281
Views
1
CrossRef citations to date
0
Altmetric
Review

Symbiotic microorganisms: prospects for treating atopic dermatitis

, , , , & ORCID Icon
Pages 911-927 | Received 23 Sep 2021, Accepted 10 Jun 2022, Published online: 19 Jun 2022

References

  • Yamada T, Saito H, Fujieda S. Present state of Japanese cedar pollinosis: the national affliction. J Allergy Clin Immunol. 2014 Mar;133(3):632–9.e5.
  • Liu P, Zhao Y, Mu Z, et al. Clinical features of adult/adolescent atopic dermatitis and Chinese criteria for atopic dermatitis. Chin Med J. 2016;129(7):757–762.
  • Weidinger S, Beck LA, Bieber T, et al. Atopic dermatitis. Nat Rev Dis Primers. 2018 Jun 21;4(1):1.
  • Ho V, Ma E, Liew H, et al. Comparing the potential for irritation of a ceramide-based moisturizer with a urea-based moisturizer for pediatric atopic dermatitis. Dermatol Ther. 2020;10(4):807–813.
  • Draelos Z, Feldman S, Berman B, et al. Tolerability of topical treatments for atopic dermatitis. Dermatol Ther. 2019;9(1):71–102.
  • Andrea MT, Mar LV, Alejandra PP, et al. Biological treatments in atopic dermatitis. J Clin Med. 2015;4(4):593–613.
  • Bonamonte D, Filoni A, Vestita M, et al. The role of the environmental risk factors in the pathogenesis and clinical outcome of atopic dermatitis. Biomed Res Int. 2019;2019:2450605.
  • Tokunaga T, Ninomiya T, Osawa Y, et al. Factors associated with the development and remission of allergic diseases in an epidemiological survey of high school students in Japan. Am J Rhinol Allergy. 2015 Mar-Apr;29(2):94–99.
  • Hassoun Y, James C, Bernstein DI. The effects of air pollution on the development of atopic disease. Clin Rev Allergy Immunol. 2019 Dec;57(3):403–414.
  • Park YM, Lee SY, Kang MJ, et al. Imbalance of gut streptococcus, clostridium, and akkermansia determines the natural course of atopic dermatitis in infant. Allergy Asthma Immunol Res. 2020 Mar;12(2):322–337.
  • Kobayashi T, Nagao K. Host-microbial dialogues in atopic dermatitis. Int Immunol. 2019;31(7):449–456.
  • 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 Apr 2;8(4):444.
  • Climent E, Martinez-Blanch JF, Llobregat L, et al. Changes in gut microbiota correlates with response to treatment with probiotics in patients with atopic dermatitis. a post hoc analysis of a clinical trial. Microorganisms. 2021 Apr 15 9(4):854.
  • Wohl DL, Curry WJ, Mauger D, et al. Intrapartum antibiotics and childhood atopic dermatitis. J Am Board Fam Med. 2015 Jan-Feb;28(1):82–89.
  • Grice EA, Segre JA. The human microbiome: our second genome. Annu Rev Genomics Hum Genet. 2012;13:151–170.
  • Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016 Aug;14(8):e1002533.
  • Quinn RA, Melnik AV, Vrbanac A, et al. Global chemical effects of the microbiome include new bile-acid conjugations. Nature. 2020 Mar;579(7797):123–129.
  • Pleguezuelos-Manzano C, Puschhof J, Rosendahl Huber A, et al. Mutational signature in colorectal cancer caused by genotoxic pks(+) E. coli. Nature. 2020 Apr;580(7802):269–273.
  • Oliphant K, Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome. 2019 Jun 13; 7(1):91.
  • Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11971–11975.
  • Szántó M, Dózsa A, Antal D, et al. Targeting the gut-skin axis-Probiotics as new tools for skin disorder management? Exp Dermatol. 2019 Nov;28(11):1210–1218.
  • Salminen S, Gibson GR, McCartney AL, et al. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut. 2004 Sep;53(9):1388–1389.
  • Savilahti EM, Kukkonen AK, Haahtela T, et al. Intestinal defensin secretion in infancy is associated with the emergence of sensitization and atopic dermatitis. Clin Exp Allergy. 2012 Mar;42(3):405–411.
