Allergy, Asthma & Immunology Research

The Korean Academy of Asthma, Allergy and Clinical Immunology (대한천식알레르기학회)
권호 표지
DOI QR코드

DOI QR Code

Microbiome in the Gut-Skin Axis in Atopic Dermatitis

  • Lee, So-Yeon (Department of Pediatrics, Childhood Asthma Atopy Center, Environmental Health Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Lee, Eun (Department of Pediatrics, Chonnam National University Hospital, Chonnam National University Medical School) ;
  • Park, Yoon Mee (Asan Institute for Life Science, University of Ulsan College of Medicine) ;
  • Hong, Soo-Jong (Department of Pediatrics, Childhood Asthma Atopy Center, Environmental Health Center, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2017.11.15
  • Accepted : 2017.12.29
  • Published : 2018.07.01
⟨ Previous Next ⟩

Abstract

The microbiome is vital for immune system development and homeostasis. Changes in microbial composition and function, termed dysbiosis, in the skin and the gut have recently been linked to alterations in immune responses and to the development of skin diseases, such as atopic dermatitis (AD). In this review, we summarize the recent findings on the gut and skin microbiome, highlighting the roles of major commensals in modulating skin and systemic immunity in AD. Although our understanding of the gut-skin axis is only beginning, emerging evidence indicates that the gut and skin microbiome could be manipulated to treat AD.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF), Korea Health Industry Development Institute (KHIDI)

References

  1. Dharmage SC, Lowe AJ, Matheson MC, Burgess JA, Allen KJ, Abramson MJ. Atopic dermatitis and the atopic march revisited. Allergy 2014; 69:17-27. https://doi.org/10.1111/all.12268
  2. Flohr C, Mann J. New insights into the epidemiology of childhood atopic dermatitis. Allergy 2014;69:3-16. https://doi.org/10.1111/all.12270
  3. Lee SY, Yu J, Ahn KM, Kim KW, Shin YH, Lee KS, et al. Additive effect between IL-13 polymorphism and cesarean section delivery/prenatal antibiotics use on atopic dermatitis: a birth cohort study (COCOA). PLoS One 2014;9:e96603. https://doi.org/10.1371/journal.pone.0096603
  4. Lee JY, Seo JH, Kwon JW, Yu J, Kim BJ, Lee SY, et al. Exposure to gene-environment interactions before 1 year of age may favor the development of atopic dermatitis. Int Arch Allergy Immunol 2012; 157:363-71. https://doi.org/10.1159/000328778
  5. Kim BJ, Lee SY, Kim HB, Lee E, Hong SJ. Environmental changes, microbiota, and allergic diseases. Allergy Asthma Immunol Res 2014;6:389-400. https://doi.org/10.4168/aair.2014.6.5.389
  6. Al-Asmakh M, Zadjali F. Use of germ-free animal models in microbiota-related research. J Microbiol Biotechnol 2015;25:1583-8. https://doi.org/10.4014/jmb.1501.01039
  7. Lebeer S, Vanderleyden J, De Keersmaecker SC. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 2010;8:171-84. https://doi.org/10.1038/nrmicro2297
  8. Ueno N, Fujiya M, Segawa S, Nata T, Moriichi K, Tanabe H, et al. Heat-killed body of lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function. Inflamm Bowel Dis 2011;17:2235-50. https://doi.org/10.1002/ibd.21597
  9. Peng Y, Li A, Yu L, Qin G. The role of probiotics in prevention and treatment for patients with allergic rhinitis: a systematic review. Am J Rhinol Allergy 2015;29:292-8. https://doi.org/10.2500/ajra.2015.29.4192
  10. Kim SO, Ah YM, Yu YM, Choi KH, Shin WG, Lee JY. Effects of probiotics for the treatment of atopic dermatitis: a meta-analysis of randomized controlled trials. Ann Allergy Asthma Immunol 2014;113:217-26. https://doi.org/10.1016/j.anai.2014.05.021
  11. Rather IA, Bajpai VK, Kumar S, Lim J, Paek WK, Park YH. Probiotics and atopic dermatitis: an overview. Front Microbiol 2016;7:507.
