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      Childhood allergy is preceded by an absence of gut lactobacilli species and higher levels of atopy‐related plasma chemokines

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          Abstract

          Detection of lactobacilli (L. casei, L. paracasei and L. rhamnosus) in feces during the first 2 months of life associates with reduced allergy‐prevalence and lower levels of atopy‐related chemokines in the first year(s) of life, and higher levels of IFN‐g and lower FeNO later in childhood. These associations between lactobacilli, allergy‐protection and the systemic immune profile were apparent also within the subgroup of children with double allergic heredity. The results indicate that the presence of certain lactobacilli species in the infant gut may influence allergy‐related parameters in the peripheral immune system, and thereby contribute to allergy‐protection.

          Summary

          Alterations in the composition and reduced diversity of the infant microbiome are associated with allergic disease in children. Further, an altered microbiota is linked to immune dysregulation, including skewing of different T helper (Th) subsets, which is also seen in atopic individuals. The aim of this study was, therefore, to investigate the associations between gut lactobacilli and Th‐related plasma factors in allergy development during childhood. A total of 194 children with known allergy status at 1 year of age were followed to 10 years of age. We used real‐time polymerase chain reaction (PCR) to investigate the presence of three lactobacilli species ( Lactobacillus casei, L. paracasei, L. rhamnosus) in infant fecal samples (collected between 1 week and 2 months of age) from a subgroup of children. Plasma chemokines and cytokines were quantified at 6 months and at 1, 2, 5 and 10 years of age with Luminex or enzyme‐linked immunosorbent assay (ELISA). Fractional exhaled nitrogen oxide (FeNO) was measured and spirometry performed at 10 years of age. The data were analysed by non‐parametric testing and a logistic regression model adjusted for parental allergy. An absence of these lactobacilli and higher levels of the chemokines BCA‐1/CXCL13, CCL17/TARC, MIP‐3α/CCL20 and MDC/CCL22 in plasma at 6 months of age preceded allergy development. The presence of lactobacilli associated with lower levels of atopy‐related chemokines during infancy, together with higher levels of interferon (IFN)‐γ and lower FeNO during later childhood. The results indicate that the presence of certain lactobacilli species in the infant gut may influence allergy‐related parameters in the peripheral immune system, and thereby contribute to allergy protection.

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          Most cited references35

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          Chemokines and chemokine receptors: positioning cells for host defense and immunity.

          Chemokines are chemotactic cytokines that control the migratory patterns and positioning of all immune cells. Although chemokines were initially appreciated as important mediators of acute inflammation, we now know that this complex system of approximately 50 endogenous chemokine ligands and 20 G protein-coupled seven-transmembrane signaling receptors is also critical for the generation of primary and secondary adaptive cellular and humoral immune responses. Recent studies demonstrate important roles for the chemokine system in the priming of naive T cells, in cell fate decisions such as effector and memory cell differentiation, and in regulatory T cell function. In this review, we focus on recent advances in understanding how the chemokine system orchestrates immune cell migration and positioning at the organismic level in homeostasis, in acute inflammation, and during the generation and regulation of adoptive primary and secondary immune responses in the lymphoid system and peripheral nonlymphoid tissue.
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            Neonatal gut microbiota associates with childhood multi–sensitized atopy and T–cell differentiation

            Altered infant human gut microbiome composition and metabolic activity are implicated in childhood atopy and asthma 1 . We hypothesized that compositionally distinct neonatal human gut microbiota exist and are differentially related to relative–risk (RR) of childhood atopy and asthma. Using stool samples (n = 298; aged 1–11 months) from a US birth cohort and 16S rRNA sequencing, neonates (median age 35 days) were divisible into three microbiota–composition states (NGM1–3). Each incurred significantly different RR for multi–sensitized atopy at age–two years and doctor–diagnosed asthma at age–four years. The highest risk group, NGM3, showed lower relative abundance of certain bacteria (e.g. Bifidobacterium, Akkermansia and Faecalibacterium), higher relative abundance of particular fungi (Candida and Rhodotorula), and a distinct fecal metabolome enriched for pro-inflammatory metabolites. Ex vivo culture of adult human peripheral T–cells with sterile fecal water from NGM3 subjects increased the proportion of CD4+ cells producing interleukin–4 and reduced the relative abundance of Foxp3+CD25+CD4+ cells. 12,13 DiHOME which discriminated NGM3 from lower–risk NGMs, recapitulated the effect of NGM3 fecal water on Foxp3+CD25+CD4+ cell relative abundance. These findings suggest that neonatal gut microbiome dysbiosis drives CD4+ T–cell dysfunction associated with childhood atopy.
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              High levels of butyrate and propionate in early life are associated with protection against atopy

