The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming

Susan L Prescott, Danica-Lea Larcombe, Alan C Logan, Christina West, Wesley Burks, Luis Caraballo, Michael Levin, Eddie Van Etten, Pierre Horwitz, Anita Kozyrskyj, Dianne E Campbell, Susan L Prescott, Danica-Lea Larcombe, Alan C Logan, Christina West, Wesley Burks, Luis Caraballo, Michael Levin, Eddie Van Etten, Pierre Horwitz, Anita Kozyrskyj, Dianne E Campbell

Abstract

Skin barrier structure and function is essential to human health. Hitherto unrecognized functions of epidermal keratinocytes show that the skin plays an important role in adapting whole-body physiology to changing environments, including the capacity to produce a wide variety of hormones, neurotransmitters and cytokine that can potentially influence whole-body states, and quite possibly, even emotions. Skin microbiota play an integral role in the maturation and homeostatic regulation of keratinocytes and host immune networks with systemic implications. As our primary interface with the external environment, the biodiversity of skin habitats is heavily influenced by the biodiversity of the ecosystems in which we reside. Thus, factors which alter the establishment and health of the skin microbiome have the potential to predispose to not only cutaneous disease, but also other inflammatory non-communicable diseases (NCDs). Indeed, disturbances of the stratum corneum have been noted in allergic diseases (eczema and food allergy), psoriasis, rosacea, acne vulgaris and with the skin aging process. The built environment, global biodiversity losses and declining nature relatedness are contributing to erosion of diversity at a micro-ecological level, including our own microbial habitats. This emphasises the importance of ecological perspectives in overcoming the factors that drive dysbiosis and the risk of inflammatory diseases across the life course.

Keywords: Allergy; Antibiotics; Biodiversity; Caesarean section; Colonisation; Cytokines; DOHaD; Ecosystems; Inflammation; Microbiome; Microbiota; NCDs; Pregnancy; Prevention; Skin.

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Figures

Fig. 1
Fig. 1
The interdependent mutualistic relationship between commensal microbes and the host maintains tissue homeostasis, inhibiting local inflammation. Regulatory responses generated in the skin also have systemic immunomodulatory effects
Fig. 2
Fig. 2
Both exogenous and endogenous factors interact with the physical and functional aspects of the skin barrier unit – through effects on both host cells and the skin microbiome – to alter both the integrity and the activity (hormonal, metabolic, and immune) of the skin
Fig. 3
Fig. 3
Erosion of environmental ecosystems is affecting biodiversity and microbial ecology. Together with declining nature-relatedness this is reducing human contact with immunomodulatory organisms found in natural environments – reflected in differences in skin microbes. This is increasingly being recognised as a risk factor for chronic inflammatory diseases
Fig. 4
Fig. 4
Early life is a critical period for establishment of both the microbiome and immune responses, with long term implications for health. Understanding modulating factors during this period could lead to targets for disease prevention

References

    1. Lehtimaki J, Karkman A, Laatikainen T, et al. Patterns in the skin microbiota differ in children and teenagers between rural and urban environments. Sci Rep. 2017;7:45651. doi: 10.1038/srep45651.
    1. Blaser MJ, Dominguez-Bello MG. The human Microbiome before birth. Cell Host Microbe. 2016;20(5):558–560. doi: 10.1016/j.chom.2016.10.014.
    1. Sanford JA, Gallo RL. Functions of the skin microbiota in health and disease. Semin Immunol. 2013;25(5):370–377. doi: 10.1016/j.smim.2013.09.005.
    1. Hanski I, von Hertzen L, Fyhrquist N, et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A. 2012;109(21):8334–8339. doi: 10.1073/pnas.1205624109.
    1. von Hertzen L, Beutler B, Bienenstock J, et al. Helsinki alert of biodiversity and health. Ann Med. 2015;47(3):218–225. doi: 10.3109/07853890.2015.1010226.
    1. Stamper CE, Hoisington AJ, Gomez OM, et al. The Microbiome of the built environment and human behavior: implications for emotional health and well-being in postmodern western societies. Int Rev Neurobiol. 2016;131:289–323. doi: 10.1016/bs.irn.2016.07.006.
    1. Nutten S. Atopic dermatitis: global epidemiology and risk factors. Ann Nutr Metab. 2015;66(Suppl 1):8–16. doi: 10.1159/000370220.
    1. Thiboutot D, Del Rosso JQ. Acne Vulgaris and the epidermal barrier: is acne Vulgaris associated with inherent epidermal abnormalities that cause impairment of barrier functions? Do any topical acne therapies Alter the structural and/or functional integrity of the epidermal barrier? J Clin Aesthet Dermatol. 2013;6(2):18–24.
    1. Boireau-Adamezyk E, Baillet-Guffroy A, Stamatas GN. Age-dependent changes in stratum corneum barrier function. Skin Res Technol. 2014;20(4):409–415. doi: 10.1111/srt.12132.
    1. Darido C, Georgy SR, Jane SM. The role of barrier genes in epidermal malignancy. Oncogene. 2016;35(44):5705–5712. doi: 10.1038/onc.2016.84.
