The emerging role of skin microbiome in atopic dermatitis and its clinical implication

References

• Boguniewicz M, Leung DY. Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol Rev. 2011;242:233–246.
   PubMed Web of Science ®Google Scholar
• Wollenberg A, Oranje A, Deleuran M, et al. ETFAD/EADV eczema task force 2015 position paper on diagnosis and treatment of atopic dermatitis in adult and paediatric patients. J Eur Acad Dermatol Venereol. 2016;30:729–747.
   PubMed Web of Science ®Google Scholar
• Ricci G, Bellini F, Dondi A, et al. Atopic dermatitis in adolescence. Dermatol Reports. 2012;4:e1.
   PubMedGoogle Scholar
• Margolis JS, Abuabara K, Bilker W, et al. Persistence of mild to moderate atopic dermatitis. JAMA Dermatol. 2014;150:593–600.
   PubMed Web of Science ®Google Scholar
• Drucker AM, Wang AR, Li WQ, et al. The burden of atopic dermatitis: summary of a report for the National Eczema Association. J Invest Dermatol. 2017;137:26–30.
   PubMed Web of Science ®Google Scholar
• Elias PM, Steinhoff M. "Outside-to-inside" (and now back to "outside") pathogenic mechanisms in atopic dermatitis. J Invest Dermatol. 2008;128:1067–1070.
   PubMed Web of Science ®Google Scholar
• Baker BS. The role of microorganisms in atopic dermatitis. Clin Exp Immunol. 2006;144:1–9.
   PubMed Web of Science ®Google Scholar
• Leyden JJ, Marples RR, Kligman AM. Staphylococcus aureus in the lesions of atopic dermatitis. Br J Dermatol. 1974;90:525–530.
   PubMed Web of Science ®Google Scholar
• Kong HH. Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med. 2011;17:320–328.
   PubMed Web of Science ®Google Scholar
• Grice EA, Kong HH, Conlan S, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324:1190–1192.
   PubMed Web of Science ®Google Scholar
• Schauber J, Gallo RL. Antimicrobial peptides and the skin immune defense system. J Allergy Clin Immunol. 2008;122:261–266.
   PubMed Web of Science ®Google Scholar
• Agrawal R, Woodfolk JA. Skin barrier defects in atopic dermatitis. Curr Allergy Asthma Rep. 2014;14:433.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Cork MJ, Danby SG, Vasilopoulos Y, et al. Epidermal barrier dysfunction in atopic dermatitis. J Invest Dermatol. 2009;129:1892–1908.
   PubMed Web of Science ®Google Scholar
• Geoghegan JA, Irvine AD, Foster TJ. Staphylococcus aureus and atopic dermatitis: a complex and evolving relationship. Trends Microbiol. 2018;26:484–497.
   PubMed Web of Science ®Google Scholar
• Fleury OM, McAleer MA, Feuillie C, et al. Clumping factor B promotes adherence of Staphylococcus aureus to corneocytes in atopic dermatitis. Infect Immun. 2017;85:e00994–16.
   PubMed Web of Science ®Google Scholar
• Werner Y, Lindberg M. Transepidermal water loss in dry and clinically normal skin in patients with atopic dermatitis. Acta Derm Venereol. 1985;65:102–105.
   PubMed Web of Science ®Google Scholar
• Sandilands A, Sutherland C, Irvine AD, et al. Filaggrin in the frontline: role in skin barrier function and disease. J Cell Sci. 2009;122:1285–1294.
   PubMed Web of Science ®Google Scholar
• Miajlovic H, Fallon PG, Irvine AD, et al. Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol. 2010;126:1184–1190.
   PubMed Web of Science ®Google Scholar
• Zeeuwen P, Ederveen T, van der Krieken D, et al. 107 Filaggrin deficiency impacts cutaneous microbiota. J Invest Dermatol. 2016;136:S179.
   Web of Science ®Google Scholar
• Jinnestal CL, Belfrage E, Back O, et al. Skin barrier impairment correlates with cutaneous Staphylococcus aureus colonization and sensitization to skin-associated microbial antigens in adult patients with atopic dermatitis. Int J Dermatol. 2014;53:27–33.
   PubMed Web of Science ®Google Scholar
• Clausen ML, Agner T, Lilje B, et al. Association of disease severity with skin microbiome and filaggrin gene mutations in adult atopic dermatitis. JAMA Dermatol. 2018;154:293–300.