              Dietary changes are suggested to play a role in the increasing prevalence of allergic diseases and asthma. Short-chain fatty acids (SCFAs) are metabolites present in certain foods and are produced by microbes in the gut following fermentation of fibers. SCFAs have been shown to have anti-inflammatory properties in animal models. Our objective was to investigate the potential role of SCFAs in the prevention of allergy and asthma.
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                Author and article information

                Contributors
                eva.sverremark@su.se
                Journal
                Clin Exp Immunol
                Clin Exp Immunol
                10.1111/(ISSN)1365-2249
                CEI
                Clinical and Experimental Immunology
                John Wiley and Sons Inc. (Hoboken )
                0009-9104
                1365-2249
                05 August 2020
                December 2020
                05 August 2020
                : 202
                : 3 ( doiID: 10.1111/cei.v202.3 )
                : 288-299
                Affiliations
                [ 1 ] Department of Molecular Biosciences The Wenner‐Gren Institute Stockholm University Stockholm Sweden
                [ 2 ] Department of Clinical Science and Education Södersjukhuset Karolinska Institutet Stockholm Sweden
                [ 3 ] Sachs’ Children and Youth Hospital Stockholm Sweden
                [ 4 ] Institute for Environmental Medicine Karolinska Institutet Stockholm Sweden
                [ 5 ] Department of Mathematics Stockholm University Stockholm Sweden
                [ 6 ] Department of Biomedical and Clinical Sciences Linköping University Linköping Sweden
                Author notes
                [*] [* ] Correspondence: E. Sverremark-Ekström, Stockholm University, Department of Molecular Biosciences, The Wenner-Gren Institute, Svante Arrhenius Väg 20C, SE 106 91 Stockholm, Sweden.

                E-mail: eva.sverremark@ 123456su.se

                Author information
                https://orcid.org/0000-0001-6271-8681
                Article
                CEI13494
                10.1111/cei.13494
                7670166
                32652542
                a273f868-2d92-40ab-ae67-8572bb068341
                © The Authors. Clinical & Experimental Immunology published by John Wiley & Sons Ltd on behalf of British Society for Immunology

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 27 March 2020
                : 21 June 2020
                : 30 June 2020
                Page count
                Figures: 6, Tables: 3, Pages: 12, Words: 7963
                Funding
                Funded by: H.K.H. Kronprinsessan Lovisas Förening för Barnasjukvård , open-funder-registry 10.13039/501100009757;
                Funded by: Stiftelsen Guldbröllopsminnet
                Funded by: Stiftelsen Olle Engkvist Byggmästare , open-funder-registry 10.13039/501100004200;
                Funded by: Vetenskapsrådet , open-funder-registry 10.13039/501100004359;
                Award ID: 2016‐01715_3
                Funded by: Föreningen Mjölkdroppen
                Funded by: Stiftelsen Frimurare Barnhuset i Stockholm , open-funder-registry 10.13039/501100006741;
                Funded by: Ellen, Walter and Lennart Hesselman Foundation for Scientific Research
                Funded by: Cancer‐ och Allergifonden
                Funded by: Astma‐ och Allergiförbundet , open-funder-registry 10.13039/501100010234;
                Funded by: Hjärt‐Lungfonden , open-funder-registry 10.13039/501100003793;
                Categories
                Original Article
                Original Articles
                Allergy
                Custom metadata
                2.0
                December 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.4 mode:remove_FC converted:17.11.2020

                Immunology
                allergy,chemokines,child,gut lactobacillus,infant,microbiota,plasma
                Immunology
                allergy, chemokines, child, gut lactobacillus, infant, microbiota, plasma

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