  12. Levkovich T, Poutahidis T, Smillie C, Varian BJ, Ibrahim YM, Lakritz JR, et al. Probiotic bacteria induce a 'glow of health'. PLoS One 2013; 8:e53867. https://doi.org/10.1371/journal.pone.0053867
  13. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012;336:489-93. https://doi.org/10.1126/science.1219328
  14. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-5. https://doi.org/10.1038/nature12726
  15. Zeng MY, Inohara N, Nunez G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol 2017;10:18-26. https://doi.org/10.1038/mi.2016.75
  16. Gensollen T, Blumberg RS. Correlation between early-life regulation of the immune system by microbiota and allergy development. J Allergy Clin Immunol 2017;139:1084-91. https://doi.org/10.1016/j.jaci.2017.02.011
  17. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012;129:434-40, 440.e1-2. https://doi.org/10.1016/j.jaci.2011.10.025
  18. Penders J, Stobberingh EE, Thijs C, Adams H, Vink C, van Ree R, et al. Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing. Clin Exp Allergy 2006;36:1602-8. https://doi.org/10.1111/j.1365-2222.2006.02599.x
  19. Lee E, Lee SY, Kang MJ, Kim K, Won S, Kim BJ, et al. Clostridia in the gut and onset of atopic dermatitis via eosinophilic inflammation. Ann Allergy Asthma Immunol 2016;117:91-92.e1. https://doi.org/10.1016/j.anai.2016.04.019
  20. Kirjavainen PV, Arvola T, Salminen SJ, Isolauri E. Aberrant composition of gut microbiota of allergic infants: a target of bifidobacterial therapy at weaning? Gut 2002;51:51-5. https://doi.org/10.1136/gut.51.1.51
  21. Nylund L, Nermes M, Isolauri E, Salminen S, de Vos WM, Satokari R. Severity of atopic disease inversely correlates with intestinal microbiota diversity and butyrate-producing bacteria. Allergy 2015; 70:241-4. https://doi.org/10.1111/all.12549
  22. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569-73. https://doi.org/10.1126/science.1241165
  23. Song H, Yoo Y, Hwang J, Na YC, Kim HS. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J Allergy Clin Immunol 2016;137:852-60. https://doi.org/10.1016/j.jaci.2015.08.021
  24. Lee MJ, Kang MJ, Lee SY, Lee E, Kim K, Won S, et al. Perturbations of gut microbiome genes in infants with atopic dermatitis according to feeding type. J Allergy Clin Immunol 2018;141:1310-9. https://doi.org/10.1016/j.jaci.2017.11.045
  25. Chang YS, Trivedi MK, Jha A, Lin YF, Dimaano L, Garcia-Romero MT. Synbiotics for prevention and treatment of atopic dermatitis: a meta-analysis of randomized clinical trials. JAMA Pediatr 2016;170: 236-42. https://doi.org/10.1001/jamapediatrics.2015.3943
  26. Huang YJ, Marsland BJ, Bunyavanich S, O'Mahony L, Leung DY, Muraro A, et al. The microbiome in allergic disease: current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J Allergy Clin Immunol 2017;139:1099-110. https://doi.org/10.1016/j.jaci.2017.02.007
  27. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3- grabbing nonintegrin. J Allergy Clin Immunol 2005;115:1260-7. https://doi.org/10.1016/j.jaci.2005.03.036
  28. Nowrouzian FL, Lina G, Hodille E, Lindberg E, Hesselmar B, Saalman R, et al. Superantigens and adhesins of infant gut commensal Staphylococcus aureus strains and association with subsequent development of atopic eczema. Br J Dermatol 2017;176:439-45. https://doi.org/10.1111/bjd.15138
  29. Gueniche A, Philippe D, Bastien P, Reuteler G, Blum S, Castiel-Higounenc I, et al. Randomised double-blind placebo-controlled study of the effect of Lactobacillus paracasei NCC 2461 on skin reactivity. Benef Microbes 2014;5:137-45. https://doi.org/10.3920/BM2013.0001
  30. Hashimoto K. Regulation of keratinocyte function by growth factors. J Dermatol Sci 2000;24 Suppl 1:S46-50. https://doi.org/10.1016/S0923-1811(00)00141-9