  • Kero J, Gissler M, Grönlund MM, et al. Mode of delivery and asthma – is there a connection? Pediatr Res. 2002 Jul;52(1):6–11.
  • Xu B, Pekkanen J, Hartikainen AL, et al. Caesarean section and risk of asthma and allergy in adulthood. J Allergy Clin Immunol. 2001 Apr;107(4):732–733.
  • Nafstad P, Magnus P, Jaakkola JJ. Risk of childhood asthma and allergic rhinitis in relation to pregnancy complications. J Allergy Clin Immunol. 2000 Nov;106(5):867–873.
  • McLoughlin K, Schluter J, Rakoff-Nahoum S, et al. Host selection of microbiota via differential adhesion. Cell Host Microbe. 2016 Apr 13 19(4):550–559.
  • Li H, Limenitakis JP, Fuhrer T, et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nat Commun. 2015 Sep 22;6:8292.
  • Mark Welch JL, Hasegawa Y, McNulty NP, et al. Spatial organization of a model 15-member human gut microbiota established in gnotobiotic mice. Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):E9105–e9114.
  • Andersson A, Lindberg M, Jakobsson H, et al. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PloS one. 2008;3(7):e2836.
  • Stearns JC, Lynch MD, Senadheera DB, et al. Bacterial biogeography of the human digestive tract. Sci Rep. 2011;1(1):170.
  • Clements SJ, RC S. Diet, the intestinal microbiota, and immune health in aging. Crit Rev Food Sci Nutr. 2018 Mar 4;58(4):651–661.
  • Wegh CAM, Geerlings SY, Knol J, et al. Postbiotics and their potential applications in early life nutrition and beyond. Int J Mol Sci. 2019 Sep 20 20(19):4673.
  • Grice EA, Kong HH, Renaud G, et al. A diversity profile of the human skin microbiota. Genome Res. 2008 Jul;18(7):1043–1050.
  • Gallo RL. Human skin is the largest epithelial surface for interaction with microbes. J Invest Dermatol. 2017 Jun;137(6):1213–1214.
  • Christensen GJ, Brüggemann H. Bacterial skin commensals and their role as host guardians. Benef Microbes. 2014 Jun 1; 5(2):201–215.
  • Dreno B, Martin R, Moyal D, et al. Skin microbiome and acne vulgaris: staphylococcus, a new actor in acne. Exp Dermatol. 2017 Sep;26(9):798–803.
  • Belkaid Y, Segre JA. Dialogue between skin microbiota and immunity. Science (New York, NY). 2014 Nov 21; 346(6212):954–959.
  • Forno E, Onderdonk AB, McCracken J, et al. Diversity of the gut microbiota and eczema in early life. Clinical and molecular allergy: CMA. 2008 Sep 22;6:11.
  • Abrahamsson TR, Jakobsson HE, Andersson AF, et al. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2012 Feb;129(2):434–40, 440.e1–2.
  • Wang M, Karlsson C, Olsson C, et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol. 2008 Jan;121(1):129–134.
  • Yu L, Deng YH, Huang YH, et al. Comparison of gut microbiota between infants with atopic dermatitis and healthy controls in Guangzhou, China. J Asthma Allergy. 2021;14:493–500.
  • Kim IS, Lee SH, Kwon YM, et al. Oral administration of β-Glucan and lactobacillus plantarum alleviates atopic dermatitis-like symptoms. J Microbiol Biotechnol. 2019 Nov 28 29(11):1693–1706.
  • Kalliomäki M, Kirjavainen P, Eerola E, et al. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001 Jan;107(1):129–134.
  • Linehan JL, Harrison OJ, Han SJ, et al. Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell. 2018 Feb 8 172(4):784–796.e18.
  • Li S, Villarreal M, Stewart S, et al. Altered composition of epidermal lipids correlates with Staphylococcus aureus colonization status in atopic dermatitis. Br J Dermatol. 2017 Oct;177(4):e125–e127.
  • Fieten KB, Totté JEE, Levin E, et al. Fecal microbiome and food allergy in pediatric atopic dermatitis: a cross-sectional pilot study. Int Arch Allergy Immunol. 2018;175(1–2):77–84.