   PubMed Web of Science ®Google Scholar
• Clausen ML, Edslev SM, Andersen PS, et al. Staphylococcus aureus colonization in atopic eczema and its association with filaggrin gene mutations. Br J Dermatol. 2017;177:1394–1400.
   PubMed Web of Science ®Google Scholar
• Yamasaki K, Gallo RL. Antimicrobial peptides in human skin disease. Eur J Dermatol. 2008;18:11–21.
   PubMed Web of Science ®Google Scholar
• Clausen ML, Slotved HC, Krogfelt KA, et al. Measurements of AMPs in stratum corneum of atopic dermatitis and healthy skin-tape stripping technique. Sci Rep. 2018;8:1666.
   PubMed Web of Science ®Google Scholar
• Clausen ML, Slotved HC, Krogfelt KA, et al. In vivo expression of antimicrobial peptides in atopic dermatitis. Exp Dermatol. 2016;25:3–9.
   PubMed Web of Science ®Google Scholar
• Jensen JM, Ahrens K, Meingassner J, et al. Differential suppression of epidermal antimicrobial protein expression in atopic dermatitis and in EFAD mice by pimecrolimus compared to corticosteroids. Exp Dermatol. 2011;20:783–788.
   PubMed Web of Science ®Google Scholar
• Vavrova K, Henkes D, Struver K, et al. Filaggrin deficiency leads to impaired lipid profile and altered acidification pathways in a 3D skin construct. J Invest Dermatol. 2014;134:746–753.
   PubMed Web of Science ®Google Scholar
• Chan A, Mauro T. Acidification in the epidermis and the role of secretory phospholipases. Dermatoendocrinol. 2011;3:84–90.
   PubMedGoogle Scholar
• Korting HC, Greiner K, Huebner K, et al. Changes in skin pH and resident flora by washing with synthetic detergent preparations at pH 5.5 and 8.5. J Cosmet Sci. 1991;42:147–158.
   Google Scholar
• Schmid-Wendtner MH, Korting HC. The pH of the skin surface and its impact on the barrier function. Skin Pharmacol Physiol. 2006;19:296–302.
   PubMed Web of Science ®Google Scholar
• Gunathilake R, Schurer NY, Shoo BA, et al. pH-regulated mechanisms account for pigment-type differences in epidermal barrier function. J Invest Dermatol. 2009;129:1719–1729.
   PubMed Web of Science ®Google Scholar
• Kleesz P, Darlenski R, Fluhr JW. Full-body skin mapping for six biophysical parameters: baseline values at 16 anatomical sites in 125 human subjects. Skin Pharmacol Physiol. 2012;25:25–33.
   PubMed Web of Science ®Google Scholar
• Hartmann AA. Effect of occlusion on resident flora, skin-moisture and skin-pH. Arch Dermatol Res. 1983;275:251–254.
   PubMed Web of Science ®Google Scholar
• Lambers H, Piessens S, Bloem A, et al. Natural skin surface pH is on average below 5, which is beneficial for its resident flora. Int J Cosmet Sci. 2006;28:359–370.
   PubMedGoogle Scholar
• Selander C, Zargari A, Mollby R, et al. Higher pH level, corresponding to that on the skin of patients with atopic eczema, stimulates the release of Malassezia sympodialis allergens. Allergy. 2006;61:1002–1008.
   PubMed Web of Science ®Google Scholar
• Eichenfield LF, Tom WL, Berger TG, et al. Guidelines of care for the management of atopic dermatitis: section 2. Management and treatment of atopic dermatitis with topical therapies. J Am Acad Dermatol. 2014;71:116–132.
   PubMed Web of Science ®Google Scholar
• Naik S, Bouladoux N, Linehan JL, et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 2015;520:104–108.
   PubMed Web of Science ®Google Scholar
• Park YJ, Lee HK. The role of skin and orogenital microbiota in protective immunity and chronic immune-mediated inflammatory disease. Front Immunol. 2018;8:1955.
   PubMed Web of Science ®Google Scholar
• 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;9:1–11.
   PubMed Web of Science ®Google Scholar
• Bianchi P, Theunis J, Casas C, et al. Effects of a new emollient-based treatment on skin microflora balance and barrier function in children with mild atopic dermatitis. Pediatr Dermatol. 2016;33:165–171.
