Cutaneous microbiome effects of fluticasone propionate cream and adjunctive bleach baths in childhood atopic dermatitis

Journal of the American Academy of Dermatology

Volumn 75, Issue 3, 2016, Pages 481-493.e8

  Gonzalez, Mercedes E ^a   Schaffer, Julie V ^a   Orlow, Seth J ^a   Gao, Zhan ^b   Li, Huilin ^a   Alekseyenko, Alexander V ^a   Blaser, Martin J ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

16S sequencing; atopic dermatitis; bleach baths; cutaneous microbiome; quantitative polymerase chain reaction; Staphylococcus aureus; topical corticosteroids

Indexed keywords

BACTERIAL DNA; BLEACHING AGENT; FLUTICASONE PROPIONATE; HYPOCHLORITE SODIUM; PLACEBO; RNA 16S; DERMATOLOGICAL AGENT; FLUTICASONE;

ARTICLE; ATOPIC DERMATITIS; CHILD; CLINICAL OUTCOME; COMMUNITY STRUCTURE; CONTROLLED STUDY; CORTICOSTEROID THERAPY; DNA SEQUENCE; FEMALE; FOLLOW UP; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; MICROFLORA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; SINGLE BLIND PROCEDURE; SKIN FLORA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; BATH; CUTANEOUS DRUG ADMINISTRATION; DERMATITIS, ATOPIC; DRUG EFFECTS; MICROBIOLOGY; PRESCHOOL CHILD; SKIN;

ADMINISTRATION, CUTANEOUS; BATHS; CHILD, PRESCHOOL; DERMATITIS, ATOPIC; DERMATOLOGIC AGENTS; FEMALE; FLUTICASONE; HUMANS; INFANT; MALE; MICROBIOTA; SINGLE-BLIND METHOD; SKIN; SODIUM HYPOCHLORITE; STAPHYLOCOCCUS AUREUS;

EID: 85016137209     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2016.04.066     Document Type: Article

References (67)

