Epithelial barrier hypothesis: Effect of the external exposome on the microbiome and epithelial barriers in allergic disease.

Zeynep Celebi Sozener, Betul Ozdel Ozturk, Pamir Cerci, Murat Turk, Begum Gorgulu Akin, Mubeccel Akdis, Seda Altiner, Umus Ozbey, Ismail Ogulur, Yasutaka Mitamura, Insu Yilmaz, Kari Nadeau, Cevdet Ozdemir, Dilsad Mungan, Cezmi A Akdis

Journal: Allergy 2022;77(5):1418-1449

PMID: 35108405

Abstract

Environmental exposure plays a major role in the development of allergic diseases. The exposome can be classified into internal (e.g., aging, hormones, and metabolic processes), specific external (e.g., chemical pollutants or lifestyle factors), and general external (e.g., broader socioeconomic and psychological contexts) domains, all of which are interrelated. All the factors we are exposed to, from the moment of conception to death, are part of the external exposome. Several hundreds of thousands of new chemicals have been introduced in modern life without our having a full understanding of their toxic health effects and ways to mitigate these effects. Climate change, air pollution, microplastics, tobacco smoke, changes and loss of biodiversity, alterations in dietary habits, and the microbiome due to modernization, urbanization, and globalization constitute our surrounding environment and external exposome. Some of these factors disrupt the epithelial barriers of the skin and mucosal surfaces, and these disruptions have been linked in the last few decades to the increasing prevalence and severity of allergic and inflammatory diseases such as atopic dermatitis, food allergy, allergic rhinitis, chronic rhinosinusitis, eosinophilic esophagitis, and asthma. The epithelial barrier hypothesis provides a mechanistic explanation of how these factors can explain the rapid increase in allergic and autoimmune diseases. In this review, we discuss factors affecting the planet's health in the context of the 'epithelial barrier hypothesis,' including climate change, pollution, changes and loss of biodiversity, and emphasize the changes in the external exposome in the last few decades and their effects on allergic diseases. In addition, the roles of increased dietary fatty acid consumption and environmental substances (detergents, airborne pollen, ozone, microplastics, nanoparticles, and tobacco) affecting epithelial barriers are discussed. Considering the emerging data from recent studies, we suggest stringent governmental regulations, global policy adjustments, patient education, and the establishment of individualized control measures to mitigate environmental threats and decrease allergic disease.

© 2022 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.

Address: Clinic of Immunology and Allergic Diseases, Ankara City Hospital, Ankara, Turkey.; School of Medicine, Department of Chest Diseases, Division of Immunology and Allergic Diseases, Ankara University, Ankara, Turkey.; Clinic of Immunology and Allergic Diseases, Eskisehir City Hospital, Eskisehir, Turkey.; Clinic of Immunology and Allergic Diseases, Kayseri City Hospital, Kayseri, Turkey.; Swiss Institute of Allergy and Asthma Research (SIAF), University of Zurich, Davos, Switzerland.; Clinic of Internal Medicine Division of Immunology and Allergic Diseases, Kahramanmaras Necip Fazil City Hospital, Kahramanmaras, Turkey.; Department of Nutrition and Diet, Ankara University, Ankara, Turkey.; Department of Chest Diseases, Division of Immunology and Allergic Diseases, Erciyes University, Kayseri, Turkey.; Sean N. Parker Center for Allergy and Asthma Research at Stanford University School of Medicine, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Stanford University, Stanford, California, USA.; Institute of Child Health, Department of Pediatric Basic Sciences, Istanbul University, Istanbul, Turkey.; Istanbul Faculty of Medicine, Department of Pediatrics, Division of Pediatric Allergy and Immunology, Istanbul University, Istanbul, Turkey.; Swiss Institute of Allergy and Asthma Research (SIAF), University of Zurich, Davos, Switzerland.; Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland.
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