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

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          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.

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          Most cited references121

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          Atopic Dermatitis: Global Epidemiology and Risk Factors

          Atopic dermatitis (AD) is a chronic inflammatory skin disease posing a significant burden on health-care resources and patients' quality of life. It is a complex disease with a wide spectrum of clinical presentations and combinations of symptoms. AD affects up to 20% of children and up to 3% of adults; recent data show that its prevalence is still increasing, especially in low-income countries. First manifestations of AD usually appear early in life and often precede other allergic diseases such as asthma or allergic rhinitis. Individuals affected by AD usually have genetically determined risk factors affecting the skin barrier function or the immune system. However, genetic mutations alone might not be enough to cause clinical manifestations of AD, and it is merely the interaction of a dysfunctional epidermal barrier in genetically predisposed individuals with harmful effects of environmental agents which leads to the development of the disease. AD has been described as an allergic skin disease, but today, the contribution of allergic reactions to the initiation of AD is challenged, and it is proposed that allergy is rather a consequence of AD in subjects with a concomitant underlying atopic constitution. Treatment at best achieves symptom control rather than cure; there is thus a strong need to identify alternatives for disease prevention.
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            Skin microbiota: a source of disease or defence?

            Microbes found on the skin are usually regarded as pathogens, potential pathogens or innocuous symbiotic organisms. Advances in microbiology and immunology are revising our understanding of the molecular mechanisms of microbial virulence and the specific events involved in the host-microbe interaction. Current data contradict some historical classifications of cutaneous microbiota and suggest that these organisms may protect the host, defining them not as simple symbiotic microbes but rather as mutualistic. This review will summarize current information on bacterial skin flora including Staphylococcus, Corynebacterium, Propionibacterium, Streptococcus and Pseudomonas. Specifically, the review will discuss our current understanding of the cutaneous microbiota as well as shifting paradigms in the interpretation of the roles microbes play in skin health and disease.
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              Regulation of the immune system by biodiversity from the natural environment: An ecosystem service essential to health

              Epidemiological studies suggest that living close to the natural environment is associated with long-term health benefits including reduced death rates, reduced cardiovascular disease, and reduced psychiatric problems. This is often attributed to psychological mechanisms, boosted by exercise, social interactions, and sunlight. Compared with urban environments, exposure to green spaces does indeed trigger rapid psychological, physiological, and endocrinological effects. However, there is little evidence that these rapid transient effects cause long-term health benefits or even that they are a specific property of natural environments. Meanwhile, the illnesses that are increasing in high-income countries are associated with failing immunoregulation and poorly regulated inflammatory responses, manifested as chronically raised C-reactive protein and proinflammatory cytokines. This failure of immunoregulation is partly attributable to a lack of exposure to organisms (“Old Friends”) from mankind’s evolutionary past that needed to be tolerated and therefore evolved roles in driving immunoregulatory mechanisms. Some Old Friends (such as helminths and infections picked up at birth that established carrier states) are almost eliminated from the urban environment. This increases our dependence on Old Friends derived from our mothers, other people, animals, and the environment. It is suggested that the requirement for microbial input from the environment to drive immunoregulation is a major component of the beneficial effect of green space, and a neglected ecosystem service that is essential for our well-being. This insight will allow green spaces to be designed to optimize health benefits and will provide impetus from health systems for the preservation of ecosystem biodiversity.
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                Author and article information

                Contributors
                susan.prescott@uwa.edu.au
                Journal
                World Allergy Organ J
                World Allergy Organ J
                The World Allergy Organization Journal
                BioMed Central (London )
                1939-4551
                22 August 2017
                22 August 2017
                2017
                : 10
                : 1
                : 29
                Affiliations
                [1 ]ISNI 0000 0004 0625 8600, GRID grid.410667.2, School of Paediatrics and Child Health, , University of Western Australia and Princess Margaret Hospital for Children, ; PO Box D184, Perth, WA 6001 Australia
                [2 ]In-FLAME Global Network, of the World Universities Network (WUN), West New York, USA
                [3 ]ISNI 0000 0004 0389 4302, GRID grid.1038.a, School of Science, , Edith Cowan University, ; 270 Joondalup Drive, Joondalup, WA 6027 Australia
                [4 ]ISNI 0000 0001 1034 3451, GRID grid.12650.30, Department of Clinical Sciences, Pediatrics, , Umeå University, ; Umeå, Sweden
                [5 ]ISNI 0000000122483208, GRID grid.10698.36, , University of North Carolina School of Medicine, ; Chapel Hill, North Carolina USA
                [6 ]ISNI 0000 0004 0486 624X, GRID grid.412885.2, , Institute for Immunological Research, University of Cartagena, ; Cartagena, Colombia
                [7 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Division of Paediatric Allergy, , University of Cape Town, ; Cape Town, South Africa
                [8 ]GRID grid.17089.37, Department of Pediatrics, , University of Alberta, ; Edmonton, Canada
                [9 ]ISNI 0000 0000 9690 854X, GRID grid.413973.b, , Children’s Hospital at Westmead, ; Sydney, Australia
                [10 ]ISNI 0000 0004 1936 834X, GRID grid.1013.3, Discipline of Child and Adolescent Health, , University of Sydney, ; Sydney, Australia
                Article
                160
                10.1186/s40413-017-0160-5
                5568566
                28855974
                ee4ff60d-3036-43c5-80a0-3bc656b767d2
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 24 March 2017
                : 28 June 2017
                Categories
                Review
                Custom metadata
                © The Author(s) 2017

                Immunology
                skin,microbiome,microbiota,inflammation,allergy,cytokines,biodiversity,colonisation,antibiotics,dohad,ecosystems,prevention,ncds,caesarean section,pregnancy

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