Early-life nasal microbiota dynamics relate to longitudinal respiratory phenotypes in urban children - 05/06/24

Doi : 10.1016/j.jaci.2023.12.032

Kathryn E. McCauley, MS ^a, Juliana Durack, PhD ^a, Kole V. Lynch, BS ^a, Douglas W. Fadrosh, MS ^a, Kei E. Fujimura, PhD ^a, Faith Vundla ^a, Mustafa Özçam, PhD ^a, Petra LeBeau, PhD ^b,^{^{∗
Petra LeBeau, PhD, is currently employed at PPD, part of Thermo Fisher Scientific, Wilmington, NC.}}, Agustin Caltroni, MA, MS ^b, Preston Burns, MS ^b, Hoang T. Tran, PhD ^b, Leonard B. Bacharier, MD ^c, Meyer Kattan, MD ^d, George T. O’Connor, MD ^e, Robert A. Wood, MD ^f, Alkis Togias, MD ^g, Homer A. Boushey, MD ^a, Daniel J. Jackson, MD ^h, James E. Gern, MD ^h,^⁎ , Susan V. Lynch, PhD ^a,^⁎
on behalf of the
National Institute of Allergy and Infectious Diseases–sponsored Childhood Asthma in Urban Settings Consortium
^a Benioff Center for Microbiome Medicine, Department of Medicine, University of California, San Francisco, Calif
^b Rho Federal Systems Division, Inc, Durham, NC
^c Division of Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine in St Louis, St Louis, Mo
^d Department of Pediatrics, Columbia University, New York, NY
^e Department of Medicine, Boston University School of Medicine, Boston, Mass
^f Departments of Pediatrics and Allergy and Immunology, Johns Hopkins University, Baltimore, Md
^g National Institute of Allergy and Infectious Diseases, Bethesda, Md
^h Department of Pediatrics, University of Wisconsin School of Medicine and Public Health, Madison, Wis

^∗Corresponding author: Susan V. Lynch, PhD, Division of Gastroenterology, Department of Medicine, University of California San Francisco, 513 Parnassus Ave, S357D, San Francisco, CA 94143.Division of GastroenterologyDepartment of MedicineUniversity of California San Francisco513 Parnassus AveS357DSan FranciscoCA94143^∗James E. Gern, MD, Division of Allergy, Immunology & Rheumatology, Department of Pediatrics, University of Wisconsin Madison, 600 Highland Ave, K4/936 CSC, Madison, WI 53792.Division of AllergyImmunology & RheumatologyDepartment of PediatricsUniversity of Wisconsin Madison600 Highland AveK4/936 CSCMadisonWI53792

Graphical abstract

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Abstract

Background

Five distinct respiratory phenotypes based on latent classes of longitudinal patterns of wheezing, allergic sensitization. and pulmonary function measured in urban children from ages from 0 to 7 years have previously been described.

Objective

Our aim was to determine whether distinct respiratory phenotypes are associated with early-life upper respiratory microbiota development and environmental microbial exposures.

Methods

Microbiota profiling was performed using 16S ribosomal RNA–based sequencing of nasal samples collected at age 12 months (n = 120) or age 36 months (n = 142) and paired house dust samples collected at 3 months (12-month, n = 73; 36-month, n = 90) from all 4 centers in the Urban Environment and Childhood Asthma (URECA) cohort.

Results

In these high-risk urban children, nasal microbiota increased in diversity between ages 12 and 36 months (ß = 2.04; P = .006). Age-related changes in microbiota evenness differed significantly by respiratory phenotypes (interaction P = .0007), increasing most in the transient wheeze group. At age 12 months, respiratory illness (R² = 0.055; P = .0001) and dominant bacterial genus (R² = 0.59; P = .0001) explained variance in nasal microbiota composition, and enrichment of Moraxella and Haemophilus members was associated with both transient and high-wheeze respiratory phenotypes. By age 36 months, nasal microbiota was significantly associated with respiratory phenotypes (R² = 0.019; P = .0376), and Moraxella-dominated microbiota was associated specifically with atopy-associated phenotypes. Analysis of paired house dust and nasal samples indicated that 12 month olds with low wheeze and atopy incidence exhibited the largest number of shared bacterial taxa with their environment.

Conclusion

Nasal microbiota development over the course of early childhood and composition at age 3 years are associated with longitudinal respiratory phenotypes. These data provide evidence supporting an early-life window of airway microbiota development that is influenced by environmental microbial exposures in infancy and associates with wheeze- and atopy-associated respiratory phenotypes through age 7 years.

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Key words : Asthma, atopy, airway microbiota, early childhood, respiratory phenotypes

Abbreviations used : GEE, HW-HA, HW-LA, LW-HA, LW-LA, OTU, QIIME, rRNA, TW-LA, URECA

Plan

Methods

Study population and outcomes

Sample collection and processing

Sample processing

Sequence data processing and quality control

Statistical analysis

Results

Nasal microbiota dynamics in childhood are related to respiratory phenotypes

Associations between nasal microbiota composition and environmental, clinical, and microbiologic factors at age 12 months

Associations between nasal microbiota composition and environmental, clinical, and microbiologic factors at age 36 months

Relationships between house dust and nasal microbiota at age 12 months differ by respiratory phenotype

Discussion

Conclusion

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Vol 153 - N° 6

P. 1563-1573 - juin 2024 Retour au numéro

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Early-life nasal microbiota dynamics relate to longitudinal respiratory phenotypes in urban children - 05/06/24

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Abstract

Background

Objective

Methods

Results

Conclusion

Plan

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