The upper-airway microbiota and loss of asthma control among asthmatic children

Yanjiao Zhou; Daniel Jackson; Leonard B. Bacharier; David Mauger; Homer Boushey; Mario Castro; Juliana Durack; Yvonne Huang; Robert F. Lemanske; Gregory A. Storch; George M. Weinstock; Kristine Wylie; Ronina Covar; Anne M. Fitzpatrick; Wanda Phipatanakul; Rachel G. Robison; Avraham Beigelman

doi:10.1038/s41467-019-13698-x

The upper-airway microbiota and loss of asthma control among asthmatic children

Yanjiao Zhou, Daniel Jackson, Leonard B. Bacharier, David Mauger, Homer Boushey, Mario Castro, Juliana Durack, Yvonne Huang, Robert F. Lemanske, Gregory A. Storch, George M. Weinstock, Kristine Wylie, Ronina Covar, Anne M. Fitzpatrick, Wanda Phipatanakul, Rachel G. Robison, Avraham Beigelman^*

^*Corresponding author for this work

Pediatrics

Research output: Contribution to journal › Article › peer-review

79 Scopus citations

Abstract

The airway microbiome has an important role in asthma pathophysiology. However, little is known on the relationships between the airway microbiome of asthmatic children, loss of asthma control, and severe exacerbations. Here we report that the microbiota’s dynamic patterns and compositions are related to asthma exacerbations. We collected nasal blow samples (n = 319) longitudinally during a clinical trial at 2 time-points within one year: randomization when asthma is under control, and at time of early loss of asthma control (yellow zone (YZ)). We report that participants whose microbiota was dominated by the commensal Corynebacterium + Dolosigranulum cluster at RD experience the lowest rates of YZs (p = 0.005) and have longer time to develop at least 2 episodes of YZ (p = 0.03). The airway microbiota have changed from randomization to YZ. A switch from the Corynebacterium + Dolosigranulum cluster at randomization to the Moraxella- cluster at YZ poses the highest risk of severe asthma exacerbation (p = 0.04). Corynebacterium’s relative abundance at YZ is inversely associated with severe exacerbation (p = 0.002).

Original language	English (US)
Article number	5714
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-13698-x
State	Published - Dec 1 2019

ASJC Scopus subject areas

Physics and Astronomy(all)
Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)

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10.1038/s41467-019-13698-x

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Zhou, Y., Jackson, D., Bacharier, L. B., Mauger, D., Boushey, H., Castro, M., Durack, J., Huang, Y., Lemanske, R. F., Storch, G. A., Weinstock, G. M., Wylie, K., Covar, R., Fitzpatrick, A. M., Phipatanakul, W., Robison, R. G., & Beigelman, A. (2019). The upper-airway microbiota and loss of asthma control among asthmatic children. Nature communications, 10(1), Article 5714. https://doi.org/10.1038/s41467-019-13698-x

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title = "The upper-airway microbiota and loss of asthma control among asthmatic children",

abstract = "The airway microbiome has an important role in asthma pathophysiology. However, little is known on the relationships between the airway microbiome of asthmatic children, loss of asthma control, and severe exacerbations. Here we report that the microbiota{\textquoteright}s dynamic patterns and compositions are related to asthma exacerbations. We collected nasal blow samples (n = 319) longitudinally during a clinical trial at 2 time-points within one year: randomization when asthma is under control, and at time of early loss of asthma control (yellow zone (YZ)). We report that participants whose microbiota was dominated by the commensal Corynebacterium + Dolosigranulum cluster at RD experience the lowest rates of YZs (p = 0.005) and have longer time to develop at least 2 episodes of YZ (p = 0.03). The airway microbiota have changed from randomization to YZ. A switch from the Corynebacterium + Dolosigranulum cluster at randomization to the Moraxella- cluster at YZ poses the highest risk of severe asthma exacerbation (p = 0.04). Corynebacterium{\textquoteright}s relative abundance at YZ is inversely associated with severe exacerbation (p = 0.002).",

author = "Yanjiao Zhou and Daniel Jackson and Bacharier, {Leonard B.} and David Mauger and Homer Boushey and Mario Castro and Juliana Durack and Yvonne Huang and Lemanske, {Robert F.} and Storch, {Gregory A.} and Weinstock, {George M.} and Kristine Wylie and Ronina Covar and Fitzpatrick, {Anne M.} and Wanda Phipatanakul and Robison, {Rachel G.} and Avraham Beigelman",

note = "Funding Information: This study was conducted by the NHLBI AsthmaNet. Please refer to the Online supplement for a list of AsthmaNet investigators and coordinators. This project was supported by the National Heart, Lung, and Blood Institute. In addition, Y.Z. and G.M.W. were supported in part with funding from The Jackson Laboratory. Funding Information: D.J.: declares receiving research grants from NHLBI, NIAID, and GlaxoSmithKline. He has received personal fees for a DSMB from Pfizer, and for advisory boards from Novartis, GlaxoSmithKline, AstraZenena, Sanofi-Regeneron, Boehringer Ingelheim, and Vifor pharma. L.B.B.: declares receiving research grants from NIH, NHLBI, NIAID. He has received personal fees from GlaxoSmithKline, Genentech, Novartis, Merck, DBV technologies, Teva, Boehringer Ingelheim, Sanofi, Regeneron, AstraZenena, Vectura, Circassia. M.C.: pharmaceutical grant funding from AstraZenena, Chiesi, Novartis, GSK, Sanofi. Consultant for Genentech, Theravance, VIAA, Teva, Sanofi, Novartis. Speaker for AstraZenena, Genentech, GSK, Regeneron, Sanofi, Teva. Received royalties from Elsevier. Y.H.: research support from the NIH for microbiome research. R.F.L.: research support from the NIH for microbiome research. W.P.: Consultant for Novartis, Genentech, Regeneron, GSK, Teva, Sanofi. R.G.R.: research support from the NIH. The remaining authors declare no competing interests. Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = dec,