  • Song H, Yoo Y, Hwang J, et al. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J Allergy Clin Immunol. 2016 Mar;137(3):852–860.
  • Koga Y, Tokunaga S, Nagano J, et al. Age-associated effect of kestose on faecalibacterium prausnitzii and symptoms in the atopic dermatitis infants. Pediatr Res. 2016 Dec;80(6):844–851.
  • Moore-Connors JM, Dunn KA, Bielawski JP, et al. Novel strategies for applied metagenomics. Inflamm Bowel Dis. 2016 Mar;22(3):709–718.
  • Lee YB, Byun EJ, Kim HS. Potential role of the microbiome in acne: A comprehensive review. J Clin Med. 2019 Jul 7;8(7):987.
  • Hong PY, Lee BW, Aw M, et al. Comparative analysis of fecal microbiota in infants with and without eczema. PloS one. 2010 Apr 1 5(4):e9964.
  • Ismail IH, Boyle RJ, Licciardi PV, et al. Early gut colonization by Bifidobacterium breve and B. catenulatum differentially modulates eczema risk in children at high risk of developing allergic disease. Pediatr Allergy Immunol. 2016 Dec;27(8):838–846.
  • Mah KW, Björkstén B, Lee BW, et al. Distinct pattern of commensal gut microbiota in toddlers with eczema. Int Arch Allergy Immunol. 2006;140(2):157–163.
  • Singh RK, Chang HW, Yan D, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med. 2017 Apr 8 15(1):73.
  • Tanaka A, Jung K, Benyacoub J, et al. Oral supplementation with lactobacillus rhamnosus CGMCC 1.3724 prevents development of atopic dermatitis in NC/NgaTnd mice possibly by modulating local production of IFN-gamma. Exp Dermatol. 2009 Dec;18(12):1022–1027.
  • Won TJ, Kim B, Lim YT, et al. Oral administration of lactobacillus strains from kimchi inhibits atopic dermatitis in NC / Nga mice. J Appl Microbiol. 2011 May;110(5):1195–1202.
  • Grönthal T, Eklund M, Thomson K, et al. UK Standards for Microbiology Investigations. Acta Vet Scand. 2015;57(1): 37.
  • Diallo M, Kengen SWM, López-Contreras AM. Sporulation in solventogenic and acetogenic clostridia. Applied microbiology and biotechnology. Appl Microbiol Biotechnol. 2021 May;105(9):3533–3557.
  • Penders J, Thijs C, van den Brandt PA, et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA birth cohort study. Gut. 2007 May;56(5):661–667.
  • 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 May;22(5):850–859.
  • Salava A, Lauerma A. Role of the skin microbiome in atopic dermatitis. Clin Transl Allergy. 2014;4(1):33.
  • Byrd AL, Deming C, Cassidy SKB, et al. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci Transl Med. 2017 Jul 5;9(397). 10.1126/scitranslmed.aal4651.
  • Williams MR, Gallo RL. The role of the skin microbiome in atopic dermatitis. Curr Allergy Asthma Rep. 2015 Nov;15(11):65.
  • Kobayashi T, Glatz M, Horiuchi K, et al. Dysbiosis and staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity. 2015 Apr 21 42(4):756–766.
  • Zhang E, Tanaka T, Tajima M, et al. Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol. 2011 Sep;55(9):625–632.
  • Sun Z, Huang S, Zhu P, et al. A microbiome-based index for assessing skin health and treatment effects for atopic dermatitis in children. mSystems. 2019 Aug 20;4(4). .
  • Reiger M, Schwierzeck V, Traidl-Hoffmann C. Atopic eczema and microbiome. Der Hautarzt; Zeitschrift fur Dermatologie, Venerologie, und verwandte Gebiete. 2019 Jun;70(6):407–415.
  • Bradley CW, Morris DO, Rankin SC, et al. Longitudinal evaluation of the skin microbiome and association with microenvironment and treatment in canine atopic dermatitis. J Invest Dermatol. 2016 Jun;136(6):1182–1190.