    1. Biniek K, Levi K, Dauskardt RH. Solar UV radiation reduces the barrier function of human skin. Proc Natl Acad Sci U S A. 2012;109(42):17111–17116. doi: 10.1073/pnas.1206851109.
    1. Del Rosso JQ, Levin J. The clinical relevance of maintaining the functional integrity of the stratum corneum in both healthy and disease-affected skin. J Clin Aesthet Dermatol. 2011;4(9):22–42.
    1. Percoco G, Merle C, Jaouen T, et al. Antimicrobial peptides and pro-inflammatory cytokines are differentially regulated across epidermal layers following bacterial stimuli. Exp Dermatol. 2013;22(12):800–806. doi: 10.1111/exd.12259.
    1. van Smeden J, Bouwstra JA. Stratum Corneum lipids: their role for the skin barrier function in healthy subjects and atopic dermatitis patients. Curr Probl Dermatol. 2016;49:8–26. doi: 10.1159/000441540.
    1. Bordenstein SR, Theis KR. Host biology in light of the Microbiome: ten principles of Holobionts and Hologenomes. PLoS Biol. 2015;13(8):e1002226. doi: 10.1371/journal.pbio.1002226.
    1. Grice EA, Kong HH, Conlan S, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324(5931):1190–1192. doi: 10.1126/science.1171700.
    1. Oh J, Byrd AL, Deming C, et al. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59–64. doi: 10.1038/nature13786.
    1. Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nature medicine. 2017;23(3):314–26.
    1. Baviera G, Leoni MC, Capra L, et al. Microbiota in healthy skin and in atopic eczema. Biomed Res Int. 2014;2014:436921. doi: 10.1155/2014/436921.
    1. Cogen AL, Nizet V, Gallo RL. Skin microbiota: a source of disease or defence? Br J Dermatol. 2008;158(3):442–455. doi: 10.1111/j.1365-2133.2008.08437.x.
    1. Simpson EL, Chalmers JR, Hanifin JM, et al. Emollient enhancement of the skin barrier from birth offers effective atopic dermatitis prevention. J Allergy Clin Immunol. 2014;134(4):818–823. doi: 10.1016/j.jaci.2014.08.005.
    1. Addor FA, Takaoka R, Rivitti EA, Aoki V. Atopic dermatitis: correlation between non-damaged skin barrier function and disease activity. Int J Dermatol. 2012;51(6):672–676. doi: 10.1111/j.1365-4632.2011.05176.x.
    1. Stremnitzer C, Manzano-Szalai K, Willensdorfer A, et al. Papain degrades tight junction proteins of human Keratinocytes in vitro and sensitizes C57BL/6 mice via the skin independent of its enzymatic activity or TLR4 activation. J Invest Dermatol. 2015;135(7):1790–1800. doi: 10.1038/jid.2015.58.
    1. Cork MJ, Danby SG, Vasilopoulos Y, et al. Epidermal barrier dysfunction in atopic dermatitis. J Investig Dermatol. 2009;129:1892–1908. doi: 10.1038/jid.2009.133.
    1. Alduraywish SA, Standl M, Lodge CJ, et al. Is there a march from early food sensitization to later childhood allergic airway disease? Results from two prospective birth cohort studies. Pediatr Allergy Immunol. 2016;28(1):30–37. doi: 10.1111/pai.12651.
    1. Hill DJ, Sporik R, Thorburn J, Hosking CS. The association of atopic dermatitis in infancy with immunoglobulin E food sensitization. J Pediatr. 2000;137(4):475–479. doi: 10.1067/mpd.2000.108207.
    1. Fallon PG, Sasaki T, Sandilands A, et al. A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet. 2009;41(5):602–608. doi: 10.1038/ng.358.
    1. Bin L, Leung DY. Genetic and epigenetic studies of atopic dermatitis. Allergy Asthma Clin Immunol. 2016;12:52. doi: 10.1186/s13223-016-0158-5.
    1. Prescott SL. The allergy epidemic: a mystery of modern life. Perth: UWA Publishing; 2011.
    1. Lim MY, You HJ, Yoon HS, et al. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut. 2017;66(6):1031–1038. doi: 10.1136/gutjnl-2015-311326.
    1. Si J, Lee S, Park JM, Sung J, Ko G. Genetic associations and shared environmental effects on the skin microbiome of Korean twins. BMC Genomics. 2015;16:992. doi: 10.1186/s12864-015-2131-y.
    1. Belkaid Y, Tamoutounour S. The influence of skin microorganisms on cutaneous immunity. Nat Rev Immunol. 2016;16(6):353–366. doi: 10.1038/nri.2016.48.
    1. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9(4):244–253. doi: 10.1038/nrmicro2537.
    1. Alsterholm M, Strombeck L, Ljung A, et al. Variation in Staphylococcus aureus Colonization in Relation to Disease Severity in Adults with Atopic Dermatitis during av Five-month Follow-up. Acta Derm Venereol. 2017;97(7):802–7.
    1. Clausen ML, Edslev SM, Andersen PS, Clemmensen K, Krogfelt KA, Agner T. Staphylococcus aureus colonization in atopic eczema and its association with filaggrin gene mutations. Br J Dermatol. 2017. [Epub ahead of print].