  31. Reichardt N, Duncan SH, Young P, Belenguer A, McWilliam Leitch C, Scott KP, et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 2014;8:1323-35. https://doi.org/10.1038/ismej.2014.14
  32. Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity 2014;40:833-42. https://doi.org/10.1016/j.immuni.2014.05.014
  33. Kaikiri H, Miyamoto J, Kawakami T, Park SB, Kitamura N, Kishino S, et al. Supplemental feeding of a gut microbial metabolite of linoleic acid, 10-hydroxy-cis-12-octadecenoic acid, alleviates spontaneous atopic dermatitis and modulates intestinal microbiota in NC/nga mice. Int J Food Sci Nutr 2017;68:941-51. https://doi.org/10.1080/09637486.2017.1318116
  34. Matsumoto M, Ebata T, Hirooka J, Hosoya R, Inoue N, Itami S, et al. Antipruritic effects of the probiotic strain LKM512 in adults with atopic dermatitis. Ann Allergy Asthma Immunol 2014;113:209-216.e7. https://doi.org/10.1016/j.anai.2014.05.002
  35. Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med 2016;22:1187-91. https://doi.org/10.1038/nm.4176
  36. Checa A, Holm T, Sjodin MO, Reinke SN, Alm J, Scheynius A, et al. Lipid mediator profile in vernix caseosa reflects skin barrier development. Sci Rep 2015;5:15740. https://doi.org/10.1038/srep15740
  37. Jin UH, Lee SO, Sridharan G, Lee K, Davidson LA, Jayaraman A, et al. Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Mol Pharmacol 2014;85:777-88. https://doi.org/10.1124/mol.113.091165
  38. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13:701-12. https://doi.org/10.1038/nrn3346
  39. Yokoyama S, Hiramoto K, Koyama M, Ooi K. Impairment of skin barrier function via cholinergic signal transduction in a dextran sulphate sodium-induced colitis mouse model. Exp Dermatol 2015; 24:779-84. https://doi.org/10.1111/exd.12775
  40. Akiyama T, Iodi Carstens M, Carstens E. Transmitters and pathways mediating inhibition of spinal itch-signaling neurons by scratching and other counterstimuli. PLoS One 2011;6:e22665. https://doi.org/10.1371/journal.pone.0022665
  41. Lee HJ, Park MK, Kim SY, Park Choo HY, Lee AY, Lee CH. Serotonin induces melanogenesis via serotonin receptor 2A. Br J Dermatol 2011;165:1344-8. https://doi.org/10.1111/j.1365-2133.2011.10490.x
  42. O'Neill CA, Monteleone G, McLaughlin JT, Paus R. The gut-skin axis in health and disease: A paradigm with therapeutic implications. BioEssays 2016;38:1167-76. https://doi.org/10.1002/bies.201600008
  43. Eyerich K, Novak N. Immunology of atopic eczema: overcoming the Th1/Th2 paradigm. Allergy 2013;68:974-82. https://doi.org/10.1111/all.12184
  44. Smith FJ, Irvine AD, Terron-Kwiatkowski A, Sandilands A, Campbell LE, Zhao Y, et al. Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nat Genet 2006;38:337-42. https://doi.org/10.1038/ng1743
  45. Seite S, Bieber T. Barrier function and microbiotic dysbiosis in atopic dermatitis. Clin Cosmet Investig Dermatol 2015;8:479-83.
  46. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, et al. Topographical and temporal diversity of the human skin microbiome. Science 2009;324:1190-2. https://doi.org/10.1126/science.1171700
  47. Kennedy EA, Connolly J, Hourihane JO, Fallon PG, McLean WH, Murray D, et al. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J Allergy Clin Immunol 2017;139:166-72. https://doi.org/10.1016/j.jaci.2016.07.029
  48. Nakatsuji T, Chen TH, Narala S, Chun KA, Two AM, Yun T, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med 2017;9:eaah4680. https://doi.org/10.1126/scitranslmed.aah4680
  49. Thomas CL, Fernandez-Penas P. The microbiome and atopic eczema: more than skin deep. Australas J Dermatol 2017;58:18-24.