  • Kim K, Hong S, Han D, et al. Dietary antigens limit mucosal immunity by inducing regulatory T cells in the small intestine. Science. 2016;351(6275):858–863.
  • Suez J, Elinav E. The path towards microbiome-based metabolite treatment. Nat Microbiol. 2017;2(6):17075.
  • Atarashi K, Tanoue T, Oshima K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013 Aug 8 500(7461):232–236.
  • Malin M, Verronen P, Korhonen H, et al. Dietary therapy with lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: evaluation of effect on gut defence mechanisms. Inflammopharmacology. 1997;5(3):219–236.
  • Pessi T, Isolauri E, Sütas Y, et al. Suppression of T-cell activation by lactobacillus rhamnosus GG-degraded bovine casein. Int Immunopharmacol. 2001 Feb;1(2):211–218.
  • Kaila M, Isolauri E, Soppi E, et al. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human lactobacillus strain. Pediatr Res. 1992 Aug;32(2):141–144.
  • Pessi T, Sütas Y, Hurme M, et al. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy. 2000 Dec;30(12):1804–1808.
  • Poutahidis T, Kleinewietfeld M, Smillie C, et al. Microbial reprogramming inhibits Western diet-associated obesity. PloS one. 2013;8(7):e68596.
  • Torii A, Torii S, Fujiwara S, et al. Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol Int. 2007 Sep;56(3):293–301.
  • Feleszko W, Jaworska J, Rha RD, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy. 2007 Apr;37(4):498–505.
  • Marschan E, Kuitunen M, Kukkonen K, et al. Probiotics in infancy induce protective immune profiles that are characteristic for chronic low-grade inflammation. Clin Exp Allergy. 2008 Apr;38(4):611–618.
  • Derrien M, Veiga P. Rethinking Diet to Aid Human-Microbe Symbiosis. Trends Microbiol. 2017 Feb;25(2):100–112.
  • Maslowski K, Vieira A, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 461(7268): 1282–1286. 2009.
  • Schwarz A, Bruhs A, Schwarz T. The Short-Chain Fatty Acid Sodium Butyrate Functions as a Regulator of the Skin Immune System. J Invest Dermatol. 2017 Apr;137(4):855–864.
  • Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017 Jan;19(1):29–41.
  • 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.
  • Mu Q, Kirby J, Reilly CM, et al. Leaky gut as a danger signal for autoimmune diseases. Front Immunol. 2017;8:598.
  • Maguire M, Maguire G. The role of microbiota, and probiotics and prebiotics in skin health. Arch Dermatol Res. 2017 Aug;309(6):411–421.
  • Majamaa H, Isolauri E. Evaluation of the gut mucosal barrier: evidence for increased antigen transfer in children with atopic eczema. Allergy Clinimmunol. 1996;97(4):985–990
  • Racine PJ, Janvier X, Clabaut M, et al. Dialog between skin and its microbiota: emergence of “cutaneous bacterial endocrinology.” Exp Dermatol. 2020 Sep;29(9):790–800.
  • Dou J, Zeng J, Wu K, et al. Microbiosis in pathogenesis and intervention of atopic dermatitis. Int Immunopharmacol. 2019 Apr;69:263–269.
  • Schlievert PM, Strandberg KL, Lin YC, et al. Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol. 2010 Jan;125(1):39–49.
  • Palm NW, de Zoete Mr, Flavell RA, et al. Immune-microbiota interactions in health and disease. Clin Immunol. 2015 Aug;159(2):122–127.
  • Naik S, Bouladoux N, Wilhelm C, et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012 Aug 31 337(6098):1115–1119.
  • Marchini G, Nelson A, Edner J, et al. Erythema toxicum neonatorum is an innate immune response to commensal microbes penetrated into the skin of the newborn infant. Pediatr Res. 2005 Sep;58(3):613–616.
  • Capone KA, Dowd SE, Stamatas GN, et al. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011 Oct;131(10):2026–2032.
  • Baldwin HE, Bhatia ND, Friedman A, et al. The role of cutaneous microbiota harmony in maintaining a functional skin barrier. J Drugs Dermatol. [2017 Jan 1];16(1):12–18.
