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Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts

A higher diversity of food items introduced in the first year of life has been inversely related to subsequent development of asthma. In the current analysis, we applied latent class analysis (LCA) to systematically assess feeding patterns and to relate them to asthma risk at school age. PASTURE (N=...

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Autores principales: Hose, Alexander J., Pagani, Giulia, Karvonen, Anne M., Kirjavainen, Pirkka V., Roduit, Caroline, Genuneit, Jon, Schmaußer-Hechfellner, Elisabeth, Depner, Martin, Frei, Remo, Lauener, Roger, Riedler, Josef, Schaub, Bianca, Fuchs, Oliver, von Mutius, Erika, Divaret-Chauveau, Amandine, Pekkanen, Juha, Ege, Markus J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8111016/
https://www.ncbi.nlm.nih.gov/pubmed/33986744
http://dx.doi.org/10.3389/fimmu.2021.651709
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author Hose, Alexander J.
Pagani, Giulia
Karvonen, Anne M.
Kirjavainen, Pirkka V.
Roduit, Caroline
Genuneit, Jon
Schmaußer-Hechfellner, Elisabeth
Depner, Martin
Frei, Remo
Lauener, Roger
Riedler, Josef
Schaub, Bianca
Fuchs, Oliver
von Mutius, Erika
Divaret-Chauveau, Amandine
Pekkanen, Juha
Ege, Markus J.
author_facet Hose, Alexander J.
Pagani, Giulia
Karvonen, Anne M.
Kirjavainen, Pirkka V.
Roduit, Caroline
Genuneit, Jon
Schmaußer-Hechfellner, Elisabeth
Depner, Martin
Frei, Remo
Lauener, Roger
Riedler, Josef
Schaub, Bianca
Fuchs, Oliver
von Mutius, Erika
Divaret-Chauveau, Amandine
Pekkanen, Juha
Ege, Markus J.
author_sort Hose, Alexander J.
collection PubMed
description A higher diversity of food items introduced in the first year of life has been inversely related to subsequent development of asthma. In the current analysis, we applied latent class analysis (LCA) to systematically assess feeding patterns and to relate them to asthma risk at school age. PASTURE (N=1133) and LUKAS2 (N=228) are prospective birth cohort studies designed to evaluate protective and risk factors for atopic diseases, including dietary patterns. Feeding practices were reported by parents in monthly diaries between the 4(th) and 12(th) month of life. For 17 common food items parents indicated frequency of feeding during the last 4 weeks in 4 categories. The resulting 153 ordinal variables were entered in a LCA. The intestinal microbiome was assessed at the age of 12 months by 16S rRNA sequencing. Data on feeding practice with at least one reported time point was available in 1042 of the 1133 recruited children. Best LCA model fit was achieved by the 4-class solution. One class showed an elevated risk of asthma at age 6 as compared to the other classes (adjusted odds ratio (aOR): 8.47, 95% CI 2.52–28.56, p = 0.001) and was characterized by daily meat consumption and rare consumption of milk and yoghurt. A refined LCA restricted to meat, milk, and yoghurt confirmed the asthma risk effect of a particular class in PASTURE and independently in LUKAS2, which we thus termed unbalanced meat consumption (UMC). The effect of UMC was particularly strong for non-atopic asthma and asthma irrespectively of early bronchitis (aOR: 17.0, 95% CI 5.2–56.1, p < 0.001). UMC fostered growth of iron scavenging bacteria such as Acinetobacter (aOR: 1.28, 95% CI 1.00-1.63, p = 0.048), which was also related to asthma (aOR: 1.55, 95% CI 1.18-2.03, p = 0.001). When reconstructing bacterial metabolic pathways from 16S rRNA sequencing data, biosynthesis of siderophore group nonribosomal peptides emerged as top hit (aOR: 1.58, 95% CI 1.13-2.19, p = 0.007). By a data-driven approach we found a pattern of overly meat consumption at the expense of other protein sources to confer risk of asthma. Microbiome analysis of fecal samples pointed towards overgrowth of iron-dependent bacteria and bacterial iron metabolism as a potential explanation.