  50. Jun SH, Lee JH, Kim SI, Choi CW, Park TI, Jung HR, et al. Staphylococcus aureus-derived membrane vesicles exacerbate skin inflammation in atopic dermatitis. Clin Exp Allergy 2017;47:85-96. https://doi.org/10.1111/cea.12851
  51. Oh J, Freeman AF, Park M, Sokolic R, Candotti F, Holland SM, et al. The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Genome Res 2013;23:2103-14. https://doi.org/10.1101/gr.159467.113
  52. Nakatsuji T, Chen TH, Two AM, Chun KA, Narala S, Geha RS, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol 2016; 136:2192-200. https://doi.org/10.1016/j.jid.2016.05.127
  53. Laborel-Preneron E, Bianchi P, Boralevi F, Lehours P, Fraysse F, Morice-Picard F, et al. Effects of the Staphylococcus aureus and Staphylococcus epidermidis secretomes isolated from the skin microbiota of atopic children on CD4+ T cell activation. PLoS One 2015;10:e0141067. https://doi.org/10.1371/journal.pone.0141067
  54. Martin H, Laborel-Preneron E, Fraysse F, Nguyen T, Schmitt AM, Redoules D, et al. Aquaphilus dolomiae extract counteracts the effects of cutaneous S. aureus secretome isolated from atopic children on CD4+ T cell activation. Pharm Biol 2016;54:2782-5. https://doi.org/10.3109/13880209.2016.1173069
  55. Kim MH, Rho M, Choi JP, Choi HI, Park HK, Song WJ, et al. A Metagenomic Analysis Provides a Culture-Independent Pathogen Detection for Atopic Dermatitis. Allergy Asthma Immunol Res 2017; 9:453-61. https://doi.org/10.4168/aair.2017.9.5.453
  56. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 2012;22:850-9. https://doi.org/10.1101/gr.131029.111
  57. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010;465:346-9. https://doi.org/10.1038/nature09074
  58. Kobayashi T, Glatz M, Horiuchi K, Kawasaki H, Akiyama H, Kaplan DH, et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 2015;42:756-66. https://doi.org/10.1016/j.immuni.2015.03.014
  59. Scharschmidt TC, Vasquez KS, Truong HA, Gearty SV, Pauli ML, Nosbaum A, et al. A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes. Immunity 2015;43:1011-21. https://doi.org/10.1016/j.immuni.2015.10.016
  60. Oh J, Byrd AL, Deming C, Conlan S, Kong HH, Segre JA; NISC Comparative Sequencing Program. Biogeography and individuality shape function in the human skin metagenome. Nature 2014;514:59-64. https://doi.org/10.1038/nature13786
  61. Chng KR, Tay AS, Li C, Ng AH, Wang J, Suri BK, et al. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. New Microbiol 2016;1:16106.