   PubMed Web of Science ®Google Scholar
• Stettler H, Kurka P, Lunau N, et al. A new topical panthenol-containing emollient: results from two randomized controlled studies assessing its skin moisturization and barrier restoration potential, and the effect on skin microflora. J Dermatolog Treat. 2017;28:173–180.
   PubMed Web of Science ®Google Scholar
• Barnes TM, Greive KA. Use of bleach baths for the treatment of infected atopic eczema. Australas J Dermatol. 2013;54:251–258.
   PubMed Web of Science ®Google Scholar
• Darsow U, Wollenberg A, Simon D, et al. ETFAD/EADV eczema task force 2009 position paper on diagnosis and treatment of atopic dermatitis. J Eur Acad Dermatol Venereol. 2010;24:317–328.
   PubMed Web of Science ®Google Scholar
• Glatz M, Jo J-H, Kennedy EA, et al. Emollient use alters skin barrier and microbes in infants at risk for developing atopic dermatitis. PloS ONE. 2018;13:e0192443.
   PubMed Web of Science ®Google Scholar
• Stalder JF, Fleury M, Sourisse M, et al. Local steroid therapy and bacterial skin flora in atopic dermatitis. Br J Dermatol. 1994;131:536–540.
   PubMed Web of Science ®Google Scholar
• Tang ML, Lahtinen SJ, Boyle RJ. Probiotics and prebiotics: clinical effects in allergic disease. Curr Opin Pediatr. 2010;22:626–634.
   PubMed Web of Science ®Google Scholar
• Di Pierro F, Colombo M, Zanvit A, et al. Use of Streptococcus salivarius K12 in the prevention of streptococcal and viral pharyngotonsillitis in children. Drug Healthc Patient Saf. 2014;6:15–20.
   PubMedGoogle Scholar
• Wu KG, Li TH, Peng HJ. Lactobacillus salivarius plus fructo-oligosaccharide is superior to fructo-oligosaccharide alone for treating children with moderate to severe atopic dermatitis: a double-blind, randomized, clinical trial of efficacy and safety. Br J Dermatol. 2012;166:129–136.
   PubMed Web of Science ®Google Scholar
• Simpson EL, Bieber T, Guttman-Yassky E, et al. Two phase 3 trials of dupilumab versus placebo in atopic dermatitis. N Engl J Med. 2016;375:2335–2348.
   PubMed Web of Science ®Google Scholar
• Engebretsen KA, Johansen JD, Kezic S, et al. The effect of environmental humidity and temperature on skin barrier function and dermatitis. J Eur Acad Dermatol Venereol. 2016;30:223–249.
   PubMed Web of Science ®Google Scholar
• Carroll CL, Balkrishnan R, Feldman SR, et al. The burden of atopic dermatitis: impact on the patient, family, and society. Pediatr Dermatol. 2005;22:192–199.
   PubMed Web of Science ®Google Scholar
• Chisolm SS, Taylor SL, Balkrishnan R, et al. Written action plans: potential for improving outcomes in children with atopic dermatitis. J Am Acad Dermatol. 2008;59:677–683.
   PubMed Web of Science ®Google Scholar
• Patel NU, D'Ambra V, Feldman SR. Increasing adherence with topical agents for atopic dermatitis. Am J Clin Dermatol. 2017;18:323–332.
   PubMed Web of Science ®Google Scholar
• Charman CR, Morris AD, Williams HC. Topical corticosteroid phobia in patients with atopic eczema. Br J Dermatol. 2000;142:931–936.
   PubMed Web of Science ®Google Scholar
• Spielman SC, LeBovidge JS, Timmons KG, et al. A review of multidisciplinary interventions in atopic dermatitis. J Clin Med. 2015;4:1156–1170.
   PubMed Web of Science ®Google Scholar
• Rubel D, Thirumoorthy T, Soebaryo RW, et al. Consensus guidelines for the management of atopic dermatitis: an Asia-Pacific perspective. J Dermatol. 2013;40:160–171.
   PubMed Web of Science ®Google Scholar
• Arkwright PD, Motala C, Subramanian H, et al. Management of difficult-to-treat atopic dermatitis. J Allergy Clin Immunol Pract. 2013;1:142–151.
   PubMed Web of Science ®Google Scholar
• Su JC, Kemp AS, Varigos GA, et al. Atopic eczema: its impact on the family and financial cost. Arch Dis Child. 1997;76:159–162.
   PubMed Web of Science ®Google Scholar