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

Abstract 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...

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Main Authors: Dinastry Pramadita Zakiudin, Anne Dorthea Bjerkenes Rø, Vibeke Videm, Torbjørn Øien, Melanie Rae Simpson
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Clinical and Molecular Allergy
Subjects:
Online Access:https://doi.org/10.1186/s12948-023-00186-3
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author Dinastry Pramadita Zakiudin
Anne Dorthea Bjerkenes Rø
Vibeke Videm
Torbjørn Øien
Melanie Rae Simpson
author_facet Dinastry Pramadita Zakiudin
Anne Dorthea Bjerkenes Rø
Vibeke Videm
Torbjørn Øien
Melanie Rae Simpson
author_sort Dinastry Pramadita Zakiudin
collection DOAJ
description Abstract 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.
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spelling doaj.art-bc3df511f29e4750b103586c58df617d2023-07-30T11:21:58ZengBMCClinical and Molecular Allergy1476-79612023-07-0121111110.1186/s12948-023-00186-3Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis preventionDinastry Pramadita Zakiudin0Anne Dorthea Bjerkenes Rø1Vibeke Videm2Torbjørn Øien3Melanie Rae Simpson4Department of Public Health and Nursing, NTNU, Norwegian University of Science and TechnologyDepartment of Clinical and Molecular Medicine, NTNU, Norwegian University of Science and TechnologyDepartment of Clinical and Molecular Medicine, NTNU, Norwegian University of Science and TechnologyDepartment of Public Health and Nursing, NTNU, Norwegian University of Science and TechnologyDepartment of Public Health and Nursing, NTNU, Norwegian University of Science and TechnologyAbstract 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.https://doi.org/10.1186/s12948-023-00186-3Atopic dermatitisBiomarkersChildrenPlasmaProbiotics
spellingShingle Dinastry Pramadita Zakiudin
Anne Dorthea Bjerkenes Rø
Vibeke Videm
Torbjørn Øien
Melanie Rae Simpson
Systemic inflammatory proteins in offspring following maternal probiotic supplementation for atopic dermatitis prevention
Clinical and Molecular Allergy
Atopic dermatitis
Biomarkers
Children
Plasma
Probiotics
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 Atopic dermatitis
Biomarkers
Children
Plasma
Probiotics
url https://doi.org/10.1186/s12948-023-00186-3
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