  62. Lack G, Fox D, Northstone K, Golding J; Avon Longitudinal Study of Parents and Children Study Team. Factors associated with the development of peanut allergy in childhood. N Engl J Med 2003;348: 977-85. https://doi.org/10.1056/NEJMoa013536
  63. Kelleher MM, Dunn-Galvin A, Gray C, Murray DM, Kiely M, Kenny L, et al. Skin barrier impairment at birth predicts food allergy at 2 years of age. J Allergy Clin Immunol 2016;137:1111-1116.e8. https://doi.org/10.1016/j.jaci.2015.12.1312
  64. Bartnikas LM, Gurish MF, Burton OT, Leisten S, Janssen E, Oettgen HC, et al. Epicutaneous sensitization results in IgE-dependent intestinal mast cell expansion and food-induced anaphylaxis. J Allergy Clin Immunol 2013;131:451-460.e1-6. https://doi.org/10.1016/j.jaci.2012.11.032
  65. Noti M, Kim BS, Siracusa MC, Rak GD, Kubo M, Moghaddam AE, et al. Exposure to food allergens through inflamed skin promotes intestinal food allergy through the thymic stromal lymphopoietinbasophil axis. J Allergy Clin Immunol 2014;133:1390-9, 1399.e1-6. https://doi.org/10.1016/j.jaci.2014.01.021
  66. Galand C, Leyva-Castillo JM, Yoon J, Han A, Lee MS, McKenzie AN, et al. IL-33 promotes food anaphylaxis in epicutaneously sensitized mice by targeting mast cells. J Allergy Clin Immunol 2016;138:1356-66. https://doi.org/10.1016/j.jaci.2016.03.056
  67. Wang Q, Du J, Zhu J, Yang X, Zhou B. Thymic stromal lymphopoietin signaling in CD4(+) T cells is required for TH2 memory. J Allergy Clin Immunol 2015;135:781-791.e3. https://doi.org/10.1016/j.jaci.2014.09.015
  68. Lee JB, Chen CY, Liu B, Mugge L, Angkasekwinai P, Facchinetti V, et al. IL-25 and CD4(+) TH2 cells enhance type 2 innate lymphoid cellderived IL-13 production, which promotes IgE-mediated experimental food allergy. J Allergy Clin Immunol 2016;137:1216-1225.e5. https://doi.org/10.1016/j.jaci.2015.09.019
  69. Chen CY, Lee JB, Liu B, Ohta S, Wang PY, Kartashov AV, et al. Induction of interleukin-9-producing mucosal mast cells promotes susceptibility to IgE-mediated experimental food allergy. Immunity 2015;43:788-802. https://doi.org/10.1016/j.immuni.2015.08.020
  70. Mondoulet L, Dioszeghy V, Puteaux E, Ligouis M, Dhelft V, Plaquet C, et al. Specific epicutaneous immunotherapy prevents sensitization to new allergens in a murine model. J Allergy Clin Immunol 2015;135:1546-1557.e4. https://doi.org/10.1016/j.jaci.2014.11.028
  71. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001;2:725-31. https://doi.org/10.1038/90667
  72. Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, et al. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol 2003;111:587-91. https://doi.org/10.1067/mai.2003.105
  73. Mah KW, Bjorksten B, Lee BW, van Bever HP, Shek LP, Tan TN, et al. Distinct pattern of commensal gut microbiota in toddlers with eczema. Int Arch Allergy Immunol 2006;140:157-63. https://doi.org/10.1159/000092555
  74. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 2007;56:661-7. https://doi.org/10.1136/gut.2006.100164
  75. van Nimwegen FA, Penders J, Stobberingh EE, Postma DS, Koppelman GH, Kerkhof M, et al. Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J Allergy Clin Immunol 2011;128:948-955.e1-3. https://doi.org/10.1016/j.jaci.2011.07.027
  76. Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann K, Lau S, et al. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol 2013;132:601-607.e8. https://doi.org/10.1016/j.jaci.2013.05.043
  77. Shi B, Bangayan NJ, Curd E, Taylor PA, Gallo RL, Leung DY, et al. The skin microbiome is different in pediatric versus adult atopic dermatitis. J Allergy Clin Immunol 2016;138:1233-6. https://doi.org/10.1016/j.jaci.2016.04.053
  78. Drago L, De Grandi R, Altomare G, Pigatto P, Rossi O, Toscano M. Skin microbiota of first cousins affected by psoriasis and atopic dermatitis. Clin Mol Allergy 2016;14:2. https://doi.org/10.1186/s12948-016-0038-z