1. Eichenfield, L.F., Ellis, C.N., Mancini, A.J., et al. Atopic dermatitis: epidemiology and pathogenesis update. Semin Cutan Med Surg 31:Suppl (2012), S3–S5.
2. Biedermann, T., Dissecting the role of infections in atopic dermatitis. Acta Derm Venereol 86 (2006), 99–109.
3. Kong, H.H., Oh, J., Deming, C., et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Research 22 (2012), 850–859.
4. Bouslimani, A., Porto, C., Rath, C.M., et al. Molecular cartography of the human skin surface in 3D. Proc Natl Acad Sci U S A 112 (2015), E2120–E2129.
5. Eichenfield, L.F., Hanifin, J.M., Luger, T.A., et al. Consensus conference on pediatric atopic dermatitis. J Am Acad Dermatol 49 (2003), 1088–1095.
6. Schmitt, J., Langan, S., Deckert, S., et al. Assessment of clinical signs of atopic dermatitis: a systematic review and recommendation. J Allergy Clin Immunol 132 (2013), 1337–1347.
7. Gao, Z., Perez, I.P., Chen, Y., et al. Quantitation of major human cutaneous bacterial and fungal populations. J Clin Microbiol 48 (2010), 3575–3581.
8. Redel, H., Gao, Z., Li, H., et al. Quantitation and composition of cutaneous microbiota in diabetic and nondiabetic men. J Infect Dis 207 (2013), 1105–1114.
9. Walters, W.A., Caporaso, J.G., Lauber, C.L., et al. PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics 27 (2011), 1159–1161.
10. Caporaso, J.G., Lauber, C.L., Walters, W.A., et al. Ultra-high- throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6 (2012), 1621–1624.
11. Grice, E.A., Kong, H.H., Conlan, S., et al. Topographical and temporal diversity of the human skin microbiome. Science 324 (2009), 1190–1192.
12. Costello, E.K., Lauber, C.L., Hamady, M., et al. Bacterial community variation in human body habitats across space and time. Science 326 (2009), 1694–1707.
13. Findley, K., Oh, J., Yang, J., et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 498 (2013), 367–370.
14. Conlon, S., Kong, H.H., Segre, J.A., Species-level analysis of DNA sequence data from the NIH Human Microbiome Project. PLoS One, 7, 2012, e47075.
15. Grice, E.A., Segre, J.A., The skin microbiome. Nat Rev Microbiol 9:4 (2011), 244–253.
16. Gao, Z., Tseng, C.H., Strober, B.E., et al. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One, 3, 2008, e2719.
17. Fahlén, A., Engstrand, L., Baker, B.S., et al. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res 304 (2012), 15–22.
18. Alekseyenko, A.V., Perez-Perez, G.I., De Souza, A., et al. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome, 23, 2013, 31.
19. Leyden, J.J., Marples, R.R., Kligman, A.M., Staphylococcus aureus in the lesions of atopic dermatitis. Br J Dermatol 90 (1974), 525–530.
20. Higaki, S., Morohashi, M., Yamagishi, T., et al. Comparative study of staphylococci from the skin of atopic dermatitis patients and from healthy subjects. Int J Dermatol 38 (1999), 265–269.
21. Gong, J.Q., Lin, L., Lin, T., et al. Skin colonization by Staphylococcus aureus in patients with eczema and atopic dermatitis and relevant combined topical therapy: a double-blind multicenter randomized controlled trial. Br J Dermatol 155 (2006), 680–687.
22. Breuer, K., Haussler, S., Kapp, A., et al. Staphylococcus aureus: colonizing features and influence of an antibacterial treatment in adults with atopic dermatitis. Br J Dermatol 147 (2002), 55–61.
23. Park, H.Y., Kim, C.R., Huh, I.S., et al. Staphylococcus aureus colonization in acute and chronic skin lesions of patients with atopic dermatitis. Ann Dermatol 25:4 (2013), 410–416.
24. Nilsson, E.J., Henning, C.G., Magnusson, J., Topical corticosteroids and Staphylococcus aureus in atopic dermatitis. J Am Acad Dermatol 27 (1992), 29–34.
25. Guzik, T.J., Bzowska, M., Kasprowicz, A., et al. Persistent skin colonization with Staphylococcus aureus in atopic dermatitis: relationship to clinical and immunological parameters. Clin Exp Allergy 35:4 (2005), 448–455.
26. Clemente, J.C., Pehrsson, E.C., Blaser, M.J., et al. The microbiome of uncontacted Amerindians. Science Advances 1:3 (2015), 1–12.
27. Horton, J.M., Gao, Z., Sullivan, M., et al. The cutaneous microbiome in out-patients presenting acutely with skin abscesses. J Infect Dis 211:12 (2015), 1895–1904.
28. Meadow, J.F., Bateman, A.C., Herkert, K.M., et al. Significant changes in the skin microbiome mediated by the sport of roller derby. Peer J 1 (2013), e53–e70.
29. Matsui, K., Nishikawa, A., Suto, H., et al. Comparative study of Staphylococcus aureus isolated from lesional and nonlesional skin of atopic dermatitis patients. Microbiol Immunol 44:11 (2000), 945–947.
30. Kedzierska, A., Kapińska-Mrowiecka, M., Czubak-Macugowska, M., et al. Susceptibility testing and resistance phenotype detection in Staphylococcus aureus strains isolated from patients with atopic dermatitis, with apparent and recurrent skin colonization. Br J Dermatol 159:6 (2008), 1290–1299.
31. Suarez-Farinas, M., Tintle, S., Shemer, A., et al. Nonlesional atopic dermatitis skin is characterized by broad terminal differentiation defects and variable immune abnormalities. J Allergy Clin Immunol 127:4 (2011), 954–964.
32. Lee, H.J., Lee, S.H., Epidermal permeability barrier defects and barrier repair therapy in atopic dermatitis. Allergy Asthma Immunol Res 6 (2014), 276–287.