  • Cogen AL, Yamasaki K, Sanchez KM, et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol. 2010 Jan;130(1):192–200.
  • Wanke I, Steffen H, Christ C, et al. Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J Invest Dermatol. 2011 Feb;131(2):382–390.
  • Lai Y, Cogen AL, Radek KA, et al. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol. 2010 Sep;130(9):2211–2221.
  • Grice EA, Segre JA. The skin microbiome. Nature Rev Microbiol. 2011 Apr;9(4):244–253.
  • Cau L, Williams MR, Butcher AM, et al. Staphylococcus epidermidis protease EcpA can be a deleterious component of the skin microbiome in atopic dermatitis. J Allergy Clin Immunol. 2021 Mar;147(3):955–966.e16.
  • Meylan P, Lang C, Mermoud S, et al. Skin Colonization by Staphylococcus aureus Precedes the Clinical Diagnosis of Atopic Dermatitis in Infancy. J Invest Dermatol. 2017 Dec;137(12):2497–2504.
  • Di Domenico EG, Cavallo I, Capitanio B, et al. Staphylococcus aureus and the cutaneous microbiota biofilms in the pathogenesis of atopic dermatitis. Microorganisms. 2019 Aug 29 7(9):301.
  • Arad G, Levy R, Nasie I, et al. Binding of superantigen toxins into the CD28 homodimer interface is essential for induction of cytokine genes that mediate lethal shock. PLoS Biol. 2011 Sep;9(9):e1001149.
  • Nakatsuji T, Chen TH, Two AM, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol. 2016 Nov;136(11):2192–2200.
  • Walev I, Martin E, Jonas D, et al. Staphylococcal alpha-toxin kills human keratinocytes by permeabilizing the plasma membrane for monovalent ions. Infect Immun. 1993 Dec;61(12):4972–4979.
  • Williams MR, Nakatsuji T, Gallo RL. Staphylococcus aureus: master manipulator of the skin. Cell Host Microbe. 2017 Nov 8; 22(5):579–581.
  • Abrahamsson TR, Jakobsson T, Böttcher MF, et al. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol. 2007 May;119(5):1174–1180.
  • Soh SE, Aw M, Gerez I, et al. Probiotic supplementation in the first 6 months of life in at risk Asian infants–effects on eczema and atopic sensitization at the age of 1 year. Clin Exp Allergy. 2009 Apr;39(4):571–578.
  • Kopp MV, Hennemuth I, Heinzmann A, et al. Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of lactobacillus GG supplementation. Pediatrics. 2008 Apr;121(4):e850–6.
  • Weston S, Halbert A, Richmond P, et al. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child. 2005 Sep;90(9):892–897.
  • Sistek D, Kelly R, Wickens K, et al. Is the effect of probiotics on atopic dermatitis confined to food sensitized children? Clin Exp Allergy. 2006 May;36(5):629–633.
  • 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 Dec;155(6):1256–1261.
  • Nakatsuji T, Yun T, Butcher A, et al. 426 clinical improvement in atopic dermatitis following autologous application of microbiome therapy targeting staphylococcus aureus. J Invest Dermatol. 2018 [2018 May 01];138(5, Supplement):S72.
  • Nakatsuji T, Hata TR, Tong Y, et al. Development of a human skin commensal microbe for bacteriotherapy of atopic dermatitis and use in a phase 1 randomized clinical trial. Nat Med. 2021;27(4):700–709.
  • Myles I, Earland N, Anderson E, et al. First-in-human topical microbiome transplantation with roseomonas mucosa for atopic dermatitis. JCI Insight. 2018;3(9):e120608.
  • Myles IA, Castillo CR, Barbian KD, et al. Therapeutic responses to roseomonas mucosa in atopic dermatitis may involve lipid-mediated TNF-related epithelial repair. Sci Transl Med. 2020;12(560):eaaz8631eaaz8631.
  • Ohshima-Terada Y, Higuchi Y, Kumagai T, et al. Complementary effect of oral administration of Lactobacillus paracasei K71 on canine atopic dermatitis. Vet Dermatol. 2015 Oct;26(5):350–3, e74–5.