Cited by

  1. When is it useful to act on microbiota in atopic children? A recent experience vol.71, pp.1, 2018, https://doi.org/10.23736/s0026-4946.18.05425-7
  2. Pathophysiology of atopic dermatitis vol.17, pp.4, 2018, https://doi.org/10.1111/ddg.13819
  3. Pathophysiologie der atopischen Dermatitis vol.17, pp.4, 2018, https://doi.org/10.1111/ddg.13819_g
  4. Microbiome of the Skin and Gut in Atopic Dermatitis (AD): Understanding the Pathophysiology and Finding Novel Management Strategies vol.8, pp.4, 2018, https://doi.org/10.3390/jcm8040444
  5. Intestinal Fatty Acid Binding Protein, a Biomarker of Intestinal Barrier, is Associated with Severity of Psoriasis vol.8, pp.7, 2018, https://doi.org/10.3390/jcm8071021
  6. Microbiota and Immune-Mediated Skin Diseases-An Overview vol.7, pp.9, 2018, https://doi.org/10.3390/microorganisms7090279
  7. Staphylococcus aureus and the Cutaneous Microbiota Biofilms in the Pathogenesis of Atopic Dermatitis vol.7, pp.9, 2019, https://doi.org/10.3390/microorganisms7090301
  8. Targeting the gut‐skin axis—Probiotics as new tools for skin disorder management? vol.28, pp.11, 2018, https://doi.org/10.1111/exd.14016
  9. Markers of microbial exposure lower the incidence of atopic dermatitis vol.75, pp.1, 2018, https://doi.org/10.1111/all.13990
  10. FFA2 Activation Ameliorates 2,4-Dinitrochlorobenzene-Induced Atopic Dermatitis in Mice vol.28, pp.3, 2018, https://doi.org/10.4062/biomolther.2019.160
  11. Caesarean delivery and the risk of atopic dermatitis in children vol.50, pp.7, 2018, https://doi.org/10.1111/cea.13668
  12. Therapeutic responses to Roseomonas mucosa in atopic dermatitis may involve lipid-mediated TNF-related epithelial repair vol.12, pp.560, 2020, https://doi.org/10.1126/scitranslmed.aaz8631
  13. Metagenomic Studies in Inflammatory Skin Diseases vol.77, pp.11, 2020, https://doi.org/10.1007/s00284-020-02163-4
  14. A compromised developmental trajectory of the infant gut microbiome and metabolome in atopic eczema vol.12, pp.1, 2018, https://doi.org/10.1080/19490976.2020.1801964
  15. Mechanisms Underlying the Skin-Gut Cross Talk in the Development of IgE-Mediated Food Allergy vol.12, pp.12, 2018, https://doi.org/10.3390/nu12123830
  16. Factores de riesgo socioambientales asociados a la presencia de síntomas de atopias en niños menores de 3 años vol.30, pp.1, 2021, https://doi.org/10.35366/100112
  17. El rol de la microbiota intestinal en la dermatitis atópica vol.30, pp.2, 2021, https://doi.org/10.35366/101177
  18. Therapeutic targeting of the IL-13 pathway in skin inflammation vol.17, pp.1, 2018, https://doi.org/10.1080/1744666x.2020.1858802
  19. Colonic Transendoscopic Enteral Tubing: Route for a Novel, Safe, and Convenient Delivery of Washed Microbiota Transplantation in Children vol.2021, pp.None, 2021, https://doi.org/10.1155/2021/6676962
  20. Effect of Acupuncture on Gut-Brain Axis Parameters in Patients with Atopic Dermatitis: A Study Protocol for a Randomized, Participant- and Assessor-Blind, Sham-Controlled Trial vol.2021, pp.None, 2018, https://doi.org/10.1155/2021/5584247
  21. Delayed Gut Colonization Shapes Future Allergic Responses in a Murine Model of Atopic Dermatitis vol.12, pp.None, 2018, https://doi.org/10.3389/fimmu.2021.650621
  22. Diversity analysis of gut microbiota between healthy controls and those with atopic dermatitis in a Chinese population vol.48, pp.2, 2021, https://doi.org/10.1111/1346-8138.15530
  23. The clinical implications of the microbiome in the development of allergy diseases vol.17, pp.2, 2018, https://doi.org/10.1080/1744666x.2021.1874353
  24. Prebiotics in atopic dermatitis prevention and management vol.78, pp.None, 2021, https://doi.org/10.1016/j.jff.2021.104352