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doi = "10.1038/s41467-019-13698-x",

language = "English (US)",

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Zhou, Y, Jackson, D, Bacharier, LB, Mauger, D, Boushey, H, Castro, M, Durack, J, Huang, Y, Lemanske, RF, Storch, GA, Weinstock, GM, Wylie, K, Covar, R, Fitzpatrick, AM, Phipatanakul, W, Robison, RG & Beigelman, A 2019, 'The upper-airway microbiota and loss of asthma control among asthmatic children', Nature communications, vol. 10, no. 1, 5714. https://doi.org/10.1038/s41467-019-13698-x

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T1 - The upper-airway microbiota and loss of asthma control among asthmatic children

AU - Zhou, Yanjiao

AU - Jackson, Daniel

AU - Bacharier, Leonard B.

AU - Mauger, David

AU - Boushey, Homer

AU - Castro, Mario

AU - Durack, Juliana

AU - Huang, Yvonne

AU - Lemanske, Robert F.

AU - Storch, Gregory A.

AU - Weinstock, George M.

AU - Wylie, Kristine

AU - Covar, Ronina

AU - Fitzpatrick, Anne M.

AU - Phipatanakul, Wanda

AU - Robison, Rachel G.

AU - Beigelman, Avraham

N1 - Funding Information: This study was conducted by the NHLBI AsthmaNet. Please refer to the Online supplement for a list of AsthmaNet investigators and coordinators. This project was supported by the National Heart, Lung, and Blood Institute. In addition, Y.Z. and G.M.W. were supported in part with funding from The Jackson Laboratory. Funding Information: D.J.: declares receiving research grants from NHLBI, NIAID, and GlaxoSmithKline. He has received personal fees for a DSMB from Pfizer, and for advisory boards from Novartis, GlaxoSmithKline, AstraZenena, Sanofi-Regeneron, Boehringer Ingelheim, and Vifor pharma. L.B.B.: declares receiving research grants from NIH, NHLBI, NIAID. He has received personal fees from GlaxoSmithKline, Genentech, Novartis, Merck, DBV technologies, Teva, Boehringer Ingelheim, Sanofi, Regeneron, AstraZenena, Vectura, Circassia. M.C.: pharmaceutical grant funding from AstraZenena, Chiesi, Novartis, GSK, Sanofi. Consultant for Genentech, Theravance, VIAA, Teva, Sanofi, Novartis. Speaker for AstraZenena, Genentech, GSK, Regeneron, Sanofi, Teva. Received royalties from Elsevier. Y.H.: research support from the NIH for microbiome research. R.F.L.: research support from the NIH for microbiome research. W.P.: Consultant for Novartis, Genentech, Regeneron, GSK, Teva, Sanofi. R.G.R.: research support from the NIH. The remaining authors declare no competing interests. Publisher Copyright: © 2019, The Author(s).

PY - 2019/12/1

Y1 - 2019/12/1

N2 - The airway microbiome has an important role in asthma pathophysiology. However, little is known on the relationships between the airway microbiome of asthmatic children, loss of asthma control, and severe exacerbations. Here we report that the microbiota’s dynamic patterns and compositions are related to asthma exacerbations. We collected nasal blow samples (n = 319) longitudinally during a clinical trial at 2 time-points within one year: randomization when asthma is under control, and at time of early loss of asthma control (yellow zone (YZ)). We report that participants whose microbiota was dominated by the commensal Corynebacterium + Dolosigranulum cluster at RD experience the lowest rates of YZs (p = 0.005) and have longer time to develop at least 2 episodes of YZ (p = 0.03). The airway microbiota have changed from randomization to YZ. A switch from the Corynebacterium + Dolosigranulum cluster at randomization to the Moraxella- cluster at YZ poses the highest risk of severe asthma exacerbation (p = 0.04). Corynebacterium’s relative abundance at YZ is inversely associated with severe exacerbation (p = 0.002).

AB - The airway microbiome has an important role in asthma pathophysiology. However, little is known on the relationships between the airway microbiome of asthmatic children, loss of asthma control, and severe exacerbations. Here we report that the microbiota’s dynamic patterns and compositions are related to asthma exacerbations. We collected nasal blow samples (n = 319) longitudinally during a clinical trial at 2 time-points within one year: randomization when asthma is under control, and at time of early loss of asthma control (yellow zone (YZ)). We report that participants whose microbiota was dominated by the commensal Corynebacterium + Dolosigranulum cluster at RD experience the lowest rates of YZs (p = 0.005) and have longer time to develop at least 2 episodes of YZ (p = 0.03). The airway microbiota have changed from randomization to YZ. A switch from the Corynebacterium + Dolosigranulum cluster at randomization to the Moraxella- cluster at YZ poses the highest risk of severe asthma exacerbation (p = 0.04). Corynebacterium’s relative abundance at YZ is inversely associated with severe exacerbation (p = 0.002).

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JO - Nature communications

JF - Nature communications

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ER -

The upper-airway microbiota and loss of asthma control among asthmatic children

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