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spelling pubmed-81110162021-05-12 Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts Hose, Alexander J. Pagani, Giulia Karvonen, Anne M. Kirjavainen, Pirkka V. Roduit, Caroline Genuneit, Jon Schmaußer-Hechfellner, Elisabeth Depner, Martin Frei, Remo Lauener, Roger Riedler, Josef Schaub, Bianca Fuchs, Oliver von Mutius, Erika Divaret-Chauveau, Amandine Pekkanen, Juha Ege, Markus J. Front Immunol Immunology A higher diversity of food items introduced in the first year of life has been inversely related to subsequent development of asthma. In the current analysis, we applied latent class analysis (LCA) to systematically assess feeding patterns and to relate them to asthma risk at school age. PASTURE (N=1133) and LUKAS2 (N=228) are prospective birth cohort studies designed to evaluate protective and risk factors for atopic diseases, including dietary patterns. Feeding practices were reported by parents in monthly diaries between the 4(th) and 12(th) month of life. For 17 common food items parents indicated frequency of feeding during the last 4 weeks in 4 categories. The resulting 153 ordinal variables were entered in a LCA. The intestinal microbiome was assessed at the age of 12 months by 16S rRNA sequencing. Data on feeding practice with at least one reported time point was available in 1042 of the 1133 recruited children. Best LCA model fit was achieved by the 4-class solution. One class showed an elevated risk of asthma at age 6 as compared to the other classes (adjusted odds ratio (aOR): 8.47, 95% CI 2.52–28.56, p = 0.001) and was characterized by daily meat consumption and rare consumption of milk and yoghurt. A refined LCA restricted to meat, milk, and yoghurt confirmed the asthma risk effect of a particular class in PASTURE and independently in LUKAS2, which we thus termed unbalanced meat consumption (UMC). The effect of UMC was particularly strong for non-atopic asthma and asthma irrespectively of early bronchitis (aOR: 17.0, 95% CI 5.2–56.1, p < 0.001). UMC fostered growth of iron scavenging bacteria such as Acinetobacter (aOR: 1.28, 95% CI 1.00-1.63, p = 0.048), which was also related to asthma (aOR: 1.55, 95% CI 1.18-2.03, p = 0.001). When reconstructing bacterial metabolic pathways from 16S rRNA sequencing data, biosynthesis of siderophore group nonribosomal peptides emerged as top hit (aOR: 1.58, 95% CI 1.13-2.19, p = 0.007). By a data-driven approach we found a pattern of overly meat consumption at the expense of other protein sources to confer risk of asthma. Microbiome analysis of fecal samples pointed towards overgrowth of iron-dependent bacteria and bacterial iron metabolism as a potential explanation. Frontiers Media S.A. 2021-04-27 /pmc/articles/PMC8111016/ /pubmed/33986744 http://dx.doi.org/10.3389/fimmu.2021.651709 Text en Copyright © 2021 Hose, Pagani, Karvonen, Kirjavainen, Roduit, Genuneit, Schmaußer-Hechfellner, Depner, Frei, Lauener, Riedler, Schaub, Fuchs, von Mutius, Divaret-Chauveau, Pekkanen and Ege https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Hose, Alexander J.
Pagani, Giulia
Karvonen, Anne M.
Kirjavainen, Pirkka V.
Roduit, Caroline
Genuneit, Jon
Schmaußer-Hechfellner, Elisabeth
Depner, Martin
Frei, Remo
Lauener, Roger
Riedler, Josef
Schaub, Bianca
Fuchs, Oliver
von Mutius, Erika
Divaret-Chauveau, Amandine
Pekkanen, Juha
Ege, Markus J.
Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title_full Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title_fullStr Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title_full_unstemmed Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title_short Excessive Unbalanced Meat Consumption in the First Year of Life Increases Asthma Risk in the PASTURE and LUKAS2 Birth Cohorts
title_sort excessive unbalanced meat consumption in the first year of life increases asthma risk in the pasture and lukas2 birth cohorts
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8111016/
https://www.ncbi.nlm.nih.gov/pubmed/33986744
http://dx.doi.org/10.3389/fimmu.2021.651709
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