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Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention

BACKGROUND: Maternal probiotic supplementation has a promising effect on atopic dermatitis (AD) prevention in infancy. In the randomised controlled study, Probiotics in the Prevention of Allergy among Children in Trondheim (ProPACT), maternal probiotics reduced the cumulative incidence of AD in thei...

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Autores principales: Zakiudin, Dinastry Pramadita, Rø, Anne Dorthea Bjerkenes, Videm, Vibeke, Øien, Torbjørn, Simpson, Melanie Rae
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10386175/
https://www.ncbi.nlm.nih.gov/pubmed/37516841
http://dx.doi.org/10.1186/s12948-023-00186-3
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author Zakiudin, Dinastry Pramadita
Rø, Anne Dorthea Bjerkenes
Videm, Vibeke
Øien, Torbjørn
Simpson, Melanie Rae
author_facet Zakiudin, Dinastry Pramadita
Rø, Anne Dorthea Bjerkenes
Videm, Vibeke
Øien, Torbjørn
Simpson, Melanie Rae
author_sort Zakiudin, Dinastry Pramadita
collection PubMed
description BACKGROUND: Maternal probiotic supplementation has a promising effect on atopic dermatitis (AD) prevention in infancy. In the randomised controlled study, Probiotics in the Prevention of Allergy among Children in Trondheim (ProPACT), maternal probiotics reduced the cumulative incidence of AD in their offspring by 40% at 2 years of age. However, our understanding on how probiotics prevented AD is still limited, and the role of inflammatory proteins in infants following maternal probiotic supplementation is unclear. We hypothesised that maternal probiotics lowered pro-inflammatory proteins and increased anti-inflammatory proteins in their 2-year-old children as a mechanism of AD prevention. We aimed to explore this hypothesis and the association between these proteins and the presence of AD, severity of AD, and the degree of preventive effect of probiotics. METHODS: Plasma samples were collected from 2-year-old children (n = 202) during the ProPACT study, a randomised placebo-controlled trial of maternal probiotic supplementation. These samples were analysed for 92 inflammatory proteins using a multiplex proximity extension assay. Associations between inflammatory proteins and the presence and severity of AD, and the degree of preventive effect, was estimated individually using regression analysis and then collectively using unsupervised cluster analysis. RESULTS: Several proteins were observed to differ between the groups. The probiotic group had lower CCL11 and IL-17C, while children with AD had higher IL-17C, MCP-4, uPA, and CD6. Cytokine CCL20 and IL-18 had moderate correlation (r = 0.35 and r = 0.46) with the severity of AD. The cluster analysis revealed that children in the cluster of samples with the highest value of immune checkpoint receptors and inflammatory suppressor enzymes showed the greatest AD preventive effect from probiotics. CONCLUSIONS: The proteins associated with both maternal probiotic supplementation and the presence and severity of AD warrant attention because of their potential biological relevance. Cluster analysis may provide a new insight when considering which subgroups benefit from probiotic supplementation. Larger studies are needed to confirm the results. Trial registration number: The study was retrospectively registered at ClinicalTrials.gov (NCT00159523) on 12nd September 2005. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12948-023-00186-3.
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spelling pubmed-103861752023-07-30 Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention Zakiudin, Dinastry Pramadita Rø, Anne Dorthea Bjerkenes Videm, Vibeke Øien, Torbjørn Simpson, Melanie Rae Clin Mol Allergy Research BACKGROUND: Maternal probiotic supplementation has a promising effect on atopic dermatitis (AD) prevention in infancy. In the randomised controlled study, Probiotics in the Prevention of Allergy among Children in Trondheim (ProPACT), maternal probiotics reduced the cumulative incidence of AD in their offspring by 40% at 2 years of age. However, our understanding on how probiotics prevented AD is still limited, and the role of inflammatory proteins in infants following maternal probiotic supplementation is unclear. We hypothesised that maternal probiotics lowered pro-inflammatory proteins and increased anti-inflammatory proteins in their 2-year-old children as a mechanism of AD prevention. We aimed to explore this hypothesis and the association between these proteins and the presence of AD, severity of AD, and the degree of preventive effect of probiotics. METHODS: Plasma samples were collected from 2-year-old children (n = 202) during the ProPACT study, a randomised placebo-controlled trial of maternal probiotic supplementation. These samples were analysed for 92 inflammatory proteins using a multiplex proximity extension assay. Associations between inflammatory proteins and the presence and severity of AD, and the degree of preventive effect, was estimated individually using regression analysis and then collectively using unsupervised cluster analysis. RESULTS: Several proteins were observed to differ between the groups. The probiotic group had lower CCL11 and IL-17C, while children with AD had higher IL-17C, MCP-4, uPA, and CD6. Cytokine CCL20 and IL-18 had moderate correlation (r = 0.35 and r = 0.46) with the severity of AD. The cluster analysis revealed that children in the cluster of samples with the highest value of immune checkpoint receptors and inflammatory suppressor enzymes showed the greatest AD preventive effect from probiotics. CONCLUSIONS: The proteins associated with both maternal probiotic supplementation and the presence and severity of AD warrant attention because of their potential biological relevance. Cluster analysis may provide a new insight when considering which subgroups benefit from probiotic supplementation. Larger studies are needed to confirm the results. Trial registration number: The study was retrospectively registered at ClinicalTrials.gov (NCT00159523) on 12nd September 2005. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12948-023-00186-3. BioMed Central 2023-07-29 /pmc/articles/PMC10386175/ /pubmed/37516841 http://dx.doi.org/10.1186/s12948-023-00186-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zakiudin, Dinastry Pramadita
Rø, Anne Dorthea Bjerkenes
Videm, Vibeke
Øien, Torbjørn
Simpson, Melanie Rae
Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title_full Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title_fullStr Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title_full_unstemmed Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title_short Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
title_sort systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10386175/
https://www.ncbi.nlm.nih.gov/pubmed/37516841
http://dx.doi.org/10.1186/s12948-023-00186-3
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