33. de Benedetto, A., Slifka, M.K., Rafaels, N.M., et al. Reductions in claudin-1 may enhance susceptibility to herpes simplex virus 1 infections in atopic dermatitis. J Allergy Clin Immunol 128:6 (2011), 1216–1224.
34. Ong, P.Y., Ohtake, T., Brandt, C., et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347 (2002), 1151–1160.
35. Nakamizo, S., Egawa, G., Honda, T., et al. Commensal bacteria and cutaneous immunity. Semin Immunopathol 37 (2015), 73–80.
36. Van Drongelen, V.V., Haisma, E.M., Out-Luiting, J.J., et al. Reduced filaggrin expression is accompanied by increased Staphylococcus aureus colonization of epidermal skin models. Clin Exp Allergy 44 (2014), 1515–1524.
37. Gao, P.S., Rafaels, N.M., Hand, T., et al. Filaggrin mutations that confer risk of atopic dermatitis confer greater risk for eczema herpeticum. J Allergy Clin Immunol 124:3 (2009), 507–513.
38. Oh, J., Freeman, A.F., NISC Comparative Sequencing Program, et al. The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Genome Res 23 (2013), 2103–2114.
39. Kobayashi, T., Glatz, M., Horiuchi, K., et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 42 (2015), 756–766.
40. Bath-Hextall, F.J., Birnie, A.J., Ravenscroft, J.C., et al. Interventions to reduce Staphylococcus aureus in the management of atopic eczema: an updated Cochrane review. Br J Dermatol 163 (2010), 12–26.
41. Huang, J.T., Abrams, M., Tlougan, B., et al. Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics 123 (2009), e808–e814.
42. Wong, S.M., Ng, T.G., Baba, R.J., et al. Efficacy and safety of sodium hypochlorite (bleach) baths in patients with moderate to severe atopic dermatitis in Malaysia. J Dermatol 40 (2013), 874–880.
43. Leung, T.H., Zhang, L.F., Wang, J., et al. Topical hypochlorite ameliorates NF-kB mediated skin diseases in mice. J Clin Invest 123 (2013), 5361–5370.
44. Uehara, Y., Nakama, H., Agematsu, K., et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect 44 (2000), 127–133.
45. Seifert, H., Dijkshoorn, L., Gerner-Smidt, P., et al. Distribution of Acinetobacter species on human skin: comparison of phenotypic and genotypic identification methods. J Clin Microbiol 35 (1997), 2819–2825.
46. Chiller, K., Selkin, B.A., Murakawa, G.J., Skin microflora and bacterial infections of the skin. J Investig Dermatol Symp Proc 6 (2001), 170–174.
47. Dominguez-Bello, M.G., Costello, E.K., 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 107 (2010), 11971–11975.
48. Iwase, T., Uehara, Y., Shinji, H., et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465 (2010), 346–349.
49. Lai, Y., Di Nardo, A., Nakatsuji, T., et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 15:12 (2009), 1377–1382.
50. Braff, M.H., Bardan, A., Nizet, V., et al. Cutaneous defense mechanisms by antimicrobial peptides. J Invest Dermatol 125:1 (2005), 9–13.
51. Shu, M., Wang, Y., Yu, J., et al. Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillin-resistant Staphylococcus aureus. PLoS One, 8, 2013, e55380.
52. Volz, T., Skabytska, Y., Guenova, E., et al. Nonpathogenic bacteria alleviating atopic dermatitis inflammation induce IL-10 producing dendritic cells and regulatory Tr1 cells. J Invest Dermatol 134 (2014), 96–104.
53. Findley, K., Grice, E.A., The skin microbiome: a focus on pathogens and their association with skin disease. PLoS Pathog, 10(10), 2014, e1004436.
54. Stadler, J.F., Fleury, M., Sourisse, M., et al. Local steroid therapy and bacterial skin flora in atopic dermatitis. Br J Dermatol 131 (1994), 536–540.
55. Hung, S.H., Lin, Y.T., Chu, C.Y., et al. Staphylococcus colonization in atopic dermatitis treated with fluticasone or tacrolimus with or without antibiotics. Ann Allergy Asthma Immunol 98:1 (2007), 51–56.
56. Flores, G.E., Seite, S., Henley, J.B., et al. Microbiome of affected and unaffected skin of patients with atopic dermatitis before and after emollient treatment. J Drugs Dermatol 13 (2014), 1365–1372.
57. Aronesty, E., Comparison of sequencing utility programs. Open Bioinformatics J 7 (2013), 1–8.
58. Caporaso, J.G., Kuczynski, J., Stombaugh, J., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
59. McDonald, D., Price, M.N., Goodrich, J., et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6 (2011), 610–618.
60. Caporaso, J.G., Bittinger, K., Bushman, F.D., et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26 (2010), 266–267.
61. Price, M.N., Dehal, P.S., Arkin, A.P., et al. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One, 5, 2010, e9490.
62. R Development Core Team. R: a language and environment for statistical computing. 2012, R Foundation for Statistical Computing, Vienna (Austria).
63. Dray, S., Dufour, A.B., The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22 (2007), 1–20.
64. Cailliez, F., The analytical solution of the additive constant problem. Psychometrika 48 (1983), 305–310.
65. Anderson, M.J., A new method for non-parametric multivariate analysis of variance. Austral Ecology 26 (2001), 32–46.
66. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57 (1995), 289–300.
67. Newson, R., Confidence intervals for rank statistics: Somers' D and extensions. Stata J 6 (2006), 309–334.