Distinct nasal airway bacterial microbiotas differentially relate to exacerbation in pediatric patients with asthma

National Institute of Allergy and Infectious Diseases–sponsored Inner-City Asthma Consortium

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Background: In infants, distinct nasopharyngeal bacterial microbiotas differentially associate with the incidence and severity of acute respiratory tract infection and childhood asthma development. Objective: We hypothesized that distinct nasal airway microbiota structures also exist in children with asthma and relate to clinical outcomes. Methods: Nasal secretion samples (n = 3122) collected after randomization during the fall season from children with asthma (6-17 years, n = 413) enrolled in a trial of omalizumab (anti-IgE) underwent 16S rRNA profiling. Statistical analyses with exacerbation as the primary outcome and rhinovirus infection and respiratory illnesses as secondary outcomes were performed. Using A549 epithelial cells, we assessed nasal isolates of Moraxella, Staphylococcus, and Corynebacterium species for their capacity to induce epithelial damage and inflammatory responses. Results: Six nasal airway microbiota assemblages, each dominated by Moraxella, Staphylococcus, Corynebacterium, Streptococcus, Alloiococcus, or Haemophilus species, were observed. Moraxella and Staphylococcus species–dominated microbiotas were most frequently detected and exhibited temporal stability. Nasal microbiotas dominated by Moraxella species were associated with increased exacerbation risk and eosinophil activation. Staphylococcus or Corynebacterium species–dominated microbiotas were associated with reduced respiratory illness and exacerbation events, whereas Streptococcus species–dominated assemblages increased the risk of rhinovirus infection. Nasal microbiota composition remained relatively stable despite viral infection or exacerbation; only a few taxa belonging to the dominant genera exhibited relative abundance fluctuations during these events. In vitro, Moraxella catarrhalis induced significantly greater epithelial damage and inflammatory cytokine expression (IL-33 and IL-8) compared with other dominant nasal bacterial isolates tested. Conclusion: Distinct nasal airway microbiotas of children with asthma relate to the likelihood of exacerbation, rhinovirus infection, and respiratory illnesses during the fall season.

Original languageEnglish (US)
Pages (from-to)1187-1197
Number of pages11
JournalJournal of Allergy and Clinical Immunology
Volume144
Issue number5
DOIs
StatePublished - Nov 2019

Fingerprint

Microbiota
Nose
Asthma
Moraxella
Pediatrics
Staphylococcus
Rhinovirus
Corynebacterium
Respiratory Tract Infections
Streptococcus
Haemophilus
Moraxella (Branhamella) catarrhalis
Virus Diseases
Random Allocation
Interleukin-8
Eosinophils
Epithelial Cells
Cytokines
Incidence
Infection

Keywords

  • 16S rRNA
  • airway
  • asthma
  • exacerbation
  • Microbiota
  • Moraxella species
  • rhinovirus
  • Staphylococcus species

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Cite this

Distinct nasal airway bacterial microbiotas differentially relate to exacerbation in pediatric patients with asthma. / National Institute of Allergy and Infectious Diseases–sponsored Inner-City Asthma Consortium.

In: Journal of Allergy and Clinical Immunology, Vol. 144, No. 5, 11.2019, p. 1187-1197.

