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Oropharyngeal microbiota clusters in children with asthma/wheeze associate with allergy, blood transcriptomic immune pathways and exacerbations risk

Oropharyngeal microbiota clusters in children with asthma/wheeze associate with allergy, blood transcriptomic immune pathways and exacerbations risk
Oropharyngeal microbiota clusters in children with asthma/wheeze associate with allergy, blood transcriptomic immune pathways and exacerbations risk

Rationale: Children with preschool wheezing or school-age asthma are reported to have airway microbial imbalances. Objectives: To identify clusters in children with asthma or wheezing using oropharyngeal microbiota profiles. Methods: Oropharyngeal swabs from the U-BIOPRED (Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes) pediatric asthma or wheezing cohort were characterized using 16S ribosomal RNA gene sequencing, and unsupervised hierarchical clustering was performed on the Bray-Curtis b-diversity. Enrichment scores of the Molecular Signatures Database hallmark gene sets were computed from the blood transcriptome using gene set variation analysis. Children with severe asthma or severe wheezing were followed up for 12-18 months, with assessment of the frequency of exacerbations. Measurements and Main Results: Oropharyngeal samples from 241 children (age range, 1-17 years; 40% female) revealed four taxa-driven clusters dominated by Streptococcus, Veillonella, Rothia, and Haemophilus. The clusters showed significant differences in atopic dermatitis, grass pollen sensitization, FEV1% predicted after salbutamol, and annual asthma exacerbation frequency during follow-up. The Veillonella cluster was the most allergic and included the highest percentage of children with two or more exacerbations per year during follow-up. The oropharyngeal clusters were different in the enrichment scores of TGF-b (transforming growth factor-β) (highest in the Veillonella cluster) and Wnt/β-catenin signaling (highest in the Haemophilus cluster) transcriptomic pathways in blood (all q values ,0.05). Conclusions: Analysis of the oropharyngeal microbiota of children with asthma or wheezing identified four clusters with distinct clinical characteristics (phenotypes) that associate with risk for exacerbation and transcriptomic pathways involved in airway remodeling. This suggests that further exploration of the oropharyngeal microbiota may lead to novel pathophysiologic insights and potentially new treatment approaches.

asthma, microbiota, phenotype, precision medicine, wheezing
1073-449X
142-154
Abdel-Aziz, Mahmoud I.
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Thorsen, Jonathan
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Hashimoto, Simone
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Vijverberg, Susanne J.H.
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Neerincx, Anne H.
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Brinkman, Paul
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van Aalderen, Wim
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Stokholm, Jakob
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Rasmussen, Morten Arendt
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Roggenbuck-Wedemeyer, Michael
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Vissing, Nadja H.
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Mortensen, Martin Steen
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Brejnrod, Asker Daniel
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Fleming, Louise J.
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Murray, Clare S.
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Fowler, Stephen J.
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Frey, Urs
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Bush, Andrew
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Singer, Florian
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Hedlin, Gunilla
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Nordlund, Björn
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Shaw, Dominick E.
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Chung, Kian Fan
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Adcock, Ian M.
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Djukanovic, Ratko
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Auffray, Charles
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Bansal, Aruna T.
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Sousa, Ana R.
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Wagers, Scott S.
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Chawes, Bo Lund
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Sørensen, Søren Johannes
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Kraneveld, Aletta D.
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Sterk, Peter J.
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Roberts, Graham
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Bisgaard, Hans
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Maitland-van der Zee, Anke H.
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Abdel-Aziz, Mahmoud I.
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Thorsen, Jonathan
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Hashimoto, Simone
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Vijverberg, Susanne J.H.
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Neerincx, Anne H.
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Brinkman, Paul
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van Aalderen, Wim
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Stokholm, Jakob
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Rasmussen, Morten Arendt
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Vissing, Nadja H.
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Brejnrod, Asker Daniel
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Fleming, Louise J.
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Murray, Clare S.
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Fowler, Stephen J.
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Frey, Urs
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Bush, Andrew
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Singer, Florian
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Hedlin, Gunilla
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Nordlund, Björn
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Shaw, Dominick E.
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Chung, Kian Fan
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Adcock, Ian M.
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Djukanovic, Ratko
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Auffray, Charles
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Sousa, Ana R.
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Wagers, Scott S.
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Chawes, Bo Lund
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Sørensen, Søren Johannes
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Kraneveld, Aletta D.
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Roberts, Graham
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Bisgaard, Hans
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Maitland-van der Zee, Anke H.
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Abdel-Aziz, Mahmoud I., Thorsen, Jonathan, Hashimoto, Simone, Vijverberg, Susanne J.H., Neerincx, Anne H., Brinkman, Paul, van Aalderen, Wim, Stokholm, Jakob, Rasmussen, Morten Arendt, Roggenbuck-Wedemeyer, Michael, Vissing, Nadja H., Mortensen, Martin Steen, Brejnrod, Asker Daniel, Fleming, Louise J., Murray, Clare S., Fowler, Stephen J., Frey, Urs, Bush, Andrew, Singer, Florian, Hedlin, Gunilla, Nordlund, Björn, Shaw, Dominick E., Chung, Kian Fan, Adcock, Ian M., Djukanovic, Ratko, Auffray, Charles, Bansal, Aruna T., Sousa, Ana R., Wagers, Scott S., Chawes, Bo Lund, Bønnelykke, Klaus, Sørensen, Søren Johannes, Kraneveld, Aletta D., Sterk, Peter J., Roberts, Graham, Bisgaard, Hans and Maitland-van der Zee, Anke H. (2023) Oropharyngeal microbiota clusters in children with asthma/wheeze associate with allergy, blood transcriptomic immune pathways and exacerbations risk. American Journal of Respiratory and Critical Care Medicine, 208 (2), 142-154. (doi:10.1164/rccm.202211-2107OC).