  • Osumi T, Shimada T, Sakaguchi M, et al. A double-blind, placebo-controlled evaluation of orally administered heat-killed Enterococcus faecalis FK-23 preparation in atopic dogs. Vet Dermatol. 2019 Apr;30(2):127–e36.
  • Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017 Mar 25 389(10075):1218–1228.
  • Aroniadis OC, Brandt LJ. Intestinal microbiota and the efficacy of fecal microbiota transplantation in gastrointestinal disease. Gastroenterol Hepatol. 2014 Apr;10(4):230–237.
  • Kim J-H, Kim K, Kim W. Gut microbiota restoration through fecal microbiota transplantation: a new atopic dermatitis therapy. Exp Mol Med. 2021 May 20; 53(5):907–916.
  • Yeom M, Sur BJ, Park J, et al. Oral administration of lactobacillus casei variety rhamnosus partially alleviates TMA-induced atopic dermatitis in mice through improving intestinal microbiota. J Appl Microbiol. 2015 Aug;119(2):560–570.
  • Kalliomäki M, Salminen S, Arvilommi H, et al. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 2001 ;357(9262):1076–1079.
  • Wickens K, Black PN, Stanley TV, et al. A differential effect of 2 probiotics in the prevention of eczema and atopy: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol. 2008 Oct;122(4):788–794.
  • Viljanen M, Savilahti E, Haahtela T, et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy. 2005;60(4):494–500.
  • Cukrowska B, Ceregra A, Maciorkowska E, et al. The effectiveness of probiotic lactobacillus rhamnosus and lactobacillus casei strains in children with atopic dermatitis and cow’s milk protein allergy: a multicenter, randomized, double blind, placebo controlled study. Nutrients. 2021 Apr 1;13(4):1169.
  • Hwang JS, Im CR, Im SH. Immune disorders and its correlation with gut microbiome. Immune Netw. 2012 Aug;12(4):129–138.
  • 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.
  • Drago L, De Vecchi E, Toscano M, et al. Treatment of atopic dermatitis eczema with a high concentration of Lactobacillus salivarius LS01 associated with an innovative gelling complex: a pilot study on adults. J Clin Gastroenterol. 2014 Nov-Dec;48(1):S47–51.
  • Bowe W, Patel NB, Logan AC. Acne vulgaris, probiotics and the gut-brain-skin axis: from anecdote to translational medicine. Benef Microbes. 2014 Jun 1; 5(2):185–199.
  • Myers B, Brownstone N, Reddy V, et al. The gut microbiome in psoriasis and psoriatic arthritis. Best Pract Res Clin Rheumatol. 2019 Dec;33(6):101494.
  • David L, Maurice C, Carmody R, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563.
  • Morales P, Fujio S, Navarrete P, et al. Impact of dietary lipids on colonic function and microbiota: an experimental approach involving orlistat-induced fat malabsorption in human volunteers. Clin Transl Gastroenterol. 2016 Apr 7 7(4):e161.
  • Knox NC, Forbes JD, Peterson CL, et al. The gut microbiome in inflammatory bowel disease: lessons learned from other immune-mediated inflammatory diseases. Am J Gastroenterol. 2019 Jul;114(7):1051–1070.
  • Myles IA, Castillo CR, Barbian KD, et al. Therapeutic responses to roseomonas mucosa in atopic dermatitis may involve lipid-mediated TNF-related epithelial repair. Sci Transl Med. 2020 Sep 9;12:(560):eaaz8631.
  • Myles IA, Earland NJ, Anderson ED, et al. First-in-human topical microbiome transplantation with Roseomonas mucosa for atopic dermatitis. JCI Insight. 2018 May 3;3:(9):e120608.
  • Francis NA, Ridd MJ, Thomas-Jones E, et al. Oral and topical antibiotics for clinically infected eczema in children: a pragmatic randomized controlled trial in ambulatory care. Ann Fam Med. 2017 Mar;15(2):124–130.
  • 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 Nov;13(11):1365–1372.
  • Maarouf M, Shi VY. Bleach for atopic dermatitis: beyond antimicrobials. Dermatitis. 2018;29(3):1.