    1. Iwase T, Uehara Y, Shinji H, et al. Staphylococcus epidermidis esp inhibits Staphylococcus aureus Biofilm formation and nasal colonization. Nature. 2010;465(7296):346–349. doi: 10.1038/nature09074.
    1. Kennedy EA, Connolly J, Hourihane JO, 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. 2016;139(1):166–172. doi: 10.1016/j.jaci.2016.07.029.
    1. Chng KR, Tay AS, Li C, et al. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nat Microbiol. 2016;1(9):16106. doi: 10.1038/nmicrobiol.2016.106.
    1. Paus R, et al. The Skin and endocrine disorders. In: Griffiths C, et al., editors. Rook’s textbook of dermatology. Ninth. London: Wiley Blackwell; 2016. pp. 1–30.
    1. Pavlovic S, Daniltchenko M, Tobin DJ, et al. Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J Investig Dermatol. 2008;128(2):434–446. doi: 10.1038/sj.jid.5701079.
    1. Mijouin L, Hillion M, Ramdani Y, et al. Effects of a skin neuropeptide (substance p) on cutaneous microflora. PLoS One. 2013;8(11):e78773. doi: 10.1371/journal.pone.0078773.
    1. N'Diaye A, Mijouin L, Hillion M, et al. Effect of substance P in Staphylococcus aureus and Staphylococcus epidermidis virulence: implication for skin homeostasis. Front Microbiol. 2016;7:506. doi: 10.3389/fmicb.2016.00506.
    1. Zhan M, Zheng W, Jiang Q, et al. Upregulated expression of substance P (SP) and NK1R in eczema and SP-induced mast cell accumulation. Cell Biol Toxicol. 2017;33(4):389–405. doi: 10.1007/s10565-016-9379-0.
    1. Lee WJ, Jung HD, Lee HJ, Kim BS, Lee SJ, Kim DW. Influence of substance-P on cultured sebocytes. Arch Dermatol Res. 2008;300(6):311–316. doi: 10.1007/s00403-008-0854-1.
    1. Negi O, Tominaga M, Tengara S, et al. Topically applied semaphorin 3A ointment inhibits scratching behavior and improves skin inflammation in NC/Nga mice with atopic dermatitis. J Dermatol Sci. 2012;66(1):37–43. doi: 10.1016/j.jdermsci.2012.01.007.
    1. Denda M. Sensing environmental factors: the emerging role of receptors in epidermal homeostasis and whole-body health. In: (Ed.) GTW, ed. Skin stress response pathways. Switzerland: Springer International Publishing; 2016.
    1. Zhu G, Janjetovic Z, Slominski A. On the role of environmental humidity on cortisol production by epidermal keratinocytes. Exp Dermatol. 2014;23(1):15–17. doi: 10.1111/exd.12275.
    1. Takei K, Denda S, Kumamoto J, Denda M. Low environmental humidity induces synthesis and release of cortisol in an epidermal organotypic culture system. Exp Dermatol. 2013;22(10):662–664. doi: 10.1111/exd.12224.
    1. Marrs T, Flohr C. The role of skin and gut microbiota in the development of atopic eczema. Br J Dermatol. 2016;175(Suppl 2):13–18. doi: 10.1111/bjd.14907.
    1. Hannigan GD, Grice EA. Microbial ecology of the skin in the era of metagenomics and molecular microbiology. Cold Spring Harb Perspect Med. 2013;3(12):a015362. doi: 10.1101/cshperspect.a015362.
    1. Mulder IE, Schmidt B, Stokes CR, et al. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol. 2009;7(1):79. doi: 10.1186/1741-7007-7-79.
    1. Naik S, Bouladoux N, Wilhelm C, et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012;337(6098):1115–1119. doi: 10.1126/science.1225152.
    1. Yuzhakova DV, Shirmanova MV, Bocharov AA, et al. Microbiota induces expression of tumor necrosis factor in postnatal mouse skin. Biochemistry (Mosc) 2016;81(11):1303–1308. doi: 10.1134/S0006297916110080.
    1. Ege MJ, Herzum I, Buchele G, et al. Prenatal exposure to a farm environment modifies atopic sensitization at birth. J Allergy Clin Immunol. 2008;122(2):407–412. doi: 10.1016/j.jaci.2008.06.011.
    1. Conrad ML, Ferstl R, Teich R, et al. Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J Exp Med. 2009;206(13):2869–2877. doi: 10.1084/jem.20090845.
    1. Brand S, Teich R, Dicke T, et al. Epigenetic regulation in murine offspring as a novel mechanism for transmaternal asthma protection induced by microbes. J Allergy Clin Immunol. 2011;128(3):618–625. doi: 10.1016/j.jaci.2011.04.035.
    1. Fyhrquist N, Ruokolainen L, Suomalainen A, et al. Acinetobacter species in the skin microbiota protect against allergic sensitization and inflammation. J Allergy Clin Immunol. 2014;134(6):1301–1309. doi: 10.1016/j.jaci.2014.07.059.
    1. Nisbet EK, Zelenski JM, Murphy SA. The nature relatedness scale: linking individuals’ connection with nature to environmental concern and behavior. Environ Behav. 2009;41:715–740. doi: 10.1177/0013916508318748.