Research output: Contribution to journalArticle

National Institute of Allergy and Infectious Diseases–sponsored Inner-City Asthma Consortium 2019, 'Distinct nasal airway bacterial microbiotas differentially relate to exacerbation in pediatric patients with asthma', Journal of Allergy and Clinical Immunology, vol. 144, no. 5, pp. 1187-1197. https://doi.org/10.1016/j.jaci.2019.05.035
National Institute of Allergy and Infectious Diseases–sponsored Inner-City Asthma Consortium. / Distinct nasal airway bacterial microbiotas differentially relate to exacerbation in pediatric patients with asthma. In: Journal of Allergy and Clinical Immunology. 2019 ; Vol. 144, No. 5. pp. 1187-1197.
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abstract = "Background: In infants, distinct nasopharyngeal bacterial microbiotas differentially associate with the incidence and severity of acute respiratory tract infection and childhood asthma development. Objective: We hypothesized that distinct nasal airway microbiota structures also exist in children with asthma and relate to clinical outcomes. Methods: Nasal secretion samples (n = 3122) collected after randomization during the fall season from children with asthma (6-17 years, n = 413) enrolled in a trial of omalizumab (anti-IgE) underwent 16S rRNA profiling. Statistical analyses with exacerbation as the primary outcome and rhinovirus infection and respiratory illnesses as secondary outcomes were performed. Using A549 epithelial cells, we assessed nasal isolates of Moraxella, Staphylococcus, and Corynebacterium species for their capacity to induce epithelial damage and inflammatory responses. Results: Six nasal airway microbiota assemblages, each dominated by Moraxella, Staphylococcus, Corynebacterium, Streptococcus, Alloiococcus, or Haemophilus species, were observed. Moraxella and Staphylococcus species–dominated microbiotas were most frequently detected and exhibited temporal stability. Nasal microbiotas dominated by Moraxella species were associated with increased exacerbation risk and eosinophil activation. Staphylococcus or Corynebacterium species–dominated microbiotas were associated with reduced respiratory illness and exacerbation events, whereas Streptococcus species–dominated assemblages increased the risk of rhinovirus infection. Nasal microbiota composition remained relatively stable despite viral infection or exacerbation; only a few taxa belonging to the dominant genera exhibited relative abundance fluctuations during these events. In vitro, Moraxella catarrhalis induced significantly greater epithelial damage and inflammatory cytokine expression (IL-33 and IL-8) compared with other dominant nasal bacterial isolates tested. Conclusion: Distinct nasal airway microbiotas of children with asthma relate to the likelihood of exacerbation, rhinovirus infection, and respiratory illnesses during the fall season.",
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AU - National Institute of Allergy and Infectious Diseases–sponsored Inner-City Asthma Consortium

AU - McCauley, Kathryn

AU - Durack, Juliana

AU - Valladares, Ricardo

AU - Fadrosh, Douglas W.

AU - Lin, Din L.

AU - Calatroni, Agustin

AU - LeBeau, Petra K.

AU - Tran, Hoang T.

AU - Fujimura, Kei E.

AU - LaMere, Brandon

AU - Merana, Geil

AU - Lynch, Kole

AU - Cohen, Robyn T.

AU - Pongracic, Jacqueline

AU - Khurana Hershey, Gurjit K.

AU - Kercsmar, Carolyn M.

AU - Gill, Michelle

AU - Liu, Andrew H.

AU - Kim, Haejin

AU - Kattan, Meyer

AU - Teach, Stephen J.

AU - Togias, Alkis

AU - Boushey, Homer A.

AU - Gern, James E.

AU - Jackson, Daniel J.

AU - Lynch, Susan V.

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N2 - Background: In infants, distinct nasopharyngeal bacterial microbiotas differentially associate with the incidence and severity of acute respiratory tract infection and childhood asthma development. Objective: We hypothesized that distinct nasal airway microbiota structures also exist in children with asthma and relate to clinical outcomes. Methods: Nasal secretion samples (n = 3122) collected after randomization during the fall season from children with asthma (6-17 years, n = 413) enrolled in a trial of omalizumab (anti-IgE) underwent 16S rRNA profiling. Statistical analyses with exacerbation as the primary outcome and rhinovirus infection and respiratory illnesses as secondary outcomes were performed. Using A549 epithelial cells, we assessed nasal isolates of Moraxella, Staphylococcus, and Corynebacterium species for their capacity to induce epithelial damage and inflammatory responses. Results: Six nasal airway microbiota assemblages, each dominated by Moraxella, Staphylococcus, Corynebacterium, Streptococcus, Alloiococcus, or Haemophilus species, were observed. Moraxella and Staphylococcus species–dominated microbiotas were most frequently detected and exhibited temporal stability. Nasal microbiotas dominated by Moraxella species were associated with increased exacerbation risk and eosinophil activation. Staphylococcus or Corynebacterium species–dominated microbiotas were associated with reduced respiratory illness and exacerbation events, whereas Streptococcus species–dominated assemblages increased the risk of rhinovirus infection. Nasal microbiota composition remained relatively stable despite viral infection or exacerbation; only a few taxa belonging to the dominant genera exhibited relative abundance fluctuations during these events. In vitro, Moraxella catarrhalis induced significantly greater epithelial damage and inflammatory cytokine expression (IL-33 and IL-8) compared with other dominant nasal bacterial isolates tested. Conclusion: Distinct nasal airway microbiotas of children with asthma relate to the likelihood of exacerbation, rhinovirus infection, and respiratory illnesses during the fall season.

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KW - 16S rRNA

KW - airway

KW - asthma

KW - exacerbation

KW - Microbiota

KW - Moraxella species

KW - rhinovirus

KW - Staphylococcus species

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