)-induced cell death.
        Int J Mol Sci. 2012; 14: 191-204
        • Guéniche A
        • Philippe D
        • Bastien P
        • et al.
        Probiotics for photoprotection.
        Dermatoendocrinol. 2009; 1: 275-279
        • Satoh T
        • Murata M
        • Iwabuchi N
        • et al.
        Effect of Bifidobacterium breve B-3 on skin photoaging induced by chronic UV irradiation in mice.
        Benef Microbes. 2015; 6: 497-504