    1. Prescott SL, Logan AC. Transforming life: a broad view of the developmental origins of health and disease concept from an ecological justice perspective. Int J Environ Res Public Health. 2016;13(11)(Nov 3).
    1. Ruokolainen L, Paalanen L, Karkman A, et al. Significant disparities in allergy prevalence and microbiota between the young people in Finnish and Russian Karelia. Clin Exp Allergy. 2017;47(5):665–674. doi: 10.1111/cea.12895.
    1. Lowry CA, Smith DG, Siebler PH, et al. The Microbiota, Immunoregulation, and mental health: implications for public health. Curr Environ Health Rep. 2016;3(3):270–286. doi: 10.1007/s40572-016-0100-5.
    1. Reber SO, Siebler PH, Donner NC, et al. Immunization with a heat-killed preparation of the environmental bacterium mycobacterium vaccae promotes stress resilience in mice. Proc Natl Acad Sci U S A. 2016;113(22):E3130–E3139. doi: 10.1073/pnas.1600324113.
    1. Jorjao AL, de Oliveira FE, Leao MV, Carvalho CA, Jorge AO, de Oliveira LD. Live and heat-killed lactobacillus rhamnosus ATCC 7469 may induce Modulatory cytokines profiles on macrophages RAW 264.7. TheScientificWorldJOURNAL. 2015;2015:716749. doi: 10.1155/2015/716749.
    1. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558(Pt 1):263–275. doi: 10.1113/jphysiol.2004.063388.
    1. Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158(4):705–721. doi: 10.1016/j.cell.2014.05.052.
    1. Logan AC, Jacka FN, Craig JM, Prescott SL. The Microbiome and mental health: looking back, moving forward with lessons from allergic diseases. Clin Psychopharmacol Neurosci. 2016;14(2):131–147. doi: 10.9758/cpn.2016.14.2.131.
    1. Bowe WP, Logan AC. Acne vulgaris, probiotics and the gut-brain-skin axis - back to the future? Gut pathogens. 2011;3(1):1. doi: 10.1186/1757-4749-3-1.
    1. Segata N. Gut Microbiome: westernization and the disappearance of intestinal diversity. Curr Biol. 2015;25(14):R611–R613. doi: 10.1016/j.cub.2015.05.040.
    1. Rook GA. Regulation of the immune system by biodiversity from the natural environment: an ecosystem service essential to health. Proc Natl Acad Sci U S A. 2013;110(46):18360–18367. doi: 10.1073/pnas.1313731110.
    1. Stiemsma LT, Reynolds LA, Turvey SE, Finlay BB. The hygiene hypothesis: current perspectives and future therapies. Immunotargets Ther. 2015;4:143–157. doi: 10.2147/ITT.S61528.
    1. World Health Organisation . Biodiversity and human health: a state of knowledge review. Switzerland: WHO; 2015.
    1. Scharschmidt TC, Vasquez KS, Truong HA, et al. A wave of regulatory T cells into neonatal skin mediates tolerance to Commensal microbes. Immunity. 2015;43(5):1011–1021. doi: 10.1016/j.immuni.2015.10.016.
    1. Kobayashi T, Glatz M, Horiuchi K, et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity. 2015;42(4):756–766. doi: 10.1016/j.immuni.2015.03.014.
    1. Jones CA, Holloway JA, Warner JO. Does atopic disease start in foetal life? Allergy. 2000;55(1):2–10. doi: 10.1034/j.1398-9995.2000.00109.x.
    1. Kemp MW, Saito M, Nitsos I, Jobe AH, Kallapur SG, Newnham JP. Exposure to in utero lipopolysaccharide induces inflammation in the fetal ovine skin. Reprod Sci. 2011;18(1):88–98. doi: 10.1177/1933719110380470.
    1. Romano-Keeler J, Weitkamp JH. Maternal influences on fetal microbial colonization and immune development. Pediatr Res. 2015;77(1–2):189–195. doi: 10.1038/pr.2014.163.
    1. Perez-Munoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017;5(1):48. doi: 10.1186/s40168-017-0268-4.
    1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra265. doi: 10.1126/scitranslmed.3008599.
    1. Gur TL, Worly BL, Bailey MT. Stress and the commensal microbiota: importance in parturition and infant neurodevelopment. Front Psychiatry. 2015;6:5. doi: 10.3389/fpsyt.2015.00005.
    1. McCloskey K, Vuillermin P, Carlin JB, et al. Perinatal microbial exposure may influence aortic intima-media thickness in early infancy. International journal of epidemiology. 2016;46(1):209–218. doi: 10.1093/ije/dyw042.
    1. West CE, Jenmalm MC, Prescott SL. The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin Exp Allergy. 2015;45(1):43–53. doi: 10.1111/cea.12332.
    1. Palmer DJ, Metcalfe J, Makrides M, et al. Early regular egg exposure in infants with eczema: a randomized controlled trial. J Allergy Clin Immunol. 2013;132(2):387–392. doi: 10.1016/j.jaci.2013.05.002.
    1. 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;107(26):11971–11975. doi: 10.1073/pnas.1002601107.