Record type: Article

Abstract

Rationale: Children with preschool wheezing or school-age asthma are reported to have airway microbial imbalances. Objectives: To identify clusters in children with asthma or wheezing using oropharyngeal microbiota profiles. Methods: Oropharyngeal swabs from the U-BIOPRED (Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes) pediatric asthma or wheezing cohort were characterized using 16S ribosomal RNA gene sequencing, and unsupervised hierarchical clustering was performed on the Bray-Curtis b-diversity. Enrichment scores of the Molecular Signatures Database hallmark gene sets were computed from the blood transcriptome using gene set variation analysis. Children with severe asthma or severe wheezing were followed up for 12-18 months, with assessment of the frequency of exacerbations. Measurements and Main Results: Oropharyngeal samples from 241 children (age range, 1-17 years; 40% female) revealed four taxa-driven clusters dominated by Streptococcus, Veillonella, Rothia, and Haemophilus. The clusters showed significant differences in atopic dermatitis, grass pollen sensitization, FEV1% predicted after salbutamol, and annual asthma exacerbation frequency during follow-up. The Veillonella cluster was the most allergic and included the highest percentage of children with two or more exacerbations per year during follow-up. The oropharyngeal clusters were different in the enrichment scores of TGF-b (transforming growth factor-β) (highest in the Veillonella cluster) and Wnt/β-catenin signaling (highest in the Haemophilus cluster) transcriptomic pathways in blood (all q values ,0.05). Conclusions: Analysis of the oropharyngeal microbiota of children with asthma or wheezing identified four clusters with distinct clinical characteristics (phenotypes) that associate with risk for exacerbation and transcriptomic pathways involved in airway remodeling. This suggests that further exploration of the oropharyngeal microbiota may lead to novel pathophysiologic insights and potentially new treatment approaches.

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Manuscript_Blue-202211-2107OC.R2 - Accepted Manuscript
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Accepted/In Press date: 9 May 2023
e-pub ahead of print date: 10 May 2023
Published date: 15 July 2023
Additional Information: Funding Information: U-BIOPRED has received funding from the Innovative Medicines Initiative Joint Undertaking under FP7 Health grant agreement 115010, resources of which are composed of financial contributions from the European Union’s Seventh Framework Programme (FP7/2007-2013) and European Federation of Pharmaceutical Industries and Associations companies’ in-kind contributions (www.imi.europa.eu). M.I.A.-A. has received a full scholarship from the Ministry of Higher Education of the Arab Republic of Egypt (2015/2016). Publisher Copyright: Copyright © 2023 by the American Thoracic Society.
Keywords: asthma, microbiota, phenotype, precision medicine, wheezing

Identifiers

Local EPrints ID: 482034
URI: http://eprints.soton.ac.uk/id/eprint/482034
ISSN: 1073-449X
PURE UUID: 5449e667-4258-4e37-a9b3-6bc7b867ac90
ORCID for Ratko Djukanovic: ORCID iD orcid.org/0000-0001-6039-5612
ORCID for Graham Roberts: ORCID iD orcid.org/0000-0003-2252-1248

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Date deposited: 18 Sep 2023 16:31
Last modified: 09 May 2024 04:01

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Contributors

Author: Mahmoud I. Abdel-Aziz
Author: Jonathan Thorsen
Author: Simone Hashimoto
Author: Susanne J.H. Vijverberg
Author: Anne H. Neerincx
Author: Paul Brinkman
Author: Wim van Aalderen
Author: Jakob Stokholm
Author: Morten Arendt Rasmussen
Author: Michael Roggenbuck-Wedemeyer
Author: Nadja H. Vissing
Author: Martin Steen Mortensen
Author: Asker Daniel Brejnrod
Author: Louise J. Fleming
Author: Clare S. Murray
Author: Stephen J. Fowler
Author: Urs Frey
Author: Andrew Bush
Author: Florian Singer
Author: Gunilla Hedlin
Author: Björn Nordlund
Author: Dominick E. Shaw
Author: Kian Fan Chung
Author: Ian M. Adcock
Author: Charles Auffray
Author: Aruna T. Bansal
Author: Ana R. Sousa
Author: Scott S. Wagers
Author: Bo Lund Chawes
Author: Klaus Bønnelykke
Author: Søren Johannes Sørensen
Author: Aletta D. Kraneveld
Author: Peter J. Sterk
Author: Graham Roberts ORCID iD
Author: Hans Bisgaard
Author: Anke H. Maitland-van der Zee

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