  • Yu Y, Dunaway S, Champer J, et al. Changing our microbiome: probiotics in dermatology. Br J Dermatol. 2020 Jan;182(1):39–46.
  • Peroni DG, Nuzzi G, Trambusti I, et al. Microbiome composition and its impact on the development of allergic diseases. Front Immunol. 2020;11:700.
  • Paharik AE, Parlet CP, Chung N, et al. Coagulase-negative staphylococcal strain prevents staphylococcus aureus colonization and skin infection by blocking quorum sensing. Cell Host Microbe. 2017 Dec 13 22(6):746–756.e5.
  • Paetzold B, Willis J, Pereira de lima J, et al. Skin microbiome modulation induced by probiotic solutions. Microbiome. 2019;7(1):95.
  • Myles IA, Williams KW, Reckhow JD, et al. Transplantation of human skin microbiota in models of atopic dermatitis. JCI Insight. 2016 Jul 7;1(10):e86955.
  • Nakatsuji T, Hata TR, Tong Y, et al. Development of a human skin commensal microbe for bacteriotherapy of atopic dermatitis and use in a phase 1 randomized clinical trial. Nat Med. 2021 Apr;27(4):700–709.
  • Ito Y, Sasaki T, Li Y, et al. Staphylococcus cohnii is a potentially biotherapeutic skin commensal alleviating skin inflammation. Cell Rep. 2021 Apr 27 35(4):109052.
  • Zeng J, Lu J. Mechanisms of action involved in ozone-therapy in skin diseases. Int Immunopharmacol. 2018 Mar;56:235–241.
  • Zeng J, Dou J, Gao L, et al. Topical ozone therapy restores microbiome diversity in atopic dermatitis. Int Immunopharmacol. 2020 Mar;80:106191.
  • Lu J, Chen M, Gao L, et al. A preliminary study on topical ozonated oil in the therapeutic management of atopic dermatitis in murine. J Dermatolog Treat. 2018 Nov;29(7):676–681.
  • Lu J, Li M, Huang J, et al. Effect of ozone on staphylococcus aureus colonization in patients with atopic dermatitis. J Cent South Univ Med sci. 2018 Feb 28;43(2):157–162.
  • Guttman-Yassky E, Gallo RL, Pavel AB, et al. A nitric oxide-releasing topical medication as a potential treatment option for atopic dermatitis through antimicrobial and anti-inflammatory activity. J Invest Dermatol. 2020 Dec;140(12):2531–2535.e2.
  • Lossius AH, Sundnes O, Ingham AC, et al. Shifts in the skin microbiota after UVB treatment in adult atopic dermatitis. Dermatology. 2021;238(1) :1–12.
  • Kim HI, Hong SH, Lee SY, et al. gardenia jasminoides ameliorates antibiotic-associated aggravation of dncb-induced atopic dermatitis by restoring the intestinal microbiome profile. Nutrients. 2021Apr 18;13(4):1349.
  • van Eck Nj, Waltman L, van Eck NJ. Software survey: vOSviewer, a computer program for bibliometric mapping. Scientometrics. 2010 Aug;84(2):523–538.
  • van Eck Nj, Waltman L, van Eck NJ. Citation-based clustering of publications using CitNetExplorer and VOSviewer. Scientometrics. 2017;111(2):1053–1070.
  • Muszer M, Noszczyńska M, Kasperkiewicz K, et al. Human microbiome: when a friend becomes an enemy. Arch Immunol Ther Exp (Warsz). 2015 Aug;63(4):287–298.
  • Flohr C, Pascoe D, Williams HC. Atopic dermatitis and the ‘hygiene hypothesis’: too clean to be true? Br J Dermatol. 2005 Feb;152(2):202–216.
  • Torres T, Ferreira E, Gonçalo M, et al. Update on atopic dermatitis. Acta medica portuguesa. 2019;32(9):606–613.
  • Kwon HK, Lee CG, So JS, et al. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A. 2010Feb 2;107(5):2159–2164.
  • Sawada J, Morita H, Tanaka A, et al. Ingestion of heat-treated lactobacillus rhamnosus GG prevents development of atopic dermatitis in NC/Nga mice. Clin Exp Allergy. 2007 Feb;37(2):296–303.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.