    1. Szabo K, Erdei L, Bolla BS, Tax G, Biro T, Kemeny L. Factors shaping the composition of the cutaneous microbiota. Br J Dermatol. 2016;176(2):344–351. doi: 10.1111/bjd.14967.
    1. Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin Microbiome early in life. J Investig Dermatol. 2011;131(10):2026–2032. doi: 10.1038/jid.2011.168.
    1. Bendiks M, Kopp MV. The relationship between advances in understanding the Microbiome and the maturing hygiene hypothesis. Curr Allergy Asthma Rep. 2013;13(5):487–494. doi: 10.1007/s11882-013-0382-8.
    1. Stensballe LG, Simonsen J, Jensen SM, Bonnelykke K, Bisgaard H. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162(4):832–838. doi: 10.1016/j.jpeds.2012.09.049.
    1. Goulet O. Potential role of the intestinal microbiota in programming health and disease. Nutr Rev. 2015;73(Suppl 1):32–40. doi: 10.1093/nutrit/nuv039.
    1. Gur TL, Shay L, Palkar AV, et al. Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain, behavior, and immunity. 2016;64:50–8.
    1. Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250–253. doi: 10.1038/nm.4039.
    1. Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016;16(1):86. doi: 10.1186/s12876-016-0498-0.
    1. Horimukai K, Morita K, Narita M, et al. Application of moisturizer to neonates prevents development of atopic dermatitis. J Allergy Clin Immunol. 2014;134(4):824–830. doi: 10.1016/j.jaci.2014.07.060.
    1. Prescott SL, Dunstan JA, Hale J, et al. Clinical effects of probiotics are associated with increased interferon-gamma responses in very young children with atopic dermatitis. Clin Exp Allergy. 2005;35(12):1557–1564. doi: 10.1111/j.1365-2222.2005.02376.x.
    1. Weston S, Halbert A, Richmond P, Prescott SL. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child. 2005;90:892–897. doi: 10.1136/adc.2004.060673.
    1. Song SJ, Lauber C, Costello EK, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife U6. 2013;2:e00458.
    1. Maier RM, Palmer MW, Andersen GL, et al. Environmental determinants of and impact on childhood asthma by the bacterial community in household dust. Appl Environ Microbiol. 2010;76(8):2663–2667. doi: 10.1128/AEM.01665-09.
    1. Meadow JF, Altrichter AE, Bateman AC, et al. Humans differ in their personal microbial cloud. PeerJ. 2015;3:e1258. doi: 10.7717/peerj.1258.
    1. Meadow JF, Altrichter AE, Kembel SW, et al. Bacterial communities on classroom surfaces vary with human contact. Microbiome. 2014;2(1):7. doi: 10.1186/2049-2618-2-7.
    1. Meadow JF, Altrichter AE, Green JL. Mobile phones carry the personal microbiome of their owners. PeerJ. 2014;2:e447. doi: 10.7717/peerj.447.
    1. Meadow JF, Altrichter AE, Kembel SW, et al. Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source. Indoor Air. 2014;24(1):41–48. doi: 10.1111/ina.12047.
    1. Caraballo L, Zakzuk J, Lee BW, et al. Particularities of allergy in the tropics. World Allergy Organ J. 2016;9:20. doi: 10.1186/s40413-016-0110-7.
    1. Meadow JF, Bateman AC, Herkert KM, O'Connor TK, Green JL. Significant changes in the skin microbiome mediated by the sport of roller derby. PeerJ. 2013;1:e53. doi: 10.7717/peerj.53.
    1. Sugita T, Cho O. Significance of changes in the skin fungal Microbiomes of astronauts staying on the International Space Station (mini special issue on space microbiology: microbial monitoring in the International Space Station: Kibo) J Dis Res. 2015;10(6):1031–1034. doi: 10.20965/jdr.2015.p1031.
    1. Sugita T, Yamazaki T, Yamada S, et al. Temporal changes in the skin Malassezia microbiota of members of the Japanese Antarctic research expedition (JARE): a case study in Antarctica as a pseudo-space environment. Med Mycol. 2015;53(7):717–724. doi: 10.1093/mmy/myv041.
    1. Audebert C, Even G, Cian A, et al. Colonization with the enteric protozoa Blastocystis is associated with increased diversity of human gut bacterial microbiota. Sci Rep. 2016;6:25255. doi: 10.1038/srep25255.
    1. Shi B, Bangayan NJ, Curd E, et al. The skin microbiome is different in pediatric versus adult atopic dermatitis. J Allergy Clin Immunol. 2016;138(4):1233–1236. doi: 10.1016/j.jaci.2016.04.053.
    1. Karkman A, Lehtimaki J, Ruokolainen L. The ecology of human microbiota: dynamics and diversity in health and disease. Ann N Y Acad Sci. 2017. [Epub ahead of print].
    1. Prescott SL, Logan AC, Millstein RA, Katszman MA. Biodiversity, the human Microbiome and mental health: moving toward a new clinical ecology for the 21st century? Int J Biodiversity 2016;Volume 2016(Article ID 2718275):1-18.