  25. Impact of diet and the bacterial microbiome on the mucous barrier and immune disorders vol.76, pp.3, 2021, https://doi.org/10.1111/all.14548
  26. Influence of constipation on atopic dermatitis: A nationwide population‐based cohort study in Taiwan vol.75, pp.3, 2018, https://doi.org/10.1111/ijcp.13691
  27. Gardenia Jasminoides Ameliorates Antibiotic-Associated Aggravation of DNCB-Induced Atopic Dermatitis by Restoring the Intestinal Microbiome Profile vol.13, pp.4, 2021, https://doi.org/10.3390/nu13041349
  28. Preventive oral supplementation with Bifidobacterium longum 51A alleviates oxazolone-induced allergic contact dermatitis-like skin inflammation in mice vol.12, pp.2, 2021, https://doi.org/10.3920/bm2020.0134
  29. A Combined Analysis of Gut and Skin Microbiota in Infants with Food Allergy and Atopic Dermatitis: A Pilot Study vol.13, pp.5, 2018, https://doi.org/10.3390/nu13051682
  30. Gut–organ axis: a microbial outreach and networking vol.72, pp.6, 2018, https://doi.org/10.1111/lam.13333
  31. Perspectives from the Society for Pediatric Research: Probiotic use in urinary tract infections, atopic dermatitis, and antibiotic-associated diarrhea: an overview vol.90, pp.2, 2018, https://doi.org/10.1038/s41390-020-01298-1
  32. Practical algorithm to inform clinical decision‐making in the topical treatment of atopic dermatitis vol.48, pp.8, 2018, https://doi.org/10.1111/1346-8138.15921
  33. TH2 sensitization in the skin‐gut‐brain axis: How early‐life Th2‐mediated inflammation may negatively perpetuate developmental and psychologic abnormalities vol.38, pp.5, 2018, https://doi.org/10.1111/pde.14657
  34. A Journey on the Skin Microbiome: Pitfalls and Opportunities vol.22, pp.18, 2021, https://doi.org/10.3390/ijms22189846
  35. ITS2 Sequencing and Targeted Meta-Proteomics of Infant Gut Mycobiome Reveal the Functional Role of Rhodotorula sp. during Atopic Dermatitis Manifestation vol.7, pp.9, 2018, https://doi.org/10.3390/jof7090748
  36. Role of maternal tryptophan metabolism in allergic diseases in the offspring vol.51, pp.10, 2018, https://doi.org/10.1111/cea.13953
  37. Effects of Feeding a Hypoallergenic Diet with a Nutraceutical on Fecal Dysbiosis Index and Clinical Manifestations of Canine Atopic Dermatitis vol.11, pp.10, 2021, https://doi.org/10.3390/ani11102985
  38. Host/Malassezia Interaction: A Quantitative, Non-Invasive Method Profiling Oxylipin Production Associates Human Skin Eicosanoids with Malassezia vol.11, pp.10, 2018, https://doi.org/10.3390/metabo11100700
  39. Effects of Heat-Killed Lactococcus lactis Strain Plasma on Skin Homeostasis-Related Genes and the Skin Microbiome among Healthy Adults: A Randomized Controlled Double-Blind Study vol.9, pp.10, 2021, https://doi.org/10.3390/microorganisms9102029
  40. Probiotics Regulate Gut Microbiota: An Effective Method to Improve Immunity vol.26, pp.19, 2018, https://doi.org/10.3390/molecules26196076
  41. The Clinical Relevance of the Microbiome in Hidradenitis Suppurativa: A Systematic Review vol.9, pp.10, 2021, https://doi.org/10.3390/vaccines9101076
  42. Metabolomics reveals microbial‐derived metabolites associated with immunoglobulin E responses in filaggrin‐related atopic dermatitis vol.32, pp.8, 2021, https://doi.org/10.1111/pai.13570
  43. Homemade Kefir Consumption Improves Skin Condition-A Study Conducted in Healthy and Atopic Volunteers vol.10, pp.11, 2018, https://doi.org/10.3390/foods10112794
  44. A Bibliometric Analysis of Atopic Dermatitis Research over the Past Three Decades and Future Perspectives vol.9, pp.12, 2018, https://doi.org/10.3390/healthcare9121749
  45. Baicalin ameliorates 2,4-dinitrochlorobenzene-induced atopic dermatitis-like skin lesions in mice through modulating skin barrier function, gut microbiota and JAK/STAT pathway vol.119, pp.None, 2018, https://doi.org/10.1016/j.bioorg.2021.105538