    1. Logan AC, Jacka FN, Prescott SL. Immune-Microbiota interactions: Dysbiosis as a Global Health issue. Curr Allergy Asthma Rep. 2016;16(2):13. doi: 10.1007/s11882-015-0590-5.
    1. Whitmee S, Haines A, Beyrer C, et al. Safeguarding human health in the Anthropocene epoch: report of the Rockefeller Foundation-lancet commission on planetary health. Lancet. 2015;386(10007):1973–2028. doi: 10.1016/S0140-6736(15)60901-1.
    1. Ecosystems and Human Well-Being: Synthesis . Millenium Ecosystem Assessment. Washington DC: Island Press; 2005.
    1. Kuo M. How might contact with nature promote human health? Promising mechanisms and a possible central pathway. Front Psychol. 2015;6:1093.
    1. Craig JM, Logan AC, Prescott SL. Natural environments, nature relatedness and the ecological theater: connecting satellites and sequencing to shinrin-yoku. J Physiol Anthropol. 2016;35:1. doi: 10.1186/s40101-016-0083-9.
    1. Nisbet EK, Zelenski JM. The NR-6: a new brief measure of nature relatedness. Front Psychol. 2013;4:813. doi: 10.3389/fpsyg.2013.00813.
    1. Capaldi CA, Dopko RL, Zelenski JM. The relationship between nature connectedness and happiness: a meta-analysis. Front Psychol. 2014;5:976. doi: 10.3389/fpsyg.2014.00976.
    1. Cox DTC, Hudson HL, Shanahan DF, Fuller RA, Gaston KJ. The rarity of direct experiences of nature in an urban population. Landsc Urban Plan. 2017;160:79–84. doi: 10.1016/j.landurbplan.2016.12.006.
    1. Braun-Fahrlander C, Riedler J, Herz U, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. New Engl J Med. 2002;347(12):869–877. doi: 10.1056/NEJMoa020057.
    1. Riedler J, Eder W, Oberfeld G, Schreuer M. Austrian children living on a farm have less hay fever, asthma and allergic sensitization. Clin Exp Allergy. 2000;30(2):194–200. doi: 10.1046/j.1365-2222.2000.00799.x.
    1. Stein MM, Hrusch CL, Gozdz J, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016;375(5):411–421. doi: 10.1056/NEJMoa1508749.
    1. Ruokolainen L, von Hertzen L, Fyhrquist N, et al. Green areas around homes reduce atopic sensitization in children. Allergy. 2015;70(2):195–202. doi: 10.1111/all.12545.
    1. Schnorr SL. The diverse microbiome of the hunter-gatherer. Nature. 2015;518(7540):S14–S15. doi: 10.1038/518S14a.
    1. Hospodsky D, Pickering AJ, Julian TR, et al. Hand bacterial communities vary across two different human populations. Microbiology. 2014;160(Pt 6):1144–1152. doi: 10.1099/mic.0.075390-0.
    1. Ying S, Zeng DN, Chi L, et al. The influence of age and gender on skin-associated microbial communities in urban and rural human populations. PLoS One. 2015;10(10):e0141842. doi: 10.1371/journal.pone.0141842.
    1. Haahtela T, Holgate S, Pawankar R, et al. The biodiversity hypothesis and allergic disease: world allergy organization position statement. World Allergy Organ J. 2013;6(1):3. doi: 10.1186/1939-4551-6-3.
    1. Timm S, Svanes C, Janson C, et al. Place of upbringing in early childhood as related to inflammatory bowel diseases in adulthood: a population-based cohort study in northern Europe. Eur J Epidemiol. 2014;29(6):429–437. doi: 10.1007/s10654-014-9922-3.
    1. Mantler A, Logan AC. Natural environments and mental health. Adv Integr Med. 2015;2(1):5–12. doi: 10.1016/j.aimed.2015.03.002.
    1. Alenius H, Pakarinen J, Saris O, et al. Contrasting immunological effects of two disparate dusts - preliminary observations. Int Arch Allergy Immunol. 2009;149(1):81–90. doi: 10.1159/000176310.
    1. Hui N, Jumpponen A, Francini G, et al. Soil microbial communities are shaped by vegetation type and park age in cities under cold climate. Environ Microbiol. 2017;19(3):1281–1295. doi: 10.1111/1462-2920.13660.
    1. Heederik D, von Mutius E. Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma? J Allergy Clin Immunol. 2012;130(1):44–50. doi: 10.1016/j.jaci.2012.01.067.
    1. Mhuireach G, Johnson BR, Altrichter AE, et al. Urban greenness influences airborne bacterial community composition. The Science of the total environment. 2016;571:680–7.
    1. Lymperopoulou DS, Adams RI, Lindow SE. Contribution of vegetation to the microbial composition of nearby outdoor air. Appl Environ Microbiol. 2016;82(13):3822–3833. doi: 10.1128/AEM.00610-16.
    1. Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;4:1431. doi: 10.1038/ncomms2441.
    1. Matthews DM, Jenks SM. Ingestion of mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice. Behav Process. 2013;96:27–35. doi: 10.1016/j.beproc.2013.02.007.
    1. Lim SK, Kwon MS, Lee J, et al. Weissella cibaria WIKIM28 ameliorates atopic dermatitis-like skin lesions by inducing tolerogenic dendritic cells and regulatory T cells in BALB/c mice. Sci Rep. 2017;7:40040. doi: 10.1038/srep40040.
    1. Lowry CA, Hollis JH, de Vries A, et al. Identification of an immune-responsive mesolimbocortical serotonergic system: potential role in regulation of emotional behavior. Neuroscience. 2007;146(2):756–772. doi: 10.1016/j.neuroscience.2007.01.067.
    1. Pelucchi C, Galeone C, Bach JF, La Vecchia C, Chatenoud L. Pet exposure and risk of atopic dermatitis at the pediatric age: a meta-analysis of birth cohort studies. J Allergy Clin Immunol. 2013;132(3):616–622. doi: 10.1016/j.jaci.2013.04.009.
    1. Thorsteinsdottir S, Thyssen JP, Stokholm J, Vissing NH, Waage J, Bisgaard H. Domestic dog exposure at birth reduces the incidence of atopic dermatitis. Allergy. 2016;71(12):1736–1744. doi: 10.1111/all.12980.
    1. GLobal Change and Public Health: Addressing the Ecological Determinants of Health. Ottawa: Canadian Public Health Association; May 2015.
    1. Wilson M. The city of tomorrow is a petri dish - by design. 2016; . Accessed 20 Nov 2016.
    1. Gardiner MM, Burkman CE, Prajzner SP. The value of urban vacant land to support arthropod biodiversity and ecosystem services. Environ Entomol. 2013;42(6):1123–1136. doi: 10.1603/EN12275.
    1. Garvin EC, Cannuscio CC, Branas CC. Greening vacant lots to reduce violent crime: a randomised controlled trial. Inj Prev. 2013;19(3):198–203. doi: 10.1136/injuryprev-2012-040439.
    1. South EC, Kondo MC, Cheney RA, Branas CC. Neighborhood blight, stress, and health: a walking trial of urban greening and ambulatory heart rate. Am J Public Health. 2015;105(5):909–913. doi: 10.2105/AJPH.2014.302526.
    1. Thaler DS. Toward a microbial Neolithic revolution in buildings. Microbiome. 2016;4:14. doi: 10.1186/s40168-016-0157-2.
    1. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2014(4):CD005496.
    1. Lau CS, Chamberlain RS. Probiotic administration can prevent necrotizing enterocolitis in preterm infants: a meta-analysis. J Pediatr Surg. 2015;50(8):1405–1412. doi: 10.1016/j.jpedsurg.2015.05.008.
    1. Srinivasjois R, Rao S, Patole S. Prebiotic supplementation in preterm neonates: updated systematic review and meta-analysis of randomised controlled trials. Clin Nutr. 2013;32(6):958–965. doi: 10.1016/j.clnu.2013.05.009.
    1. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–1697. doi: 10.1126/science.1177486.
    1. Myles IA, Williams KW, Reckhow JD, et al. Transplantation of human skin microbiota in models of atopic dermatitis. JCI Insight. 2016;1(10).
    1. Szollosi AG, Gueniche A, Jammayrac O, et al. Bifidobacterium longum extract exerts pro-differentiating effects on human epidermal keratinocytes, in vitro. Exp Dermatol. 2017;26(1):92–94. doi: 10.1111/exd.13130.
    1. Gueniche A, Bastien P, Ovigne JM, et al. Bifidobacterium longum lysate, a new ingredient for reactive skin. Exp Dermatol. 2010;19(8):e1–e8. doi: 10.1111/j.1600-0625.2009.00932.x.
    1. Lopes EG, Moreira DA, Gullon P, Gullon B, Cardelle-Cobas A, Tavaria FK. Topical application of probiotics in skin: adhesion, antimicrobial and antibiofilm in vitro assays. J Appl Microbiol. 2017;122(2):450–461. doi: 10.1111/jam.13349.
    1. Baquerizo Nole KL, Yim E, Keri JE. Probiotics and prebiotics in dermatology. J Am Acad Dermatol. 2014;71(4):814–821. doi: 10.1016/j.jaad.2014.04.050.
    1. Seite S, Oresajo C. Using a specific emollient to manage skin microbiome dysbiosis. J Am Acad Dermatol. 2016;74(5):AB89. Supplement 1.
    1. Seite 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. doi: 10.2147/CCID.S121910.
    1. Al-Ghazzewi FH, Tester RF. Effect of konjac glucomannan hydrolysates and probiotics on the growth of the skin bacterium Propionibacterium acnes in vitro. Int J Cosmet Sci. 2010;32(2):139–142. doi: 10.1111/j.1468-2494.2009.00555.x.
    1. Bateni E, Tester RF, Al-Ghazzewi F, Bateni S, Alvani K, Piggott J. The use of Konjac Glucomannan Hydrolysates (GMH) to improve the health of the skin and reduce acne Vulgaris. Am J Dermatol Venereol. 2013;2(2):10–14.
    1. Cuello-Garcia CA, Fiocchi A, Pawankar R, et al. World allergy organization-McMaster University guidelines for allergic disease prevention (GLAD-P): Prebiotics. World Allergy Organ J. 2016;9:10. doi: 10.1186/s40413-016-0102-7.
    1. Fiocchi A, Pawankar R, Cuello-Garcia C, et al. World allergy organization-McMaster University guidelines for allergic disease prevention (GLAD-P): Probiotics. World Allergy Organ J. 2015;8(1):4. doi: 10.1186/s40413-015-0055-2.
    1. Fabbrocini G, Bertona M, Picazo O, Pareja-Galeano H, Monfrecola G, Emanuele E. Supplementation with lactobacillus rhamnosus SP1 normalises skin expression of genes implicated in insulin signalling and improves adult acne. Benef Microbes. 2016;7(5):625–630. doi: 10.3920/BM2016.0089.
    1. Ishii Y, Sugimoto S, Izawa N, Sone T, Chiba K, Miyazaki K. Oral administration of Bifidobacterium breve attenuates UV-induced barrier perturbation and oxidative stress in hairless mice skin. Arch Dermatol Res. 2014;306(5):467–473. doi: 10.1007/s00403-014-1441-2.
    1. Logan AC, Venket Rao A, Irani D. Chronic fatigue syndrome: lactic acid bacteria may be of therapeutic value. Med Hypotheses. 2003;60(6):915–923. doi: 10.1016/S0306-9877(03)00096-3.
    1. Logan AC, Katzman M. Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses. 2005;64:533–538. doi: 10.1016/j.mehy.2004.08.019.
    1. Huang R, Wang K, Hu J. Effect of Probiotics on Depression: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients. 2016;8(8).
    1. Pirbaglou M, Katz J, de Souza RJ, Stearns JC, Motamed M, Ritvo P. Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials. Nutr Res. 2016;36(9):889–898. doi: 10.1016/j.nutres.2016.06.009.
    1. Gluck U, Gebbers JO. Ingested probiotics reduce nasal colonization with pathogenic bacteria (Staphylococcus aureus, Streptococcus Pneumoniae, and beta-hemolytic streptococci) Am J Clin Nutr. 2003;77(2):517–520.
    1. Schuijt TJ, Lankelma JM, Scicluna BP, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65(4):575–583. doi: 10.1136/gutjnl-2015-309728.
    1. Xu HL, Wen LM, Hardy LL, Rissel C. Associations of outdoor play and screen time with nocturnal sleep duration and pattern among young children. Acta Paediatr. 2016;105(3):297–303. doi: 10.1111/apa.13285.
    1. Trinh L, Wong B, Faulkner GE. The independent and interactive associations of screen time and physical activity on mental health, school connectedness and academic achievement among a population-based sample of youth. J Can Acad Child Ado. 2015;24(1):17–24.
    1. Feng Q, Zhang QL, Du Y, Ye YL, He QQ. Associations of physical activity, screen time with depression, anxiety and sleep quality among Chinese college freshmen. PLoS One. 2014;9(6):e100914. doi: 10.1371/journal.pone.0100914.
    1. Soga M, Gaston KJ, Yamaura Y, Kurisu K, Hanaki K. Both Direct and Vicarious Experiences of Nature Affect Children’s Willingness to Conserve Biodiversity. Int J Environ Res Public Health. 2016;13(6).
    1. Lewis M, Townsend M. ‘ecological embeddedness’ and its public health implications: findings from an exploratory study. EcoHealth. 2015;12(2):244–252. doi: 10.1007/s10393-014-0987-y.
    1. Lohr VI, Pearson-Mims CH. The relative influence of childhood activities and demographics on adult appreciation for the role of trees in human well-being. Acta Hortic. 2004;639:253–259. doi: 10.17660/ActaHortic.2004.639.33.
    1. Lohr VI, Pearson-Mims CH. Children’s active and passive interactions with plants influence their attitudes and actions toward trees and gardening as adults. HortTechnology. 2005;15(3):472–476.
    1. Greenblum S, Carr R, Borenstein E. Extensive strain-level copy-number variation across human gut microbiome species. Cell. 2015;160(4):583–594. doi: 10.1016/j.cell.2014.12.038.
    1. Chiou WL. Oral tetracyclines may not be effective in treating acne: dominance of the placebo effect. Int J Clin Pharmacol Ther. 2012;50(3):157–161. doi: 10.5414/CP201650.
    1. Barnard E, Shi B, Kang D, Craft N, Li H. The balance of metagenomic elements shapes the skin microbiome in acne and health. Sci Rep. 2016;6:39491. doi: 10.1038/srep39491.
    1. Campbell CE, Strassmann BI. The blemishes of modern society? Acne prevalence in the Dogon of Mali. Evol Med Public Health. 2016;2016(1):325–337. doi: 10.1093/emph/eow027.
    1. Cordain L, Lindeberg S, Hurtado M, Hill K, Eaton SB, Brand-Miller J. Acne vulgaris: a disease of western civilization. Arch Dermatol. 2002;138(12):1584–1590. doi: 10.1001/archderm.138.12.1584.
    1. Hoisington AJ, Brenner LA, Kinney KA, Postolache TT, Lowry CA. The microbiome of the built environment and mental health. Microbiome. 2015;3:60. doi: 10.1186/s40168-015-0127-0.

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